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Conversion of Cerrado savannas into exotic pastures: The relative importance of vegetation and food resources for dung beetle assemblages
Agriculture, Ecosystems and Environment 288 (2020) 106709
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Conversion of Cerrado savannas into exotic pastures: The relative importance of vegetation and food resources for dung beetle assemblages
T
Renan Macedoa, , Livia Dorneles Audinoa, Vanesca Korasakib, Julio Louzadac ⁎
a
Departamento de Entomologia, Universidade Federal de Lavras, Lavras, Minas Gerais, 37200-000 Brazil Departamento de Ciências Exatas e da Terra, Universidade do Estado de Minas Gerais, Frutal, 38200-000 Brazil c Departamento de Biologia, Universidade Federal de Lavras, Lavras, Minas Gerais, 37200-000, Brazil b
ARTICLE INFO
ABSTRACT
Keywords: Neotropical savannas Vegetation complexity Land use change Scarabaeinae Introduced pastures
Replacing native savannas with exotic pastures not only alters vegetation structure, but it also increases herbivorous cattle dung quantity consequently changing the food resource available for dung beetles. Therefore, this study aims at investigating the relative importance of vegetation structure regarding food resource types to determine dung beetle assemblage in Cerrado savannas and exotic pastures. We carried out a sampling of dung beetles in 30 areas of Cerrado sensu stricto and 30 in areas of exotic pastures across nine municipalities of Minas Gerais state, Brazil, by using pitfall traps baited with cattle dung and human feces. We also characterized these areas according to their herbaceous density, complexity (fractal dimension) and canopy cover. Our study demonstrates that the complete conversion of Cerrado sensu stricto into exotic pasture has a negative effect on dung beetle assemblages. The same dung types differed completely in dung beetle assemblages in native savannas and exotic pasture regarding richness, abundance, species composition and dominance patterns. These findings suggest that environmental filters in exotic pastures, as low cover canopy and herbaceous complexity simplification, probably restrict the establishment of species from Cerrado. We also found different dung beetle communities by comparing pitfall traps baited with cow dung and human feces within the same land use. Thus, alterations in food resources played a secondary role, but were also important. We suggest that increasing herbaceous complexity and canopy cover along with diversifying livestock in exotic pastures could potentially avoid the loss of dung beetles species and their associated ecosystem services.
1. Introduction Cerrado is an important tropical grassy phytogeographic domain that harbors a unique biodiversity and provides significant ecological services to humankind (Bond and Parr, 2010; Overbeck et al., 2015; Parr et al., 2014). Despite its importance, this ecosystem have been neglected regarding conservation public policies and are facing considerable threats due to human disturbance (Klink and Machado, 2005; Overbeck et al., 2015). The existence of large and relatively flat areas of native grasslands and savannas was decisive to determine human occupation in Cerrado, leading to the development of agriculture and animal husbandry (Klink and Moreira, 2002). This enhanced conversion of Cerrado into exotic pastures generating as a direct consequence of an increase in cattle herd (Horgan, 2001). Therefore, Cerrado is an important cattle ranching region, mainly based on extensive pastures (Klink and Machado, 2005). Despite being a subtle land use change (replacement of an open
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environment with another open environment), the substitution of Cerrado savannas with exotic pastures is considered one of the main causes of biodiversity loss and community disassembly (Almeida et al., 2011; Benito et al., 2004; Klink and Machado, 2005). To understand and obtain rapid and reliable responses on how land use change affects biodiversity, many studies have used bioindicators (Blaum et al., 2009; Verdú et al., 2011). Some insect groups, such as dung beetles (Coleoptera: Scarabaeinae), can be utilized for such purpose (Davis et al., 2012). Dung beetles are considered one of the best cost-effective bioindicator groups for being sensitive to ecosystem changes, broadly distributed, with well-known taxonomy and ecology, in addition to easy, low-cost sampling. For these reasons, they have been widely used to assess the anthropogenic impacts on tropical ecosystems (Gardner et al., 2008; Nichols and Gardner, 2011). Native grasslands and savannas of Cerrado have a great potential to serve as a species source for introduced pastures (Sano et al., 2000), since they are open environments that occupy almost 20% of the
Correspondence author at: Departamento de Entomologia, Universidade Federal de Lavras, 37200-000, Lavras, Minas Gerais, Brazil. E-mail address: [email protected] (R. Macedo).
https://doi.org/10.1016/j.agee.2019.106709 Received 22 June 2018; Received in revised form 1 October 2019; Accepted 5 October 2019 0167-8809/ Published by Elsevier B.V.
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Brazilian territory located between two huge tropical forests: Atlantic Forest and Amazon (Beuchle et al., 2015; Myers et al., 2000). However, dung beetle diversity is extremely low in exotic pastures in relation to native savannas, and species composition differs completely between these two land uses (Almeida et al., 2011; Davis et al., 2014; Horgan, 2008). Nevertheless, there are no studies investigating whether these effects are a result of changes in vegetation structure or food resource. The substitution of native savannas with exotic pastures causes modification in vegetation complexity. Cerrado savannas represent an herbaceous ecosystem that show some sparse shrubs and a few small trees, and exotic pastures are mainly composed by one species of grass (Oliveira and Marquis, 2002). This substitution can also change the quality and quantity of food resources, mainly as a consequence of alterations in fauna and flora in exotic pastures. Dung beetles are mostly coprophagous (Halffter and Matthews, 1966) and an important food resource for these insects in native savannas is the presence of omnivorous mammal dung (Davis et al., 2012). Besides omnivorous mammals, it is also possible to find carnivores and a few herbivores, since Cerrado presents a highly diverse mammalian fauna (around 194 species recorded) (Marinho-Filho et al., 2002). Mammalian assemblages are affected by the conversion of native savannas into exotic pastures, which generates a decrease in native mammal dung (Cáceres et al., 2010). For this reason, exotic pastures mainly display a high amount of herbivorous cattle dung (˜22 kg dung fresh per animal/day) (Fincher, 1981).Cattle dung is different from the dung produced by native herbivores from Cerrado (Rahagalala et al., 2009), since cattle dung pads are larger and more humid than native herbivores dung (Dickinson et al., 1981). Several studies have already confirmed that dung beetles present high specificity regarding dung type (e.g. Louzada and Silva, 2009; Tshikae et al., 2008; Martín-Piera and Lobo, 1996). Thus, the input of cattle dung can also be an important driver of dung beetle assemblage change after the introduction of exotic pastures in Cerrado. This study aims at investigating the importance of the herbaceous density and complexity, canopy cover and input cattle dung, an exotic food source to dung beetle assemblage in the introduced pastures. We tested the following hypothesis: changes in dung beetle assemblage are driven by the reduction of canopy cover, low herbaceous density and complexity with lower effect of dung types changes. In this context, if dung beetle assemblages are being influenced by changes in vegetation structure, then the assemblages will be different between native savanna and exotic pasture even when sampled using the same dung types. However, if dung beetles are influenced only by changes in food resources, then dung beetle assemblages sampled with omnivorous dung baits and herbivorous dung baits will be similar between Cerrado and exotic pastures.
