1 3 J Insect Conserv (2016) 20:957–970 DOI 10.1007/s10841-016-9928-0 ORIGINAL PAPER Edge and land use efects on dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae) in Brazilian cerrado vegetation Felipe Martello1  · Fernando Andriolli2 · Thamyrys Bezerra de Souza3 · Pavel Dodonov3 · Milton Cezar Ribeiro1  Received: 17 February 2016 / Accepted: 5 October 2016 / Published online: 12 November 2016 © Springer International Publishing Switzerland 2016 particularly in landscapes with a pasture matrix. However, this land use disrupts the species composition of commu- nities, indicating that communities located in cerrado and pasture have a distinct species composition, and that both communities are afected by edge distance. Thus, anthro- pogenic land uses may severely afect dung beetles, and this impact can extend to communities located in cerrado remnants as well as to those in matrices, with possible con- sequences for ecological processes such as decomposition and nutrient cycling. Keywords Brazilian savanna · Sugarcane · Pasture · Eucalyptus · Akaike’s Information Criterion Introduction Habitat fragmentation is one of the major threats to bio- diversity (Butchart et  al. 2010). Among its most perva- sive efects are those related to changes in microhabitat conditions at the interface between natural and anthro- pogenic land uses, a phenomenon referred to as edge inluence (Fahrig 2003). Over 20 % of the remaining for- est vegetation worldwide is located within 100  m of an edge (Haddad et al. 2015) and therefore may be subject to severe edge inluence (Harper et al. 2005). This situation may be even worse in some tropical forests—for example, nearly 50 % of the Brazilian Atlantic forest area is 100 m or less from the edge of the forest (Ribeiro et al. 2009). Vegetation edges in human-dominated landscapes are characterized by changes in species composition (Foggo et  al. 2001; Harper et  al. 2005), with a greater abun- dance of generalist and invasive species than in undis- turbed areas (Laurance et  al. 2002). Soil insects, which are responsible for important ecological processes such Abstract The Edge Inluence is one of the most perva- sive efects of habitat fragmentation, as many forest rem- nants in anthropogenic landscapes are within 100  m of edges. Forest remnants may also afect the surrounding anthropogenic matrix, possibly resulting in a matrix–edge– remnant diversity gradient for some species groups. We sampled dung beetles in 15 agricultural landscapes using pitfall traps placed along transects in matrix–edge–rem- nant gradients. The remnants were a native savanna-like vegetation, the cerrado, and the matrix was composed of three human-dominated environments (sugarcane, eucalyp- tus, pasture). More species were observed in cerrado rem- nants than in adjacent land uses. Dung beetles were also more abundant in the cerrado than in the landscape matrix of sugarcane and eucalypt, but not of pasture. Dung beetles were severely afected by anthropogenic land uses, and not- withstanding their high abundance in some land uses such as pasture, the species richness in these areas tended to be smaller than in the cerrado remnants. We also found that the inluence of the edge was evident only for abundance, Electronic supplementary material The online version of this article (doi:10.1007/s10841-016-9928-0) contains supplementary material, which is available to authorized users. * Felipe Martello felipemartello@gmail.com 1 Spatial Ecology and Conservation Lab (LEEC), Ecology Department, São Paulo State University, UNESP, Avenida 24 A, 1515 Bela Vista, Rio Claro, SP, Brazil 2 Post Graduation Program in Ecology, National Institute of Amazon Research – INPA, Av. André Araújo, 2936 Manaus, AM, Brazil 3 Applied Ecology and Conservation Lab, Biological Science Department, State University of Santa Cruz, UESC, Rodovia Ilhéus-Itabuna, km 16, 45662-000 Ilhéus, BA, Brazil http://orcid.org/0000-0003-1243-9750 http://crossmark.crossref.org/dialog/?doi=10.1007/s10841-016-9928-0&domain=pdf http://dx.doi.org/10.1007/s10841-016-9928-0 958 J Insect Conserv (2016) 20:957–970 1 3 as decomposition and nutrient cycling (Whitford 1996; Brussaard et  al. 1997), are among the groups afected by edges in both tropical and temperate regions (Meyer et al. 2009; Delgado et al. 2013a, b; Barrera et al. 2015). Still, notwithstanding the large number of studies dem- onstrating the inluence of edges on diferent organisms, many others have failed to detect edge-related gradients, and there is still no consensus on how edges afect some organisms (Ries et al. 2004). Edge inluence may depend on the type of matrix sur- rounding the forest fragments (Delgado et  al. 2007; Pohl- man et al. 2007; Kowal and Cartar 2012). Edge inluence is expected to be greater when the fragment and the adjacent land use are more dissimilar in terms of vegetation struc- ture, ecological processes and/or microclimate (Ries et al. 2004; Harper et  al. 2005). For example, higher-contrast edges exerted a stronger edge inluence than lower-contrast edges on air moisture in the Brazilian cerrado (Dodonov et al. 2013), on dung beetles in Argentinian Atlantic Forest (Peyras et al. 2013), and on lying insects in New Zealand (Campbell et al. 2011). Thus, when edge contrast is lower, the microclimate and vegetation at the edge may be simi- lar to the reference conditions, and an organism may occur with equal abundance at the edge and in the fragment’s interior, even if it is more or less abundant in the matrix. The same applies to the efects exerted by the vegetation remnant on the surrounding matrix. Conversely, some stud- ies failed to detect a relationship between edge contrast and vegetation structure (Dodonov et  al. 2013) or plant litter biomass (Dodonov et al. 2016) in the cerrado, showing that this relationship is not universal. Furthermore, a number of organisms, particularly the more generalist ones, may use the matrix habitat as well as the native vegetation remnants. For example, matrix habi- tats may be important to, or at least usable as complemen- tary habitat (Ries et  al. 2004) by, non-volant small mam- mals (Martin et  al. 2012; Cooney et  al. 2015), by birds (Hansbauer et  al. 2009) and by several arthropod species (Borges and Brown 2001; Dennis et al. 2006). Even organ- isms that survive better in forested environments may use the matrix, albeit with lower abundances than in the vegeta- tion fragments. The abundance of diferent organisms and the number of species of a given group in the fragments and in the matrix will depend on the resources available in each environment and will therefore vary between matrix types (Ries et al. 2004; Driscoll et al. 2013). For example, in comparison to a monoculture matrix, an agroforestry matrix may ofer a larger quantity of resources and will probably harbor a greater number of species occurring in greater abundances. Both the edge contrast and matrix suit- ability may afect the existence and shape of edge-related gradients in agricultural landscapes, with edge contrast afecting the gradient’s degree of conspicuousness, and the matrix quality afecting the diference in abundance between the forest and the matrix. To aid in understanding the efects of diferent matrices on edge inluence and the distribution of organisms, we addressed the variation in richness and abundance of an important group of soil insects—the dung beetles (Coleop- tera: Scarabaeinae)—in Brazilian cerrado fragments and the surrounding human-dominated environments in South- east Brazil. We focused on this group of organisms because they are highly diverse in tropical regions and provide sev- eral ecosystem functions such as decomposition of organic matter in nutrient cycling, improvement of physical and chemical properties of soil, parasite suppression and sec- ondary seed dispersion (Nichols et al. 2007, 2008; Campos and Hernández 2013). In addition, due to their association with vegetation structure (Hanski and Camberfort 1991a, b; Nichols et al. 2007; Gardner et al. 2010; Almeida et al. 2011), they are sensitive to habitat alteration and are one of the irst organisms to be afected by anthropogenic dis- turbance (Larsen and Forsyth 2005). For that reason, and because dung beetles are easily sampled and have a well- known ecology and taxonomy, these insects are widely used for biodiversity monitoring, especially in agricultural or anthropogenic environments (Audino et al. 2014; Figuei- ras et al. 2015). Coprophagy, the consumption of faeces, is the funda- mental feature of the biology of Scarabaeinae and deter- mines characteristics of behavior, morphology, develop- ment and distribution (Halfter and Matthews 1996). Dung beetles use faeces for feeding or oviposition (Hanski and Cambefort 1991a, b), and resource partitioning, through diferent dung-manipulation strategies, allows the coex- istence of many species (Hanski and Cambefort 1991a, b). Regarding dung-manipulation strategies, this group is divided into three guilds: telecoprids (rollers—adults group an amount of faeces into a ball and roll it some distance from the point of origin); paracoprids (tunnelers—adults dig tunnels in the soil under the faeces); and endocoprids (dwellers—adults and larvae feed within the fresh faecal deposits). These dung-manipulation strategies feature much variation regarding the depth, speed and amount of faeces buried (Doube 1990). The several ecosystem functions pro- vided by dung beetles are more dependent on these func- tional properties and combinations of species than on spe- cies richness alone (Slade et al. 2007), and this functional richness may decrease as a result of habitat loss and frag- mentation (Barragán et al. 2011). We assessed how the abundance, richness and com- position of dung beetles as a whole and of the diferent dung-manipulation strategies (telecoprids, paracoprids and endocoprids) in Brazilian cerrado (a savanna-like vegetation) fragments are afected by diferent land uses: pasture; sugarcane (Saccharum officinarum) plantations; 959J Insect Conserv (2016) 20:957–970 1 3 and eucalypt (Eucalyptus spp.) plantations. We expected species richness, for dung beetles as a whole and for each guild, to be greater in the cerrado than in the adja- cent matrices due to increased resource variability. We expected total dung beetle abundance to be greater in the pasture than in the cerrado due to resource availability, but to be lower in the other matrices compared to the cer- rado. This hypothesis also relects the pattern expected for paracoprids, as this guild is