and Marquis, 2002). However, since the 1980′s native grasslands and savannas of Cerrado are being replaced with exotic pastures for livestock production. These introduced pastures are generally monocultures of one common species of an exotic grass, such as Urochloa spp. (Syn. Brachiaria spp.). Currently, exotic pastures of Urochloa spp. cover wide areas of the Cerrado biome, generally becoming degraded-exotic pastures due to inadequate management practices (Cavalcanti and Joly, 2002). Over the past years, more than half of the original cover of Cerrado has been taken for livestock (Klink and Machado, 2005; Marris, 2005). Thus, Cerrado is an important cattle ranching region and its bovine herd has been growing substantially since the 1980s and is considered one of the most important regions for the beef production (Marris, 2005). Cerrado sensu stricto covers approximately 70% of the Cerrado biome and is an herbaceous ecosystem dominated by grasses and containing some sparse trees of 3–8 m tall and shrubs. These trees and shrubs provides nearly ˜30% of crown cover for this ecosystem (Oliveira-Filho and Ratter, 2002). Native savannas study sites had not been used to raise cattle mainly because the native vegetation is not adequate for grazing activities (McManus et al., 2011). Compared to African savannas, Cerrado savannas show very few large mammals and is essentially constituted of small and medium-sized animals, such as bats, rodents, primates, carnivores and didelphimorph marsupials. The largest herbivores recorded in areas of native Cerrado are the South American tapir, Tapirus terrestris, and species of small deers (Cervidae), from the genus Mazama, Blastocerus and Ozotocerus, occurring in small densities (Marinho-Filho et al., 2002). 2.2. Dung beetle survey We conducted our sampling in two types of land use systems: Cerrado sensu stricto (native savanna) and exotic pasture (Urochloa spp.). All exotic pastures sampled were similar regarding its vegetation and management characteristics. These areas were extensive pastures, composed predominantly by Urochloa spp. and used for cattle ranching to produce beef and/or milk. Thus, differently from native savannas, all exotic pastures presented cattle. We sampled dung beetles in areas of Cerrado sensu stricto and exotic pasture in ten landscape windows (at least 20 km apart). The distribution of these ten landscape windows encompasses nine municipalities (Fig. 1). For each landscape window, we sampled three sites of each land use type representing a total of 30 areas of Cerrado and 30 areas of exotic pasture. Each sampling site received five sampling points, 50 m apart, placed along a linear transect. The sampling points were constituted of two pitfall traps (3 m apart), one baited with human feces (25 g of human feces) and another with cattle dung (500 g of cattle herbivorous dung). We used human feces as a proxy for native’s omnivorous mammalian dung. Several studies have already showed that human feces can attract a greater number of dung beetle’s species, as well as that these species are generally different from the ones sampled in herbivorous dung (Puker et al., 2013; Whipple and Hoback, 2012). Our sampling effort amounted 150 sampling points per land use type, numbering 600 pitfall traps across ten landscape windows. We carried out the sampling during the rainy season, from January to February 2012, the most suitable period to sample dung beetle assemblage (Medina and Paixão-Lopes, 2014) and used pitfall traps in the field for 48 h. The inside of each trap was added with a solution containing water, salt and detergent. The trap baited with human feces received a plastic cup containing the bait, while the trap with cow dung received a nylon sachet containing cow dung suspended in a stake in the center of the trap. Sampled beetles were sent to the Universidade Federal de Lavras (UFLA) for identification at species level; upon uncertainty, a morphospecies number was given. Vouchers were deposited in Laboratório de Ecologia e Conservação de Invertebrados (Laboratory of Ecology and Conservation of Invertebrates) UFLA and in the
2. Methods 2.1. Study area We carried out this study in areas of native Brazilian savannas (Cerrado sensu stricto) and exotic pastures located in the municipalities of Montes Claros, Pitangui, Martinho Campos, Pompéu, Felixlândia, Curvelo, Pirapora, Buritizeiro, and Claro das Poções, in the Northeast Minas Gerais State, Brazil (Fig. 1, Appendix A – Table A1 in Supplementary material). The average annual temperature varies from 18 °C to 28 °C, and rainfall, from 800 mm to 2000 mm, with a very strong dry season during the autumn and winter (April–September). The regional biome climate is tropical savanna Aw (Köppen) (Oliveira and Marquis, 2002). The studied region was originally covered with typical phyto physiognomies of the Cerrado biome, which is composed predominantly by open native vegetation, such as grasslands (“campo limpo”) or savannas (“Cerrado sensu strictu”), and dense woodland (“Cerradão”) (Oliveira 2
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Fig. 1. Ten sampled landscape windows and its location in Minas Gerais state, Brazil. The grid represents coordinates in UTM (Universal Transverse Mercator) zone 23S – SAD69. The figure is composed by three minor figures. There is localization of Minas Gerais state in the Brazil, a localization of sampled points in Minas Gerais state and the last with a close in sample points, that represent a municipalities of Montes Claros, Pitangui, Martinho Campos, Pompéu, Felixlândia, Curvelo, Pirapora, Buritizeiro, and Claro das Poções, in the Northeast Minas Gerais State, Brazil.
Entomology Section of the Zoological Collection, Federal University of Mato Grosso (UFMT).
the herbaceous vegetation through the percentage of black pixels and white pixels from a dichromatic picture. For these two measures, we used the average of four pictures per sample point. We also took five photographs of the canopy, one at each sampling point (five per site) using a digital camera equipped with hemispherical lens (8 mm). The photographs were taken at 1 m above the ground and oriented towards the sky to be able to characterize canopy openness and analyzed using a Gap Light Analyser software package version 2 (Frazer et al., 1999).
2.3. Vegetation structure We characterized the vegetation of the sampling sites according to the following three variables: (1) herbaceous vegetation density, (2) herbaceous complexity, measured as the fractal dimension of vegetation, and (3) canopy openness. Measurement of these variables enables to assess habitat heterogeneity/homogeneity from open ecosystems (Gries et al., 2011; Marsden et al., 2002; Silva et al., 2010). It also reflects how the conversion of Cerrado sensu stricto into exotic pastures can alter natural environment original characteristics. Herbaceous vegetation and canopy openness can influence atmospheric and soil surface luminosity, humidity and temperature (Edmondson et al., 2016; Jennings et al., 1999; Özkan and Gökbulak, 2017). These abiotic characteristics affect dung beetle’s survival, reproduction, nidification, development, as well as food availability and attractiveness (Hanski and Cambeforti, 1991). Additionally, herbaceous density and complexity can hinder dung beetle’s flight displacement (Gries et al., 2011; Morse et al., 1985). To record herbaceous vegetation density and fractal dimension, we used a method proposed by Nobis (2005). Between two traps of each sampling point, a black panel of 1 m2 was placed vertically 10 cm above the ground. We took four photographs at a three-meter distance from the panel, one per cardinal direction using a digital camera. We analyzed the pictures by using the software Sidelook 1.1.01 (Nobis, 2005), which allows to calculate vegetation density and fractal dimension of
2.4. Statistical analysis We used generalized linear mixed models (GLMMs) to examine differences in mean species richness and abundance of dung beetles sampled with cattle dung and human feces between the land use types (native savannas and exotic pastures). Sampling site was considered the sample unit and land use type per dung type were considered explanatory variables and richness and abundance the response variables. In the models, we used landscape windows as a random factor and Poisson errors corrected for overdispersion (Quasi-Poisson) (O’Hara and Kotze, 2010). To correct overdispersion we fitted GLMM models with multivariate normal random effects by using Penalized QuasiLikelihood. All GLMMs were submitted to residual analysis to evaluate the adequacy of residual distribution. This analysis was performed in the R statistical programming language using ‘MASS’ package, function “glmmPQL” (Ripley and Bates, 2018). Subsequently, a Tukey contrast analysis using “multicomp” package (Hothorn et al., 2017) was performed to verify which categories were distinct regarding the response 3
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variables. We also compared dung beetle’s total species richness between native savannas and exotic pastures sampled with cattle dung and human feces using individual based interpolation and extrapolation curves within 95% confidence intervals (Colwell et al., 2012). We built interpolation and extrapolation curves since the number of individuals varied between land uses and baits, which can influence total species richness (Colwell et al., 2012). This analysis was performed using INEXT online implemented by R software (Chao et al., 2016). To observe dominance patterns in dung beetle assemblages sampled with pitfall traps baited with human feces and cattle dung in native savannas and exotic pastures, we constructed abundance distribution curves using the transformation log + 1. To graphically express changes in dung beetle species composition associated with each land use and dung types, we performed a nonmetric dimensional analysis (NMDS) over a Bray–Curtis similarity matrix with standardized and square-root transformed data, considering the sampling site as sample unit. To investigate whether dung beetle assemblage composition is different between land use and dung types, we applied a multivariate analysis of variance with permutations (PERMANOVA). In the model, the landscape windows was considered a random factor and land use and dung type and the interaction between land use types and baits as a fixed factor. We also identified the major species driving species composition patterns of dung beetle assemblages using similarity percentage analysis (SIMPER). SIMPER calculates the average dissimilarity among all pairs of samples by assessing the relative dissimilarity contributed per species to determine species composition differences among land use types and baits. NMDS, PERMANOVA and SIMPER analyses were performed on the Primer v.6 software with PERMANOVA+ (Anderson et al., 2008). We performed a variance partitioning analysis to evaluate the relative importance of vegetation structure and food resources to explain dung beetle species richness, abundance and composition inside each land use (Wezel et al., 2009) considering the sampling point as sample unit. This analysis was based on partial redundancy analysis for multivariate response data (e.g., species composition) as well as on partial multiple linear regression for univariate response data (e.g., species richness and abundance). Variance partitioning is ideal to decompose the variation of the response variables into independent and joint effects of suites of predictor variables (Borcard et al., 1992; Wezel et al., 2009). Data on herbaceous vegetation density, fractal dimension of the herbaceous vegetation and canopy openness represented the vegetation group of predictor variables and the dung type represented the food resources group of predictor variables. Prior to variance partitioning analysis, species trait composition was Hellinger-transformed. The variance partitioning analysis was performed using R software, vegan package, function varpart (Oksanen et al., 2014). Subsequently, we evaluated the individual contribution and the relationship of each vegetation variable (herbaceous vegetation density, fractal dimension of the herbaceous vegetation and canopy openness) with species richness, abundance and species composition using linear regression for univariate data and redundancy analysis for multivariate data. We performed this analysis separately for native savanna and exotic pastures data using vegan package in R environment (Oksanen et al., 2014). To verify how Cerrado sensu stricto and exotic pastures differ according to vegetation variables we performed generalized linear models (GLMs). In the models, land use systems categories was considered the predictor variable and each vegetation variable the response variable. We built the models by applying Gaussian distribution for herbaceous vegetation density and complexity and Quasi Binomial distribution for canopy openness in R software package (R Core Team, 2018), followed by residual analysis to check for the error distribution and model adequacy (Appendix B, Figure B1 in Supplementary material).
3. Results Almost half of all sampled species (45–46% species) were exclusive to native savannas. Of these native savanna’s exclusive species, five were collected only in pitfall traps baited with cattle dung, 21 only in pitfall traps baited using human feces and 20 in both dung types. In contrast, only seven species were exclusive to exotic pastures (6.9% of all sampled species). Of these seven species, one was collected only in pitfall traps baited using cattle dung and six only in pitfall traps baited with human feces. Forty-eight species (47% of all sampled species) were sampled in both land use systems. Of these species, one was sampled only using cattle dung and ten only with human feces. The complete information on the individuals collected according to the land use and type dung is in the supplementary material (Appendix C, Table C1 in Supplementary material). Richness was higher in native savannas in relation to exotic pastures; when considering both, dung beetles sampled with human feces and cattle dung. The highest mean values of species richness were obtained in traps baited using human feces in native savannas. Exotic pastures presented the lowest values of species richness. We obtained the lowest abundance values in exotic pastures in traps baited with human feces (Appendix D, Table D1; Fig. 2 in Supplementary material). Up controlling the differences in abundance among land use systems and baits through interpolation and extrapolation curves, total species richness was higher in traps baited using human feces in native savannas and lower in exotic pastures in cattle dung. Dung beetle’s total species richness presented intermediate values and was similar between traps baited using cattle dung in native savannas and baited using human feces in exotic pastures (Fig. 3).
Fig. 2. Mean species richness and abundance of dung beetles sampled with human feces and cattle dung in Brazilian native savannas and exotic pastures. Different letters above bars indicate statistically significant differences (P < 0.05). Error bars represent ± standard errors.
4
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Table 1 Results of the permutational analysis of variance (PERMANOVA) indicating whether the categories of landscape windows, land use systems (native savanna and exotic pasture), baits (cattle dung and human feces) and the interaction between land use systems and baits are different according to species composition. Pseudo-F and p-value are presented for the main test and test statistic (t) and p-values for each pair-wise comparison. * p-values < 0.05. Source of variation Landscape window Land use system Baits Land use systems:baits Post hoc comparison Land use systems: baits Pasture/cattle dung vs. pasture/human feces Pasture/cattle dung vs. savanna/cattle dung Pasture/cattle dung vs. savanna/human feces Pasture/human feces vs. savanna/cattle dung Pasture/human feces vs. savanna/human feces Savanna/cattle dung vs. savanna/human feces
Fig. 3. Individual-based interpolation and extrapolation curves from four samples of dung beetles from Minas Gerais, Brasil: 1) native savannas sampled with pitfall traps baited with cattle dung; 2) native savannas sampled with pitfall traps baited with human feces; 3) exotic pastures sampled with pitfall traps baited with cattle dung, and; 4) exotic pastures sampled with pitfall traps baited with human feces. Dotted lines represent 95% confidence intervals of each curve, continuous lines the interpolation curves and dashed lines the extrapolation curves.
Pseudo-F
p
11.09 4.96 10.47 6.43
0.0001* 0.0001* 0.0001* 0.0001*
t 3.03 2.33 3.11 2.12 2.05 2.55
p 0.0001* 0.0005* 0.0001* 0.0001* 0.0002* 0.0001*
Fig. 5. Distribution patterns (NMDS) of the sampling points comparing assemblage composition (Bray-Curtis similarity) between feces humans and cattle dung, in Brazilian savannas and exotic pastures, showing centroids (larger circles and squares) and dispersion of points to centroid (lines). Dark grey circles represent exotic pastures/cattle dung, white circles represent exotic pastures/human feces, light grey squares represent native savannas/cattle dung and black squares native savannas/human feces.
Fig. 4. Rank abundance distribution of dung beetles species sampled with pitfall traps baited with cattle dung and human feces in native savannas and exotic pastures. Light grey squares represent native savannas/cattle dung and black squares native savannas/human feces, dark grey circles represent exotic pastures/cattle dung, white circles represent exotic pastures/human feces. “a” = Ateuchus aff. pauperatus; “b” = Ontherus appendiculatus; “c” = Dichotomius bos; “d” = Agamopus viridis; “e” = Canthon fortemaginatus; “f” = Uroxys sp. C; “g” = Canthon simulans; “h” = Digithontophagus gazella; “i” = Onthophagus hirculus; “j” = Trichillum externepunctum; “l” = Canthon aff. podagricus.
variation in species richness, abundance and species composition of native savannas, respectively (Fig. 6A). Both vegetation and food resources determined species richness and composition. However, for species richness, vegetation structure was more important than food resources. Regarding abundance, all total variation explained was attributed to vegetation alone, being the only significant group of predictor variables. In the case of exotic pastures, variance partitioning models explained 11%, 10% and 15% of the variation in species richness, abundance and species composition, respectively (Fig. 6B). In all cases, both groups of predictor variables were considered significant. However, only for species composition, food resources proved more important than vegetation. In native savannas, canopy openness and herbaceous complexity proved the most important vegetation variables to determine species richness, abundance and species composition. Species composition was also influenced by herbaceous density in these native environments. In contrast, only herbaceous complexity was important to establish species richness and composition in exotic pastures; in addition, abundance was only influenced by herbaceous density (Table 2).
Abundance distribution curves of exotic pastures are steeper regarding native savannas, which presented shallower slopes (Appendix D, Table D1; Fig. 2 in Supplementary material). Dominance patterns was also different in the same land use type between cattle dung and human feces, where evenness of assemblages sampled using cattle dung are lower in regarding the assemblages sampled using human feces. Additionally, exotic species Digithontophagus gazella was one of the most dominant species only in cattle dung of exotic pastures (Fig. 4). Species composition was different among dung beetle assemblage sampled using cattle dung in native savannas human feces in native savannas, cattle dung in exotic pastures, and human feces in exotic pastures (Table 1; Fig. 5). Appendix E, Table E1 “in Supplementary material” illustrates the main species responsible for the differences in species composition among land use and dung. Variance partitioning models explained 24%, 15% and 10% of the 5
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The same dung types collected completely different dung beetle assemblages in native savannas and exotic pastures. Mean species richness and abundance were always lower in exotic pastures regardless of the dung used. Furthermore, dominance patterns and species composition of beetles that feed on omnivorous and herbivorous dung are different between native savannas and exotic pastures. These findings suggest that, besides changes in food resources, other ecological filters found in exotic pastures restrict the colonization, establishment and population increase for several species from Cerrado sensu stricto. Our results highlight that one of these ecological filters is vegetation structure. Variance partitioning models showed that dung beetles in native savannas are being mainly driven by vegetation characteristics. It is well known that vegetation structure can influence dung beetles even in open environment systems (Almeida et al., 2011; Davis et al., 2010; Gries et al., 2011; Martello et al., 2016). In native savannas, herbaceous complexity and canopy cover were the most important variables to explain dung beetle communities. In our study, the areas of Cerrado sensu stricto presented a higher degree of canopy cover and herbaceous complexity when compared to exotic pastures (Appendix B in Supplementary material). A simplification of the vegetation structure reduces the vegetation complexity modifying microhabitat conditions, exposing arthropods to higher levels of light, wind, temperature, lower humidity and predators (Gunnarsson, 1990; Van Klink et al., 2014). Still, vegetation complexity can probably increase the number of available niches (Klopfer and MacArthur, 1960), enabling the existence of a larger amount of species (Nittérus and Gunnarsson, 2006; Silva et al., 2010). Thus, more complex and closed native savannas generally present higher species richness (Blaum et al., 2009; Tews et al., 2004). Herbaceous complexity was also important for exotic pastures, where higher levels of complexity lead to a higher number of species and individuals. From the vegetation variables that we measured, canopy cover was the only unimportant to explain species richness, abundance, and composition in exotic pastures. This occurred because most of the pastures from our study did not present any degree of canopy cover. Herbaceous density was the least important variable for both native savannas and exotic pastures, probably because these systems did not differ in relation to this variable (Appendix B in Supplementary material). We suggest that the increase of the herbaceous complexity and canopy cover in exotic pastures can be an important insight to avoid the loss of dung beetles species. Increasing vegetation structure complexity could therefore avert biodiversity and ecosystem services loss in exotic pastures. Despite their importance, the vegetation variables explained only a small fraction of dung beetles species richness, abundance as well as composition in native savannas and exotic pastures. This high unexplained fraction of the variance may reflect the effects of unmeasured environmental variables in our study area and can decrease with the inclusion of other variables, such as soil type (Bottinelli et al., 2015; Halffter and Matthews, 1966; Manning et al., 2016), soil compaction (Herrick and Lal, 1995; Navarrete and Halffter, 2008) and landscape
Fig. 6. Variance partitioning models showing individual fractions of variation explained by vegetation and food resources (baits). The first panel shows results for native savannas when considering species richness, abundance and species composition and the second panel for exotic pastures. Vegetation (white) and food resource (black) fractions indicate unique contributions towards the overall amount of variance explained, and the striped fraction indicates the redundant portion co-explained by each. * = p values < 0.05.