often the most abundant, and its behavior of storing faeces in underground tunnels enables these species to survive in drier environments. Finally, we expected to observe edge-related gradients in the low-contrast matrix, namely eucalypt (due to its forest-like phytophysionomy) and pasture (low manage- ment), because these environments present less difer- ence between the cerrado and the adjacent matrix, allow- ing species that are characteristic of both environments to use the edge zone. In the high-contrast matrix, namely sugarcane, we expected a discontinuous pattern, as many species would be restricted to either the cerrado or the matrix (Fig. 1). Methods Study area We performed this study in 15 agricultural landscapes com- posed of fragments of cerrado sensu stricto vegetation sur- rounded by diferent land uses. The landscapes are located in the Corumbataí river basin, São Paulo State, Southeast Brazil, between latitudes 22°04′46″S and 22°41′28″S and longitudes 47°26′23″W and 47°56′15″W (Fig. 2). The cer- rado is characterized by a savanna woodland with a discon- tinuous canopy layer and tree heights between 5 and 8 m; heliophilous grasses, sedges, herbaceous species and sub- shrubs occupy its ground layer (Coutinho 1978; Ribeiro and Walter 2008). Three of the studied fragments were Fig. 1 Schematic representation of expected responses of dung bee- tle abundance and species richness, total and per guild, to distance from edge for three diferent land uses (pasture, eucalypt and sug- arcane). Two horizontal lines represent the categorical fragment— matrix model and a non-linear curve represents the gradient model 960 J Insect Conserv (2016) 20:957–970 1 3 surrounded by pastures, ive by eucalypt plantations and seven by sugarcane plantations (Table  1). Pastures were large open areas without intensive management (applica- tion of herbicides or pesticides) and with low stocking rates (between 0.3 and 1.14 cattle per hectare) (Sparovek et  al. 2011). This region is characterized by a subtropical dry- winter climate (Valente 2001) with average yearly precipi- tation of about 1,400  mm, 80 % of which is concentrated between October and February (Zavatini and Cano 1993). Dung beetle sampling and identiication In each of the study fragments, we established two tran- sects placed 50  m apart and perpendicular to the frag- ment’s edge. Each transect contained eight pitfall traps, four in the matrix and four in the fragment, with 25  m between adjacent traps. Although the distance between traps was smaller than recommended for independent samples (Larsen and Forsyth 2005; Silva and Hernán- dez 2015), a wider spacing could have precluded the detection of edge-related gradients. The traps closest to the fragment − matrix boundary within each transect were positioned in both the fragment and the matrix at 12.5 m from the boundary. The traps were composed of a 1-L cylindrical receptacle holding 250 mL of water with 2 % detergent, saturated with sodium chloride to minimize decomposition. At the center of the receptacle, we placed human faeces as bait in a 50-mL plastic cup suspended from a wire, and we covered the trap with a tilted Sty- rofoam disk for protection against rain and desiccation of the bait (Hernandez and Vaz-de-Mello 2009). As only human faeces were used as an attractant, only copropha- gous Scarabaeinae were sampled. The traps were exposed for 48 h, after which their contents were passed through a ine mesh and deposited in plastic bags with 70 % alcohol for subsequent processing and species identiication in the lab. Each transect was sampled three times between December 2011, January and February 2012, the period of highest abundance of this group in southern Brazil (Hernández and Vaz-de-Mello 2009). Fig. 2 Satellite image of the location of the study landscapes. The small map indicates the location of the image (black rectangle) within the State of São Paulo (dark grey), Brazil (light grey). Polygons rep- resent the type of matrix that composed the cerrado boundaries: squares represent pasture, triangles represent eucalyptus plantations, and circles represents sugarcane plantations 961J Insect Conserv (2016) 20:957–970 1 3 Dung beetles were then identiied to the most detailed taxonomic level possible, and information on their guilds was obtained from the literature (Halfter and Matthew 1996; Doube 1990; Vulinec 2002; Alarcón et al. 2009; Lib- eral et al. 2011; Beiroz 2012). Data analysis For the analyses, we pooled the data for each distance, along each transect, thus combining the data from the three campaigns and the two transects corresponding to each distance. We then used the landscapes with each dominant land use (pasture, eucalypt or sugarcane) as replicates, thus having 3–8 replicates at each distance for each land use. We used total abundance and richness and the abundance and richness of each guild as response variables. We analyzed the relationship of each response variable with positions along the transect by adjusting three compet- itive models: a null model, a categorical fragment–matrix model, and a continuous interior–edge–matrix model, which we called the gradient model. The adjustments were made as generalized linear or additive mixed models with a Poisson distribution. The null model