4. Discussion Our study indicates that changes in dung beetle assemblage due to the conversion of Cerrado sensu stricto into exotic pastures are mainly driven by modifications in vegetation structure. Alterations in food resources are secondary at determining dung beetle assemblage modifications; however, it is still important to determine richness, abundance species composition in these two land uses.
Table 2 Amount of variation in species richness, abundance and assemblage composition explained by the vegetation individual predictor variables (canopy openness, herbaceous vegetation density, fractal dimension of the herbaceous vegetation) in native savannas and exotic pastures. R-squared were calculated using linear regression for species richness and abundance, and using redundancy analysis for assemblage composition (P-values were generated using a permutation procedure). Richness System
Variable
Native savanna
Canopy openness Fractal Density Canopy openness Fractal Density
Exotic pasture
R
2
0.04 0.06 0.007 0.00006 0.07 0.009
Abundance 2
P
R
0.001*** 0.001*** 0.13 0.9 0.001*** 0.09
0.08 0.03 0.003 0.00005 0.00001 0.07
6
Composition 2
P
R
0.001*** 0.005** 0.3 0.9 0.9 0.007**
0.02 0.02 0.009 0.005 0.03 0.003
P 0.001*** 0.001*** 0.002** 0.2 0.001*** 0.5
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context (Roslin and Koivunen, 2001; Tabarelli and Vaz-de-mello, 2015; Verdú et al., 2011). Substitution of native savannas with exotic pastures and the consequent changes in vegetation facilitate the colonization and dominance of species that are habitat generalists in exotic pastures (see Horgan, 2007). For example, most of exotic pastures dominant species are highly found in modified environments: Dichotomius bos, Trichillum externepunctatum, Onthophagus hirculus and Digithontophagus gazella (Tissiani et al., 2017). Digitonthophagus gazella (Génier and Davis, 2017) is an African dung beetle species, introduced in Brazil for the first time in 1989. Nowadays, it is widely distributed throughout Brazil (Génier and Davis, 2017; Matavelli and Louzada, 2008). In our study, this exotic species was one of the most abundant in introduced pastures, being mainly sampled with cattle dung. In native savannas, it was only found six individuals. This result indicates that the substitution of highly diverse Cerrado native savannas to monocultures of the nonindigenous grass Urochloa sp. and the introduction of a non-native mammal (cattle) can facilitate the invasion and dominance of an exotic dung beetle species (Simberloff and Von Holle, 1999). Digitonthophagus gazella is an extremely good competitor and used to feed on feces of large mammals (Génier and Davis, 2017). Probably the high diversity of dung beetle species found in native savannas can represent a resistance to the invasion of this exotic species (Elton, 1958). We also found different dung beetle communities when we compared pitfall traps baited with cow dung and human feces within the same land use, corroborating that dung type can have an influence in dung beetle assembling. Several dung beetles species are specialists according to dung type (Martín-Piera and Lobo, 1996; Tshikae et al., 2008; Whipple and Hoback, 2012). This trophic preference exists because dung types are different according to its physical-chemical attributes (Dormont et al., 2010; Tshikae et al., 2008). Different dung types vary regarding the chemical odors released by them to water content, nutritional qualities, fiber and dropping size (Halffter and Matthews, 1966; Tshikae et al., 2008). Still, dung quality and attractiveness are inherent to the physiology, digestion, and bacterial microflora present in the mammal, and are not a result of food type alone (Whipple and Hoback, 2012). For this reason, changes in dung type, such as nitrogen-rich omnivore droppings for pads of ruminant herbivores, and a decrease in the quantity of a preferred dung can cause species loss, reduce population size and modify species composition (Tshikae et al., 2013). Differently from native savannas, food resources were more important than vegetation structure at determining dung beetle assemblages in exotic pastures. Exotic pastures present a more simplified vegetation structure, which probably makes food resources more important to drive species distribution (Horgan, 2008). In this context, the input of cattle dung is an important factor to determine which species are going to be found in exotic pastures (Louzada and Silva, 2009). Domestic livestock increase the abundance of some species due to their ability to manipulate dung of domestic mammals that were not present before (Horgan, 2008). Probably, vegetation is not as important as food resources, because the species found in exotic pastures are generally habitat generalists (Horgan, 2008). Species richness and abundance captured in pitfalls baited with cow dung were higher in native savannas against exotic pastures, which emphasizes that dung beetles of native savannas can be attracted to herbivorous dung. Cattle was introduced in Brazil 500 years ago, enabling some native dung beetles to utilize cow dung as food resource (Louzada and Silva, 2009). According to Louzada and Silva (2009), there are many species of dung beetles from several Brazilian regions active in exotic pastures feeding on cattle dung. However, our results show that these beetles are mostly different from the ones captured with cattle dung in native savannas. Additionally, we found a small number of species that feed on omnivorous dung in exotic pastures, which is probably being driven by the small number of individuals
found in this land use with human feces. This is reflected by the interpolation/extrapolation curves (Fig. 3), since when abundance of land system/baits was put at the same level, total species richness of exotic pastures/omnivorous dung was the same in relation to native savannas/ cattle dung. These results suggests that the lack of omnivorous dung in exotic pastures is limiting the carrying capacity in this land use systems. Probably the introduction of omnivorous dung in this modified ecosystem may enable a species richness increase. Understanding which ecological filters determine dung beetle assembling in native savannas and exotic pastures is extremely important to guide management practices. To obtain a more diverse dung beetle assemblage in exotic pastures it is important to increase its vegetation complexity first and secondly to raise another type of domestic animal together with cattle (e.g. horses, sheeps) to increase the diversity of food resources for dung beetles. It would be also important to preserve patches of Cerrado within a mosaic of exotic pastures, to enable the conservation of native species that do not survive in exotic pastures and to facilitate the colonization of dung beetles species between these two land use systems. Diversifying dung beetle assemblage in exotic pastures will consequently increase the ecological services performed by these beetles (Louzada and Silva, 2009; Murilo et al., 2013), such as biological pest control and soil fertilization (Nichols et al., 2008). Declaration of Competing Interest The authors declare no potential competing interests. Also, this manuscript has not been published elsewhere, and all authors have approved its submission. Acknowledgments We would like to thank all land-owners who allowed us to work in their rural properties. Special thanks are given to Fabio Frazão, Leandro Morimoto and Victor Hugo Oliveira for their help in fieldwork, and to the EPAMIG of Pitangui, Minas Gerais. We also thank Fernando Vaz de Mello and Fernando Silva for their valuable contribution in species identification. Thanks to Daiany Joner for her help in making the sampling map. The author Renan Macedo was financed by CAPES and Julio Louzada was funded by CNPQ. L.D. Audino is supported by CNPq, proc. PDJ 150776/2017-9. Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.agee.2019.106709. References Almeida, S., Louzada, J., Sperber, C., Barlow, J., 2011. Subtle land-use change and tropical biodiversity: dung beetle communities in cerrado grasslands and exotic pastures. Biotropica 43, 704–710. Anderson, M.J., Gorley, R.N., Clarke, K.R., 2008. Primer. Benito, N., Brossard, M., Pasini, A., Guimarães, M.D.F., Bobillier, B., 2004. Transformations of soil macroinvertebrate populations after native vegetation conversion to pasture cultivation (Brazilian Cerrado). Eur. J. Soil Biol. 40, 147–154. https://doi.org/10.1016/j.ejsobi.2005.02.002. Beuchle, R., Grecchi, R.C., Shimabukuro, Y.E., Seliger, R., Eva, H.D., Sano, E., Achard, F., 2015. Land cover changes in the Brazilian Cerrado and Caatinga biomes from 1990 to 2010 based on a systematic remote sensing sampling approach. Appl. Geogr. 58, 116–127. https://doi.org/10.1016/j.apgeog.2015.01.017. Blaum, N., Seymour, C., Rossmanith, E., Schwager, M., Jeltsch, F., 2009. Changes in arthropod diversity along a land use driven gradient of shrub cover in savanna rangelands: identification of suitable indicators. Biodivers. Conserv. 18, 1187–1199. https://doi.org/10.1007/s10531-008-9498-x. Bond, W.J., Parr, C.L., 2010. Beyond the forest edge: ecology, diversity and conservation of the grassy biomes. Biol. Conserv. 143, 2395–2404. https://doi.org/10.1016/j. biocon.2009.12.012. Borcard, D., Legendre, P., Drapeau, P., 1992. Partialling out the spatial component of ecological variation. Ecology 73, 1045–1055. Bottinelli, N., Jouquet, P., Grimaldi, M., Peng, X., 2015. Why is the influence of soil macrofauna on soil structure only considered by soil ecologists? Soil Tillage Res. 146,
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Conversion of Cerrado savannas into exotic pastures: The relative importance of vegetation and food resources for dung beetle assemblages
T
Renan Macedoa, , Livia Dorneles Audinoa, Vanesca Korasakib, Julio Louzadac ⁎
a
Departamento de Entomologia, Universidade Federal de Lavras, Lavras, Minas Gerais, 37200-000 Brazil Departamento de Ciências Exatas e da Terra, Universidade do Estado de Minas Gerais, Frutal, 38200-000 Brazil c Departamento de Biologia, Universidade Federal de Lavras, Lavras, Minas Gerais, 37200-000, Brazil b
ARTICLE INFO
ABSTRACT
Keywords: Neotropical savannas Vegetation complexity Land use change Scarabaeinae Introduced pastures
Replacing native savannas with exotic pastures not only alters vegetation structure, but it also increases herbivorous cattle dung quantity consequently changing the food resource available for dung beetles. Therefore, this study aims at investigating the relative importance of vegetation structure regarding food resource types to determine dung beetle assemblage in Cerrado savannas and exotic pastures. We carried out a sampling of dung beetles in 30 areas of Cerrado sensu stricto and 30 in areas of exotic pastures across nine municipalities of Minas Gerais state, Brazil, by using pitfall traps baited with cattle dung and human feces. We also characterized these areas according to their herbaceous density, complexity (fractal dimension) and canopy cover. Our study demonstrates that the complete conversion of Cerrado sensu stricto into exotic pasture has a negative effect on dung beetle assemblages. The same dung types differed completely in dung beetle assemblages in native savannas and exotic pasture regarding richness, abundance, species composition and dominance patterns. These findings suggest that environmental filters in exotic pastures, as low cover canopy and herbaceous complexity simplification, probably restrict the establishment of species from Cerrado. We also found different dung beetle communities by comparing pitfall traps baited with cow dung and human feces within the same land use. Thus, alterations in food resources played a secondary role, but were also important. We suggest that increasing herbaceous complexity and canopy cover along with diversifying livestock in exotic pastures could potentially avoid the loss of dung beetles species and their associated ecosystem services.
1. Introduction Cerrado is an important tropical grassy phytogeographic domain that harbors a unique biodiversity and provides significant ecological services to humankind (Bond and Parr, 2010; Overbeck et al., 2015; Parr et al., 2014). Despite its importance, this ecosystem have been neglected regarding conservation public policies and are facing considerable threats due to human disturbance (Klink and Machado, 2005; Overbeck et al., 2015). The existence of large and relatively flat areas of native grasslands and savannas was decisive to determine human occupation in Cerrado, leading to the development of agriculture and animal husbandry (Klink and Moreira, 2002). This enhanced conversion of Cerrado into exotic pastures generating as a direct consequence of an increase in cattle herd (Horgan, 2001). Therefore, Cerrado is an important cattle ranching region, mainly based on extensive pastures (Klink and Machado, 2005). Despite being a subtle land use change (replacement of an open
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environment with another open environment), the substitution of Cerrado savannas with exotic pastures is considered one of the main causes of biodiversity loss and community disassembly (Almeida et al., 2011; Benito et al., 2004; Klink and Machado, 2005). To understand and obtain rapid and reliable responses on how land use change affects biodiversity, many studies have used bioindicators (Blaum et al., 2009; Verdú et al., 2011). Some insect groups, such as dung beetles (Coleoptera: Scarabaeinae), can be utilized for such purpose (Davis et al., 2012). Dung beetles are considered one of the best cost-effective bioindicator groups for being sensitive to ecosystem changes, broadly distributed, with well-known taxonomy and ecology, in addition to easy, low-cost sampling. For these reasons, they have been widely used to assess the anthropogenic impacts on tropical ecosystems (Gardner et al., 2008; Nichols and Gardner, 2011). Native grasslands and savannas of Cerrado have a great potential to serve as a species source for introduced pastures (Sano et al., 2000), since they are open environments that occupy almost 20% of the
Correspondence author at: Departamento de Entomologia, Universidade Federal de Lavras, 37200-000, Lavras, Minas Gerais, Brazil. E-mail address: [email protected] (R. Macedo).
https://doi.org/10.1016/j.agee.2019.106709 Received 22 June 2018; Received in revised form 1 October 2019; Accepted 5 October 2019 0167-8809/ Published by Elsevier B.V.
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Brazilian territory located between two huge tropical forests: Atlantic Forest and Amazon (Beuchle et al., 2015; Myers et al., 2000). However, dung beetle diversity is extremely low in exotic pastures in relation to native savannas, and species composition differs completely between these two land uses (Almeida et al., 2011; Davis et al., 2014; Horgan, 2008). Nevertheless, there are no studies investigating whether these effects are a result of changes in vegetation structure or food resource. The substitution of native savannas with exotic pastures causes modification in vegetation complexity. Cerrado savannas represent an herbaceous ecosystem that show some sparse shrubs and a few small trees, and exotic pastures are mainly composed by one species of grass (Oliveira and Marquis, 2002). This substitution can also change the quality and quantity of food resources, mainly as a consequence of alterations in fauna and flora in exotic pastures. Dung beetles are mostly coprophagous (Halffter and Matthews, 1966) and an important food resource for these insects in native savannas is the presence of omnivorous mammal dung (Davis et al., 2012). Besides omnivorous mammals, it is also possible to find carnivores and a few herbivores, since Cerrado presents a highly diverse mammalian fauna (around 194 species recorded) (Marinho-Filho et al., 2002). Mammalian assemblages are affected by the conversion of native savannas into exotic pastures, which generates a decrease in native mammal dung (Cáceres et al., 2010). For this reason, exotic pastures mainly display a high amount of herbivorous cattle dung (˜22 kg dung fresh per animal/day) (Fincher, 1981).Cattle dung is different from the dung produced by native herbivores from Cerrado (Rahagalala et al., 2009), since cattle dung pads are larger and more humid than native herbivores dung (Dickinson et al., 1981). Several studies have already confirmed that dung beetles present high specificity regarding dung type (e.g. Louzada and Silva, 2009; Tshikae et al., 2008; Martín-Piera and Lobo, 1996). Thus, the input of cattle dung can also be an important driver of dung beetle assemblage change after the introduction of exotic pastures in Cerrado. This study aims at investigating the importance of the herbaceous density and complexity, canopy cover and input cattle dung, an exotic food source to dung beetle assemblage in the introduced pastures. We tested the following hypothesis: changes in dung beetle assemblage are driven by the reduction of canopy cover, low herbaceous density and complexity with lower effect of dung types changes. In this context, if dung beetle assemblages are being influenced by changes in vegetation structure, then the assemblages will be different between native savanna and exotic pasture even when sampled using the same dung types. However, if dung beetles are influenced only by changes in food resources, then dung beetle assemblages sampled with omnivorous dung baits and herbivorous dung baits will be similar between Cerrado and exotic pastures.