assumes that the response variable is homogeneous along the transect and is not afected by the position along the transect nor by the environment. The fragment–matrix model assumes that the response variables do not vary with distance into the frag- ment nor into the matrix, but may vary between these two environments (e.g. total abundance in sugarcane landscapes in Fig.  1). The gradient model assumes that the response variables are related to their position along the transect (from −85  m into matrix to 85  m into the interior of the cerrado, where zero is the edge transitional zone), with- out explicitly diferentiating between fragment and matrix (e.g. total abundance in eucalypt and pasture landscapes in Fig.  1). Thus, the fragment-matrix model considers only diferences between the two environments (habitat and matrix), whereas the gradient model is able to account for edge inluence and for continuous variation along the tran- sect. The null model was represented by a linear intercept- only model; the fragment–matrix model, by a generalized linear model with the two habitat types modeled as categor- ical variables; and the gradient model, by an additive model with a smoothing function for distance along the transects. In all analyses, we included the sampled landscape as a ran- dom factor and calculated the (Laplace approximate) maxi- mum likelihood. The optimal amount of smoothing in the gradient model was deined by means of a cross-validation procedure (Zuur et al. 2009). Using Akaike’s Information Criterion corrected for small sample size (AICc), we calculated the values for the three models as well as for the diference in the AICc of each model relative to the model with the smallest AIC value (∆AICc). We selected the model with the small- est AICc when the ∆AICc of other models was >2.0, as models with a ∆AIC of 2.0 or less may be considered as having substantial support (Burnham and Anderson 2002). Although there are several criticisms of the use of an arbitrary cutof to determine which model is best (Burnham and Anderson 2014; Murtaugh 2014; Valpine 2014), we chose to deine an a priori cutof because of the large number of response variables, which would otherwise have made a more thorough assessment of the support for each model too subjective. When two or more Table 1 Characteristics of the study areas of dung beetle communities, including the dominant matrix, its municipality (all in São Paulo State, Southeastern Brazil), coordinates of each landscape (decimal degrees) and total number of species found in each study site and in the corresponding fragment and matrix Landscapes P1–P3 are occupied by a pasture matrix, E1–E5 by eucalypt and S1–S7 by sugarcane Landscape Matrix Municipality Coordinates Number of species Latitude Longitude Total Cerrado Matrix P1 Pasture Analândia −22.115 −47.646 17 14 13 P2 Pasture Corumbataí −22.270 −47.656 35 34 21 P3 Pasture Analândia −22.244 −47.688 20 16 14 E1 Eucalypt Itirapina −22.252 −47.759 23 14 19 E2 Eucalypt Brotas −22.301 −47.896 23 19 17 E3 Eucalypt São Carlos −22.092 −47.877 23 12 16 E4 Eucalypt Analândia −22.146 −47.649 30 19 17 E5 Eucalypt Analândia −22.135 −47.634 25 19 15 S1 Sugarcane Itirapina −22.247 −47.707 21 16 7 S2 Sugarcane Itirapina −22.184 −47.876 28 17 25 S3 Sugarcane Brotas −22.259 −48.154 25 21 14 S4 Sugarcane Brotas −22.310 −48.120 26 18 15 S5 Sugarcane Brotas −22.291 −48.161 35 27 16 S6 Sugarcane Brotas −22.294 −48.095 34 22 22 S7 Sugarcane Analândia −22.146 −47.640 18 15 9 962 J Insect Conserv (2016) 20:957–970 1 3 models had small ∆AICc values, we selected the simplest model. When both the gradient and the fragment–matrix models had ∆AICc of 2.0 or less, we selected the simpler fragment–matrix model because it assumes that there are diferences between the two areas but no edge inluence. When the simplest null model was among the models with a ∆AICc of 2.0 or less, we considered it as the best model because it assumes neither edge inluence nor dif- ferences between the two areas. When either the fragment–matrix or the gradient model was selected, we also noted whether species richness was greater in the fragment or the matrix. Thus, there were ive possible outcomes for each response variable at each landscape type: no response (null model); greater abun- dance in the matrix, with no gradient; greater abundance in the fragment, with no gradient; greater abundance in the matrix, with a gradient indicating edge inluence; or greater abundance in the fragment, with a gradient indicating edge inluence. We also performed a non-metric multidimensional scal- ing ordination (NMDS) of all landscapes, using Bray-Curtis distance, to describe and interpret the patterns of commu- nity composition along the edge distance. All analyses were performed in R 3.2.4 (R Core Team 2015). The null and fragment − matrix model were adjusted with the glmer function of the lme4 package (Bates et al. 2015), whereas the gradient models were adjusted with the gamm4 package (Wood and Sheipl 2014), based on the mgcv (Wood 2011) package. The AICc values were obtained with the MuMIn package (Barton 2015). The NMDS ordination was performed with the vegan package (Oksanen et al. 2013). Results In the 15 study areas, we sampled a total of 8398 individ- uals, belonging to 57 