and Marquis, 2002). However, since the 1980′s native grasslands and savannas of Cerrado are being replaced with exotic pastures for livestock production. These introduced pastures are generally monocultures of one common species of an exotic grass, such as Urochloa spp. (Syn. Brachiaria spp.). Currently, exotic pastures of Urochloa spp. cover wide areas of the Cerrado biome, generally becoming degraded-exotic pastures due to inadequate management practices (Cavalcanti and Joly, 2002). Over the past years, more than half of the original cover of Cerrado has been taken for livestock (Klink and Machado, 2005; Marris, 2005). Thus, Cerrado is an important cattle ranching region and its bovine herd has been growing substantially since the 1980s and is considered one of the most important regions for the beef production (Marris, 2005). Cerrado sensu stricto covers approximately 70% of the Cerrado biome and is an herbaceous ecosystem dominated by grasses and containing some sparse trees of 3–8 m tall and shrubs. These trees and shrubs provides nearly ˜30% of crown cover for this ecosystem (Oliveira-Filho and Ratter, 2002). Native savannas study sites had not been used to raise cattle mainly because the native vegetation is not adequate for grazing activities (McManus et al., 2011). Compared to African savannas, Cerrado savannas show very few large mammals and is essentially constituted of small and medium-sized animals, such as bats, rodents, primates, carnivores and didelphimorph marsupials. The largest herbivores recorded in areas of native Cerrado are the South American tapir, Tapirus terrestris, and species of small deers (Cervidae), from the genus Mazama, Blastocerus and Ozotocerus, occurring in small densities (Marinho-Filho et al., 2002). 2.2. Dung beetle survey We conducted our sampling in two types of land use systems: Cerrado sensu stricto (native savanna) and exotic pasture (Urochloa spp.). All exotic pastures sampled were similar regarding its vegetation and management characteristics. These areas were extensive pastures, composed predominantly by Urochloa spp. and used for cattle ranching to produce beef and/or milk. Thus, differently from native savannas, all exotic pastures presented cattle. We sampled dung beetles in areas of Cerrado sensu stricto and exotic pasture in ten landscape windows (at least 20 km apart). The distribution of these ten landscape windows encompasses nine municipalities (Fig. 1). For each landscape window, we sampled three sites of each land use type representing a total of 30 areas of Cerrado and 30 areas of exotic pasture. Each sampling site received five sampling points, 50 m apart, placed along a linear transect. The sampling points were constituted of two pitfall traps (3 m apart), one baited with human feces (25 g of human feces) and another with cattle dung (500 g of cattle herbivorous dung). We used human feces as a proxy for native’s omnivorous mammalian dung. Several studies have already showed that human feces can attract a greater number of dung beetle’s species, as well as that these species are generally different from the ones sampled in herbivorous dung (Puker et al., 2013; Whipple and Hoback, 2012). Our sampling effort amounted 150 sampling points per land use type, numbering 600 pitfall traps across ten landscape windows. We carried out the sampling during the rainy season, from January to February 2012, the most suitable period to sample dung beetle assemblage (Medina and Paixão-Lopes, 2014) and used pitfall traps in the field for 48 h. The inside of each trap was added with a solution containing water, salt and detergent. The trap baited with human feces received a plastic cup containing the bait, while the trap with cow dung received a nylon sachet containing cow dung suspended in a stake in the center of the trap. Sampled beetles were sent to the Universidade Federal de Lavras (UFLA) for identification at species level; upon uncertainty, a morphospecies number was given. Vouchers were deposited in Laboratório de Ecologia e Conservação de Invertebrados (Laboratory of Ecology and Conservation of Invertebrates) UFLA and in the
2. Methods 2.1. Study area We carried out this study in areas of native Brazilian savannas (Cerrado sensu stricto) and exotic pastures located in the municipalities of Montes Claros, Pitangui, Martinho Campos, Pompéu, Felixlândia, Curvelo, Pirapora, Buritizeiro, and Claro das Poções, in the Northeast Minas Gerais State, Brazil (Fig. 1, Appendix A – Table A1 in Supplementary material). The average annual temperature varies from 18 °C to 28 °C, and rainfall, from 800 mm to 2000 mm, with a very strong dry season during the autumn and winter (April–September). The regional biome climate is tropical savanna Aw (Köppen) (Oliveira and Marquis, 2002). The studied region was originally covered with typical phyto physiognomies of the Cerrado biome, which is composed predominantly by open native vegetation, such as grasslands (“campo limpo”) or savannas (“Cerrado sensu strictu”), and dense woodland (“Cerradão”) (Oliveira 2
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Fig. 1. Ten sampled landscape windows and its location in Minas Gerais state, Brazil. The grid represents coordinates in UTM (Universal Transverse Mercator) zone 23S – SAD69. The figure is composed by three minor figures. There is localization of Minas Gerais state in the Brazil, a localization of sampled points in Minas Gerais state and the last with a close in sample points, that represent a municipalities of Montes Claros, Pitangui, Martinho Campos, Pompéu, Felixlândia, Curvelo, Pirapora, Buritizeiro, and Claro das Poções, in the Northeast Minas Gerais State, Brazil.
Entomology Section of the Zoological Collection, Federal University of Mato Grosso (UFMT).
the herbaceous vegetation through the percentage of black pixels and white pixels from a dichromatic picture. For these two measures, we used the average of four pictures per sample point. We also took five photographs of the canopy, one at each sampling point (five per site) using a digital camera equipped with hemispherical lens (8 mm). The photographs were taken at 1 m above the ground and oriented towards the sky to be able to characterize canopy openness and analyzed using a Gap Light Analyser software package version 2 (Frazer et al., 1999).
2.3. Vegetation structure We characterized the vegetation of the sampling sites according to the following three variables: (1) herbaceous vegetation density, (2) herbaceous complexity, measured as the fractal dimension of vegetation, and (3) canopy openness. Measurement of these variables enables to assess habitat heterogeneity/homogeneity from open ecosystems (Gries et al., 2011; Marsden et al., 2002; Silva et al., 2010). It also reflects how the conversion of Cerrado sensu stricto into exotic pastures can alter natural environment original characteristics. Herbaceous vegetation and canopy openness can influence atmospheric and soil surface luminosity, humidity and temperature (Edmondson et al., 2016; Jennings et al., 1999; Özkan and Gökbulak, 2017). These abiotic characteristics affect dung beetle’s survival, reproduction, nidification, development, as well as food availability and attractiveness (Hanski and Cambeforti, 1991). Additionally, herbaceous density and complexity can hinder dung beetle’s flight displacement (Gries et al., 2011; Morse et al., 1985). To record herbaceous vegetation density and fractal dimension, we used a method proposed by Nobis (2005). Between two traps of each sampling point, a black panel of 1 m2 was placed vertically 10 cm above the ground. We took four photographs at a three-meter distance from the panel, one per cardinal direction using a digital camera. We analyzed the pictures by using the software Sidelook 1.1.01 (Nobis, 2005), which allows to calculate vegetation density and fractal dimension of
2.4. Statistical analysis We used generalized linear mixed models (GLMMs) to examine differences in mean species richness and abundance of dung beetles sampled with cattle dung and human feces between the land use types (native savannas and exotic pastures). Sampling site was considered the sample unit and land use type per dung type were considered explanatory variables and richness and abundance the response variables. In the models, we used landscape windows as a random factor and Poisson errors corrected for overdispersion (Quasi-Poisson) (O’Hara and Kotze, 2010). To correct overdispersion we fitted GLMM models with multivariate normal random effects by using Penalized QuasiLikelihood. All GLMMs were submitted to residual analysis to evaluate the adequacy of residual distribution. This analysis was performed in the R statistical programming language using ‘MASS’ package, function “glmmPQL” (Ripley and Bates, 2018). Subsequently, a Tukey contrast analysis using “multicomp” package (Hothorn et al., 2017) was performed to verify which categories were distinct regarding the response 3
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variables. We also compared dung beetle’s total species richness between native savannas and exotic pastures sampled with cattle dung and human feces using individual based interpolation and extrapolation curves within 95% confidence intervals (Colwell et al., 2012). We built interpolation and extrapolation curves since the number of individuals varied between land uses and baits, which can influence total species richness (Colwell et al., 2012). This analysis was performed using INEXT online implemented by R software (Chao et al., 2016). To observe dominance patterns in dung beetle assemblages sampled with pitfall traps baited with human feces and cattle dung in native savannas and exotic pastures, we constructed abundance distribution curves using the transformation log + 1. To graphically express changes in dung beetle species composition associated with each land use and dung types, we performed a nonmetric dimensional analysis (NMDS) over a Bray–Curtis similarity matrix with standardized and square-root transformed data, considering the sampling site as sample unit. To investigate whether dung beetle assemblage composition is different between land use and dung types, we applied a multivariate analysis of variance with permutations (PERMANOVA). In the model, the landscape windows was considered a random factor and land use and dung type and the interaction between land use types and baits as a fixed factor. We also identified the major species driving species composition patterns of dung beetle assemblages using similarity percentage analysis (SIMPER). SIMPER calculates the average dissimilarity among all pairs of samples by assessing the relative dissimilarity contributed per species to determine species composition differences among land use types and baits. NMDS, PERMANOVA and SIMPER analyses were performed on the Primer v.6 software with PERMANOVA+ (Anderson et al., 2008). We performed a variance partitioning analysis to evaluate the relative importance of vegetation structure and food resources to explain dung beetle species richness, abundance and composition inside each land use (Wezel et al., 2009) considering the sampling point as sample unit. This analysis was based on partial redundancy analysis for multivariate response data (e.g., species composition) as well as on partial multiple linear regression for univariate response data (e.g., species richness and abundance). Variance partitioning is ideal to decompose the variation of the response variables into independent and joint effects of suites of predictor variables (Borcard et al., 1992; Wezel et al., 2009). Data on herbaceous vegetation density, fractal dimension of the herbaceous vegetation and canopy openness represented the vegetation group of predictor variables and the dung type represented the food resources group of predictor variables. Prior to variance partitioning analysis, species trait composition was Hellinger-transformed. The variance partitioning analysis was performed using R software, vegan package, function varpart (Oksanen et al., 2014). Subsequently, we evaluated the individual contribution and the relationship of each vegetation variable (herbaceous vegetation density, fractal dimension of the herbaceous vegetation and canopy openness) with species richness, abundance and species composition using linear regression for univariate data and redundancy analysis for multivariate data. We performed this analysis separately for native savanna and exotic pastures data using vegan package in R environment (Oksanen et al., 2014). To verify how Cerrado sensu stricto and exotic pastures differ according to vegetation variables we performed generalized linear models (GLMs). In the models, land use systems categories was considered the predictor variable and each vegetation variable the response variable. We built the models by applying Gaussian distribution for herbaceous vegetation density and complexity and Quasi Binomial distribution for canopy openness in R software package (R Core Team, 2018), followed by residual analysis to check for the error distribution and model adequacy (Appendix B, Figure B1 in Supplementary material).
3. Results Almost half of all sampled species (45–46% species) were exclusive to native savannas. Of these native savanna’s exclusive species, five were collected only in pitfall traps baited with cattle dung, 21 only in pitfall traps baited using human feces and 20 in both dung types. In contrast, only seven species were exclusive to exotic pastures (6.9% of all sampled species). Of these seven species, one was collected only in pitfall traps baited using cattle dung and six only in pitfall traps baited with human feces. Forty-eight species (47% of all sampled species) were sampled in both land use systems. Of these species, one was sampled only using cattle dung and ten only with human feces. The complete information on the individuals collected according to the land use and type dung is in the supplementary material (Appendix C, Table C1 in Supplementary material). Richness was higher in native savannas in relation to exotic pastures; when considering both, dung beetles sampled with human feces and cattle dung. The highest mean values of species richness were obtained in traps baited using human feces in native savannas. Exotic pastures presented the lowest values of species richness. We obtained the lowest abundance values in exotic pastures in traps baited with human feces (Appendix D, Table D1; Fig. 2 in Supplementary material). Up controlling the differences in abundance among land use systems and baits through interpolation and extrapolation curves, total species richness was higher in traps baited using human feces in native savannas and lower in exotic pastures in cattle dung. Dung beetle’s total species richness presented intermediate values and was similar between traps baited using cattle dung in native savannas and baited using human feces in exotic pastures (Fig. 3).
Fig. 2. Mean species richness and abundance of dung beetles sampled with human feces and cattle dung in Brazilian native savannas and exotic pastures. Different letters above bars indicate statistically significant differences (P < 0.05). Error bars represent ± standard errors.
4
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Table 1 Results of the permutational analysis of variance (PERMANOVA) indicating whether the categories of landscape windows, land use systems (native savanna and exotic pasture), baits (cattle dung and human feces) and the interaction between land use systems and baits are different according to species composition. Pseudo-F and p-value are presented for the main test and test statistic (t) and p-values for each pair-wise comparison. * p-values < 0.05. Source of variation Landscape window Land use system Baits Land use systems:baits Post hoc comparison Land use systems: baits Pasture/cattle dung vs. pasture/human feces Pasture/cattle dung vs. savanna/cattle dung Pasture/cattle dung vs. savanna/human feces Pasture/human feces vs. savanna/cattle dung Pasture/human feces vs. savanna/human feces Savanna/cattle dung vs. savanna/human feces
Fig. 3. Individual-based interpolation and extrapolation curves from four samples of dung beetles from Minas Gerais, Brasil: 1) native savannas sampled with pitfall traps baited with cattle dung; 2) native savannas sampled with pitfall traps baited with human feces; 3) exotic pastures sampled with pitfall traps baited with cattle dung, and; 4) exotic pastures sampled with pitfall traps baited with human feces. Dotted lines represent 95% confidence intervals of each curve, continuous lines the interpolation curves and dashed lines the extrapolation curves.
Pseudo-F
p
11.09 4.96 10.47 6.43
0.0001* 0.0001* 0.0001* 0.0001*
t 3.03 2.33 3.11 2.12 2.05 2.55
p 0.0001* 0.0005* 0.0001* 0.0001* 0.0002* 0.0001*
Fig. 5. Distribution patterns (NMDS) of the sampling points comparing assemblage composition (Bray-Curtis similarity) between feces humans and cattle dung, in Brazilian savannas and exotic pastures, showing centroids (larger circles and squares) and dispersion of points to centroid (lines). Dark grey circles represent exotic pastures/cattle dung, white circles represent exotic pastures/human feces, light grey squares represent native savannas/cattle dung and black squares native savannas/human feces.
Fig. 4. Rank abundance distribution of dung beetles species sampled with pitfall traps baited with cattle dung and human feces in native savannas and exotic pastures. Light grey squares represent native savannas/cattle dung and black squares native savannas/human feces, dark grey circles represent exotic pastures/cattle dung, white circles represent exotic pastures/human feces. “a” = Ateuchus aff. pauperatus; “b” = Ontherus appendiculatus; “c” = Dichotomius bos; “d” = Agamopus viridis; “e” = Canthon fortemaginatus; “f” = Uroxys sp. C; “g” = Canthon simulans; “h” = Digithontophagus gazella; “i” = Onthophagus hirculus; “j” = Trichillum externepunctum; “l” = Canthon aff. podagricus.
variation in species richness, abundance and species composition of native savannas, respectively (Fig. 6A). Both vegetation and food resources determined species richness and composition. However, for species richness, vegetation structure was more important than food resources. Regarding abundance, all total variation explained was attributed to vegetation alone, being the only significant group of predictor variables. In the case of exotic pastures, variance partitioning models explained 11%, 10% and 15% of the variation in species richness, abundance and species composition, respectively (Fig. 6B). In all cases, both groups of predictor variables were considered significant. However, only for species composition, food resources proved more important than vegetation. In native savannas, canopy openness and herbaceous complexity proved the most important vegetation variables to determine species richness, abundance and species composition. Species composition was also influenced by herbaceous density in these native environments. In contrast, only herbaceous complexity was important to establish species richness and composition in exotic pastures; in addition, abundance was only influenced by herbaceous density (Table 2).
Abundance distribution curves of exotic pastures are steeper regarding native savannas, which presented shallower slopes (Appendix D, Table D1; Fig. 2 in Supplementary material). Dominance patterns was also different in the same land use type between cattle dung and human feces, where evenness of assemblages sampled using cattle dung are lower in regarding the assemblages sampled using human feces. Additionally, exotic species Digithontophagus gazella was one of the most dominant species only in cattle dung of exotic pastures (Fig. 4). Species composition was different among dung beetle assemblage sampled using cattle dung in native savannas human feces in native savannas, cattle dung in exotic pastures, and human feces in exotic pastures (Table 1; Fig. 5). Appendix E, Table E1 “in Supplementary material” illustrates the main species responsible for the differences in species composition among land use and dung. Variance partitioning models explained 24%, 15% and 10% of the 5
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The same dung types collected completely different dung beetle assemblages in native savannas and exotic pastures. Mean species richness and abundance were always lower in exotic pastures regardless of the dung used. Furthermore, dominance patterns and species composition of beetles that feed on omnivorous and herbivorous dung are different between native savannas and exotic pastures. These findings suggest that, besides changes in food resources, other ecological filters found in exotic pastures restrict the colonization, establishment and population increase for several species from Cerrado sensu stricto. Our results highlight that one of these ecological filters is vegetation structure. Variance partitioning models showed that dung beetles in native savannas are being mainly driven by vegetation characteristics. It is well known that vegetation structure can influence dung beetles even in open environment systems (Almeida et al., 2011; Davis et al., 2010; Gries et al., 2011; Martello et al., 2016). In native savannas, herbaceous complexity and canopy cover were the most important variables to explain dung beetle communities. In our study, the areas of Cerrado sensu stricto presented a higher degree of canopy cover and herbaceous complexity when compared to exotic pastures (Appendix B in Supplementary material). A simplification of the vegetation structure reduces the vegetation complexity modifying microhabitat conditions, exposing arthropods to higher levels of light, wind, temperature, lower humidity and predators (Gunnarsson, 1990; Van Klink et al., 2014). Still, vegetation complexity can probably increase the number of available niches (Klopfer and MacArthur, 1960), enabling the existence of a larger amount of species (Nittérus and Gunnarsson, 2006; Silva et al., 2010). Thus, more complex and closed native savannas generally present higher species richness (Blaum et al., 2009; Tews et al., 2004). Herbaceous complexity was also important for exotic pastures, where higher levels of complexity lead to a higher number of species and individuals. From the vegetation variables that we measured, canopy cover was the only unimportant to explain species richness, abundance, and composition in exotic pastures. This occurred because most of the pastures from our study did not present any degree of canopy cover. Herbaceous density was the least important variable for both native savannas and exotic pastures, probably because these systems did not differ in relation to this variable (Appendix B in Supplementary material). We suggest that the increase of the herbaceous complexity and canopy cover in exotic pastures can be an important insight to avoid the loss of dung beetles species. Increasing vegetation structure complexity could therefore avert biodiversity and ecosystem services loss in exotic pastures. Despite their importance, the vegetation variables explained only a small fraction of dung beetles species richness, abundance as well as composition in native savannas and exotic pastures. This high unexplained fraction of the variance may reflect the effects of unmeasured environmental variables in our study area and can decrease with the inclusion of other variables, such as soil type (Bottinelli et al., 2015; Halffter and Matthews, 1966; Manning et al., 2016), soil compaction (Herrick and Lal, 1995; Navarrete and Halffter, 2008) and landscape
Fig. 6. Variance partitioning models showing individual fractions of variation explained by vegetation and food resources (baits). The first panel shows results for native savannas when considering species richness, abundance and species composition and the second panel for exotic pastures. Vegetation (white) and food resource (black) fractions indicate unique contributions towards the overall amount of variance explained, and the striped fraction indicates the redundant portion co-explained by each. * = p values < 0.05.