species and 21 genera. We observed between 3 and 165 (mean of 25.1 ± 40.1 SD) individu- als per pitfall in the diferent matrices and between 13 and 118 (mean of 44.9 ± 26.9) individuals per pitfall in the fragments (Fig. 3). The mean number of species per Fig. 3 Abundance of dung beetle species, per resource allocation guild, sampled in landscapes composed of the Brazilian savanna, cer- rado (positive values of distance from edge), and three diferent land uses (negative values of distance from edge). Vertical dotted lines represent edges between cerrado and its adjacent matrix 963J Insect Conserv (2016) 20:957–970 1 3 pitfall ranged from 2.3 to 10.9 (mean of 5.5 ± 2.4) spe- cies in the matrix and from 5 to 15.1 (mean of 8.9 ± 2.8) in the cerrado. The paracoprid guild was the richest in species (32 species), followed by the telecoprid (18 spe- cies) and the endoprid (seven species), and the abundance of most species difered between the matrix and the rem- nants (Fig. 3). The most abundant guild in both cerrado and matrix (regardless of the type of land use) was the paracoprid, with 3496 individuals in cerrado (mean of 10.53 ± 12.56 per pitfall) and 1578 individuals in difer- ent matrices (mean of 5.42 ± 9.65 per pitfall). The endo- coprid guild had 986 individuals sampled in the cerrado (mean of 2.97 ± 7.09 per pitfall) and 807 individuals in diferent matrices (mean of 2.77 ± 12.61 per pitfall). The telecoprid was the least abundant guild, with 907 indi- viduals sampled in the cerrado (mean of 2.73 ± 3.67 per pitfall) and 624 individuals in diferent matrices (mean of 2.14 ± 7.01 per pitfall). The patterns of total abundance and richness var- ied among land uses, and their response to edge dis- tance always followed the same pattern demonstrated by the paracoprid guild. Total and paracoprid abundances decreased linearly from the matrix into the cerrado in the pasture landscapes (gradient model), but they were greater in the cerrado than in the matrices of the euca- lypt and sugarcane landscapes, with no edge inluence detected (Fig.  4). The numbers of total and paracoprid species did not vary between matrix and cerrado in the pasture landscapes and were smaller in the matrices of the other landscapes (Fig.  5). The abundance of endo- coprids was greater in the matrices than in the cerrado in the pasture and sugarcane landscapes, but smaller in the matrices of the eucalypt landscapes, with no detect- able edge inluence in any landscape (habitat−matrix model) (Fig.  4). The richness of this guild was greater in the matrices than in the cerrado in the eucalypt and Fig. 4 Abundance of dung beetle resource allocation guilds sampled in landscapes composed by the Brazilian savanna, cerrado (positive values of distance from edge), and three diferent land uses (nega- tive values of distance from edge). Vertical lines at zero value on x-axes represent the edge between the two environments composing the landscape. Black lines represent the selected model, expressing the response of dung beetles to edge distance: dashed line represents the gradient model, two dotted lines represent the fragment-matrix model, and continuous lines represent the null model 964 J Insect Conserv (2016) 20:957–970 1 3 sugarcane landscapes, with no edge inluence detected, and it did not change between habitats in the pasture landscapes. The ∆AICc values of the models are pre- sented as supplementary material. The NMDS ordination revealed that patterns of dung beetle species composition along transects difer depend- ing on the matrix adjacent to the remnant (Fig. 6). In edges adjacent to sugarcane matrix, there was either a gradual transition in dung beetle composition along transects or a fuzzy diferentiation between the communities located in either the matrix or the cerrado. Conversely, the ordination analysis of the pasture matrix showed a much clearer difer- entiation between the matrix and the cerrado. The composi- tion of dung beetles in the eucalypt matrix showed a dif- ferentiation between the communities located in the matrix and those in the cerrado, with a more evident edge zone (Fig. 6). Discussion Our results showed great variation in the abundance and richness of dung beetles between the cerrado fragments and the adjacent matrix. This variation was observed for all beetles, for guilds and for some species. Our expecta- tions regarding the number of dung beetle species were mostly conirmed, which was generally larger in the cer- rado fragments than in the adjacent matrix. This indi- cates that, even though many dung beetle species are able to survive in the matrix, the natural vegetation ofers a greater variety of resources and habitats for their sur- vival. Regarding beetle abundances, our expectations were mostly conirmed: dung beetles were frequently more abundant in the pasture than in the adjacent cer- rado, but less abundant in the other anthropogenic land uses. Dung beetle abundance depends on the speciic land Fig. 5 Richness of dung beetle resource allocation guilds sampled in landscapes composed of the Brazilian savanna, cerrado (positive values of distance from edge), and three diferent land uses (negative values of distance from edge). Vertical lines at zero value on x-axes represent the edge between the two environments