4. Discussion Our study indicates that changes in dung beetle assemblage due to the conversion of Cerrado sensu stricto into exotic pastures are mainly driven by modifications in vegetation structure. Alterations in food resources are secondary at determining dung beetle assemblage modifications; however, it is still important to determine richness, abundance species composition in these two land uses.
Table 2 Amount of variation in species richness, abundance and assemblage composition explained by the vegetation individual predictor variables (canopy openness, herbaceous vegetation density, fractal dimension of the herbaceous vegetation) in native savannas and exotic pastures. R-squared were calculated using linear regression for species richness and abundance, and using redundancy analysis for assemblage composition (P-values were generated using a permutation procedure). Richness System
Variable
Native savanna
Canopy openness Fractal Density Canopy openness Fractal Density
Exotic pasture
R
2
0.04 0.06 0.007 0.00006 0.07 0.009
Abundance 2
P
R
0.001*** 0.001*** 0.13 0.9 0.001*** 0.09
0.08 0.03 0.003 0.00005 0.00001 0.07
6
Composition 2
P
R
0.001*** 0.005** 0.3 0.9 0.9 0.007**
0.02 0.02 0.009 0.005 0.03 0.003
P 0.001*** 0.001*** 0.002** 0.2 0.001*** 0.5
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context (Roslin and Koivunen, 2001; Tabarelli and Vaz-de-mello, 2015; Verdú et al., 2011). Substitution of native savannas with exotic pastures and the consequent changes in vegetation facilitate the colonization and dominance of species that are habitat generalists in exotic pastures (see Horgan, 2007). For example, most of exotic pastures dominant species are highly found in modified environments: Dichotomius bos, Trichillum externepunctatum, Onthophagus hirculus and Digithontophagus gazella (Tissiani et al., 2017). Digitonthophagus gazella (Génier and Davis, 2017) is an African dung beetle species, introduced in Brazil for the first time in 1989. Nowadays, it is widely distributed throughout Brazil (Génier and Davis, 2017; Matavelli and Louzada, 2008). In our study, this exotic species was one of the most abundant in introduced pastures, being mainly sampled with cattle dung. In native savannas, it was only found six individuals. This result indicates that the substitution of highly diverse Cerrado native savannas to monocultures of the nonindigenous grass Urochloa sp. and the introduction of a non-native mammal (cattle) can facilitate the invasion and dominance of an exotic dung beetle species (Simberloff and Von Holle, 1999). Digitonthophagus gazella is an extremely good competitor and used to feed on feces of large mammals (Génier and Davis, 2017). Probably the high diversity of dung beetle species found in native savannas can represent a resistance to the invasion of this exotic species (Elton, 1958). We also found different dung beetle communities when we compared pitfall traps baited with cow dung and human feces within the same land use, corroborating that dung type can have an influence in dung beetle assembling. Several dung beetles species are specialists according to dung type (Martín-Piera and Lobo, 1996; Tshikae et al., 2008; Whipple and Hoback, 2012). This trophic preference exists because dung types are different according to its physical-chemical attributes (Dormont et al., 2010; Tshikae et al., 2008). Different dung types vary regarding the chemical odors released by them to water content, nutritional qualities, fiber and dropping size (Halffter and Matthews, 1966; Tshikae et al., 2008). Still, dung quality and attractiveness are inherent to the physiology, digestion, and bacterial microflora present in the mammal, and are not a result of food type alone (Whipple and Hoback, 2012). For this reason, changes in dung type, such as nitrogen-rich omnivore droppings for pads of ruminant herbivores, and a decrease in the quantity of a preferred dung can cause species loss, reduce population size and modify species composition (Tshikae et al., 2013). Differently from native savannas, food resources were more important than vegetation structure at determining dung beetle assemblages in exotic pastures. Exotic pastures present a more simplified vegetation structure, which probably makes food resources more important to drive species distribution (Horgan, 2008). In this context, the input of cattle dung is an important factor to determine which species are going to be found in exotic pastures (Louzada and Silva, 2009). Domestic livestock increase the abundance of some species due to their ability to manipulate dung of domestic mammals that were not present before (Horgan, 2008). Probably, vegetation is not as important as food resources, because the species found in exotic pastures are generally habitat generalists (Horgan, 2008). Species richness and abundance captured in pitfalls baited with cow dung were higher in native savannas against exotic pastures, which emphasizes that dung beetles of native savannas can be attracted to herbivorous dung. Cattle was introduced in Brazil 500 years ago, enabling some native dung beetles to utilize cow dung as food resource (Louzada and Silva, 2009). According to Louzada and Silva (2009), there are many species of dung beetles from several Brazilian regions active in exotic pastures feeding on cattle dung. However, our results show that these beetles are mostly different from the ones captured with cattle dung in native savannas. Additionally, we found a small number of species that feed on omnivorous dung in exotic pastures, which is probably being driven by the small number of individuals
found in this land use with human feces. This is reflected by the interpolation/extrapolation curves (Fig. 3), since when abundance of land system/baits was put at the same level, total species richness of exotic pastures/omnivorous dung was the same in relation to native savannas/ cattle dung. These results suggests that the lack of omnivorous dung in exotic pastures is limiting the carrying capacity in this land use systems. Probably the introduction of omnivorous dung in this modified ecosystem may enable a species richness increase. Understanding which ecological filters determine dung beetle assembling in native savannas and exotic pastures is extremely important to guide management practices. To obtain a more diverse dung beetle assemblage in exotic pastures it is important to increase its vegetation complexity first and secondly to raise another type of domestic animal together with cattle (e.g. horses, sheeps) to increase the diversity of food resources for dung beetles. It would be also important to preserve patches of Cerrado within a mosaic of exotic pastures, to enable the conservation of native species that do not survive in exotic pastures and to facilitate the colonization of dung beetles species between these two land use systems. Diversifying dung beetle assemblage in exotic pastures will consequently increase the ecological services performed by these beetles (Louzada and Silva, 2009; Murilo et al., 2013), such as biological pest control and soil fertilization (Nichols et al., 2008). Declaration of Competing Interest The authors declare no potential competing interests. Also, this manuscript has not been published elsewhere, and all authors have approved its submission. Acknowledgments We would like to thank all land-owners who allowed us to work in their rural properties. Special thanks are given to Fabio Frazão, Leandro Morimoto and Victor Hugo Oliveira for their help in fieldwork, and to the EPAMIG of Pitangui, Minas Gerais. We also thank Fernando Vaz de Mello and Fernando Silva for their valuable contribution in species identification. Thanks to Daiany Joner for her help in making the sampling map. The author Renan Macedo was financed by CAPES and Julio Louzada was funded by CNPQ. L.D. Audino is supported by CNPq, proc. PDJ 150776/2017-9. Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.agee.2019.106709. References Almeida, S., Louzada, J., Sperber, C., Barlow, J., 2011. Subtle land-use change and tropical biodiversity: dung beetle communities in cerrado grasslands and exotic pastures. Biotropica 43, 704–710. Anderson, M.J., Gorley, R.N., Clarke, K.R., 2008. Primer. Benito, N., Brossard, M., Pasini, A., Guimarães, M.D.F., Bobillier, B., 2004. Transformations of soil macroinvertebrate populations after native vegetation conversion to pasture cultivation (Brazilian Cerrado). Eur. J. Soil Biol. 40, 147–154. https://doi.org/10.1016/j.ejsobi.2005.02.002. Beuchle, R., Grecchi, R.C., Shimabukuro, Y.E., Seliger, R., Eva, H.D., Sano, E., Achard, F., 2015. Land cover changes in the Brazilian Cerrado and Caatinga biomes from 1990 to 2010 based on a systematic remote sensing sampling approach. Appl. Geogr. 58, 116–127. https://doi.org/10.1016/j.apgeog.2015.01.017. Blaum, N., Seymour, C., Rossmanith, E., Schwager, M., Jeltsch, F., 2009. Changes in arthropod diversity along a land use driven gradient of shrub cover in savanna rangelands: identification of suitable indicators. Biodivers. Conserv. 18, 1187–1199. https://doi.org/10.1007/s10531-008-9498-x. Bond, W.J., Parr, C.L., 2010. Beyond the forest edge: ecology, diversity and conservation of the grassy biomes. Biol. Conserv. 143, 2395–2404. https://doi.org/10.1016/j. biocon.2009.12.012. Borcard, D., Legendre, P., Drapeau, P., 1992. Partialling out the spatial component of ecological variation. Ecology 73, 1045–1055. Bottinelli, N., Jouquet, P., Grimaldi, M., Peng, X., 2015. Why is the influence of soil macrofauna on soil structure only considered by soil ecologists? Soil Tillage Res. 146,
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