composing the landscape. Black lines represent the selected model, expressing the response of dung beetles to edge distance: two dotted lines represent the fragment-matrix model, and continuous lines represent the null model 965J Insect Conserv (2016) 20:957–970 1 3 use being considered, and simply classifying land uses as either natural or anthropogenic does not provide an ade- quate description of the impacts on the community. Scarabeinae difer in their preference regarding physi- cal and chemical characteristics of faeces (Gittings and Giller 1998) and have been shown to discriminate dif- ferences in nutritional value (Verdú and Galante 2004), dung shape (Gordon and Cartwright 1974), water and/ or ibre content (Verdú and Galante 2004) and dung size (Peck and Howden 1984). Thus, increasing the diversity of faeces (especially from large mammals) promotes an increase in the diversity of dung beetles (Nichols et  al. 2009). Although pastures may have a greater abundance of resources than other land uses, these resources usu- ally come from a single provider—cattle. The domi- nance of cattle in this matrix suggests high competition between species that prefer this resource, resulting in the dominance of only a few species (Louzada and Silva 2009; Almeida et  al. 2011). Moreover, high cattle den- sity causes soil compaction, which has negative impacts on dung beetle diversity (Almeida et  al. 2011). In this study, we detected an increase in the total abundance of dung beetles in the pasture matrix, as would be expected from the increase in resource quantity. Contrarily to our expectations, the richness in the pasture landscapes did not change between the matrix and the adjacent cer- rado. However, this outcome does not mean an absence of change between dung communities located in these two habitats, since the NMDS ordination showed that the composition of communities located in these adja- cent habitats were diferent, indicating that the pasture modiies the community composition of dung beetles to a greater degree than the adjacent cerrado. Although most dung beetles in tropical savanna are not host spe- cialists (Spector and Ayzama 2003), the characteristics of the habitat wherein the dung is located, as well as the competition between species, can play a key role in deter- mining the community composition (Roslin and Vijanen 2011). In highly modiied habitats, dung beetle communities are characterized by the dominance of a few species, with small-bodied species tending to aggregate more than large- bodied species, possibly as a result of having smaller niche diferences (Koller et  al. 1999; Scheler 2005; Nichols et al. 2007; Simmons and Ridsdill-Smith 2011). The loss of large-bodied beetles may have signiicant secondary conse- quences for community structure and subsequent patterns of ecological function; for example, in the function of waste removal, large-bodied beetles remove disproportionately more dung than smaller-bodied beetles (Larsen and For- syth 2005; Slade et al. 2007; Dangles et al. 2012). In this study, the small-bodied Trichillum externumpunctatum was an abundant species in the pasture and sugarcane matrices. This species is generally found in pastures in Brazil (Flech- tmann et al. 1995; Koller et al. 1999; Aidar et al. 2000), and its high abundance in environments with elevated tempera- tures, such as pastures and sugarcane plantations, may be an outcome of a nidiication behavior (Alarcón et al. 2009) that difers from other endocoprids (Cambefort and Han- ski 1991). In this species, neither brood masses nor balls are prepared by the female, and after the feeding stage, the larva leaves the mass of faeces to pupate in the soil under- neath it, thus moving to a more humid environment (De Maria et al. 1999; Alarcón et al. 2009). The lower abundance and richness of dung beetles in most land uses exposes the severe impact of land-use changes on dung beetles and relects the contrast between the cerrado and the adjacent matrices. The diferences between the physical conditions of adjacent habitats can explain our results. For example, soil humidity and struc- ture play a key role in dung beetle reproduction, as these factors are essential for nest construction (Fincher 1973). Fig. 6 Non-metric multidimensional scaling ordination (NMDS) of dung beetles sampled in transects in landscapes composed of the Brazilian savanna, cerrado (fragment), and three diferent land uses (matrix) 966 J Insect Conserv (2016) 20:957–970 1 3 Moreover, the biodiversity of both adults and larvae of dung beetles depends closely on the presence of mammals, since their faeces and carcasses are used as resources (food and nests) by many species (Hanski and Cambefort 1991a, b). Although some mammals are able to use eucalypt plan- tations (Lyra-Jorge et al. 2010), this is not likely for higher- contrast matrices such as sugarcane. Considering that dung beetle abundance may be an indicator of the abun- dance of mammals (Andresen and Laurance 2007; Nichols et al. 2009), our results also indicate severe impacts of the eucalypt and sugarcane matrices on mammal abundance (Andresen and Laurance 2007; Nichols et al. 2009). Regarding dung-manipulation strategies, the higher pro- portion of paracoprids compared to the other guilds has also been found in others studies in the Neotropics (Lou- zada and Lopes 1997; Liberal et  al. 2011; Silva and Di Mare 2012). The higher abundance of this guild might be an outcome of a low competition rate (Hanski and Cam- befort 1991a, b) and changes regarding the usage of both land and faecal resources (Halfter and Edmonds 1982), allowing the occurrence of ecologically similar species and increasing the regional diversity of paracoprids (Louzada and Lopes 1997). Paracoprids were most abundant in the pasture matrix; this environment is more advantageous to them than to the other guilds because (1) endocoprids live inside faeces and are more sensitive to high temperatures in pasture, due to the acceleration of faecal drying (Klein 1989); (2) telecoprids roll away large faecal masses in a short time span, and this costs more energy per time than tunneling behavior (Krell et al. 2003). In pasture and sug- arcane matrices, the abundance of endocoprids was mainly due to Trichillum externumpunctatum, which has a diferent nidiication behavior (Alarcón et al. 2009) than other endo- coprids (Cambefort and Hanski 1991), allowing the larvae and pupae to develop in a consistently moist environment (De Maria et al. 1999; Alarcón et al. 2009). In landscapes where eucalypt was present, the abun- dance of all functional guilds was higher in the cerrado than in the matrix, whereas the patterns observed for other land uses difered depending on the guild. It is known that the presence of all guilds in an environment maximizes ecosystem functions (Slade et  al. 2007), as the presence of paracoprid and telecoprid species increases seed dis- persal, edaphic aeration, and the incorporation of organic matter in the soil. Furthermore, the combined efect of the endocoprids and paracoprids results in a synergistic pattern that facilitates faecal transference to the soil and stimulates microbial activity, with important consequences for soil carbon cycling (Menéndez et  al. 2016). Thus, it appears that the services provided by dung beetles are most impaired in eucalypt land uses. Although eucalypt planta- tions are structurally similar to cerrado fragments and may have a high rate of natural regeneration (Dodonov et  al. 2014), this land use largely consists of managed monocul- tures subject to the application of fertilizers and pesticides and periodic clear-cutting (FAO 2006). These features, as well as the high water demand and the release of allelo- pathic substances that are characteristic of this tree, have a severe impact on soil structure, which reduces the resil- ience and biodiversity of dung beetle communities (Lugo 1997). The NMDS ordination showed that edge communi- ties in eucalypt landscapes had an intermediate composi- tion between those in the cerrado and the adjacent matrix. Thus, while the eucalypt landscapes exhibit decreased abundance of all guilds, the species composition across the edge appears to change smoothly rather than abruptly. Such a pattern reveals that the system that causes less drastic changes in vegetation structure and remains part of the for- est cover may ofer conditions more favorable to dung bee- tles in communities located near to the native habitat micro- climate (Halfter and Matthews 1996; Halfter and Arellano 2002). The matrix may not be devoid of resources, and dif- ferent edge-related patterns may be evident depending on whether the resources present in the matrix supplement or complement those found in the cerrado. Supplemen- tary resources provide additional material to that present within the cerrado, whereas complementary resources are essential for the species/species group in question, but are unavailable in the cerrado. (Ries et  al. 2004). The euca- lypt matrix probably contains the same type of resources as the cerrado, and therefore, species composition at their interface is not likely to vary much, though abundance may change. Conversely, species composition may vary substan- tially when the resources present in the matrix difer from those in the cerrado. This may be particularly evident with structurally diferent habitats such as pastures and cerrado. Our expectations regarding edge inluence were only partially corroborated. The gradient model, indicat- ing edge inluence, was selected for abundance only in the pasture landscape. This outcome indicates that the variation in abundance is more gradual in this landscape despite the disruption of species composition between the pasture and the cerrado, and despite the negative inlu- ence of pasture on dung beetle abundance in communities located near the edge. This may relect not only a nega- tive efect of the pasture on the adjacent cerrado—result- ing, for example, from an altered microclimate (Dodo- nov et al. 2013)—but also an efect of the cerrado on the pasture matrix, whereby the cerrado edge creates more favorable conditions in the matrix. This latter phenom- enon has sometimes been called the‘forest efect’ and has been observed, for example, in areas disturbed by insect outbreaks (Franklin et al. 2015) and in agricultural areas adjacent to forest fragments (González et al. 2015). The forest efect may afect factors as diverse as vegetation 967J Insect Conserv (2016) 20:957–970 1 3 composition (Bueno and Lambí 2015), microclimate (Baker et al. 2014) and predatory insects (González et al. 2015), which can provide resources for mammals in afected areas, consequently afording resources for dung beetles. Unlike the patterns observed for dung beetle abundance, an edge inluence on species richness was never evident for any landscape, whether for the beetles as a whole or for the diferent guilds. A possible explanation for this can be that with the sampling efort varying according to habitat, the cumulative function of the number of species may have underestimated the richness in cerrado and overestimated it in the disturbed habitat, which may highlight the difer- ences between adjacent environments and hiding gradient patterns. However a weak or non-signiicant edge inluence on dung beetle diversity is commonly observed, even in studies with diferent sampling design (Durães et al. 2005; Feer 2008; Campbell et al. 2011), and species richness also seems to be scarcely afected by edges in the cerrado. This pattern may be partially due to the patchy and ephemeral nature of their resources (manure and carcasses), mak- ing these insects mobile and eicient in tracking those resources throughout the landscape (Roslin 2000). In addi- tion, similar to other savannas, the cerrado is a naturally patchy environment with alternating patches of greater or smaller woody plant cover (Wiegand et al. 2006; Gonçalves and Batalha 2011). Furthermore, small-sized cerrado mam- mals may not be afected by edges at the scale of this study (Di Napoli and Caceres 2012). Thus, the distribution of dung beetles in our study fragments may be suiciently het- erogeneous to preclude the detection of edge inluence on the number of species (Harper et al. 2005). Besides the fact that most of dung beetles in tropi- cal savannas are not host specialists (Spector and Ayzama 2003), the diferences in mammal communities between the diferent land uses (Lyra-Jorge et al. 2010; Martin et al. 2012) as well as the presence of the dung of generalist and edge-preferring mammals at the edge may aid in explain- ing our results. It must also be considered that dung beetles may use all of the studied matrices to some degree, albeit often with lower abundance, as shown by the results above. An edge inluence on species richness could be more evident if we were to consider more inhospitable matri- ces such as urban areas or highways (Noreika and Kotze 2012). Still, a lack of relationship between edge contrast and edge inluence has been observed for other variables in the cerrado, including vegetation height, canopy closure and plant litter biomass (Dodonov et al. 2013, 2016). The great diversity of this group of beetles results in a myriad of environmental and resource preferences as well as difer- ences in movement capabilities among species, leading to a variation in edge-related patterns among the species such that the loss of some species at the edges is compensated by other species (Barbero et  al. 1999; Peyras et  al. 2013; Figueiras et al. 2015). Finally, landscape features also play a key role in the detection of the edge inluence on organisms, especially in highly fragmented and heterogeneous landscapes (Ries et  al. 2004). One of the best-known landscape metrics to have an impact on edge inluence is habitat area, since small patches have higher densities of edge area (Fletcher et al. 2007; Banks-Leite et al. 2010). As dung beetles are sensitive to patch size (Feer and Hingrat 2005; Horgan 2007), area and edge efects interact synergistically in such a way that small patches may be unable to sustain species that avoid edges; hence a misdetection of the edge inluence (Ewers et al. 2007). Thus, the inclusion of larger fragments could have aided in the detection of edge inluence on spe- cies richness. However, considering that small remnants dominate highly fragmented regions such as Southeast Bra- zil, our results are representative of the patterns that may be observed in this region. In conclusion, we showed clear efects of diferent land uses on the abundance, richness and composition of dung beetles as a whole and of the diferent dung-manipulation strategies in an agricultural landscape containing cerrado fragments. We also demonstrated the occurrence of edge inluence on the abundance of this group, albeit only in the pasture matrix. Although edge inluence was not often observed for species richness, there were great diferences between the vegetation remnants and the adjacent land uses for both richness and abundance. Thus, anthropogenic land uses, including low-contrast ones such as eucalypt planta- tions, tend to decrease the abundance and richness of dung beetles, with possible consequences for several ecological processes including decomposition and nutrient cycling. These efects may extend into the cerrado remnants, decreasing their core area, the impacts being especially severe considering the high degree of fragmentation of this vegetation. Acknowledgments We thank Mateus Fernando de Souza for aid in several phases of the research, especially on species identiication; Sean Miki Hieda and Carlos Fonseca for ield work support; Prof. Fernando Vaz-de-Melo for aid in species identiication, and Megan King for proofreading the manuscript. 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