Dung removal increases under higher dung beetle functional diversity regardless of grazing intensification.

Dung removal by macrofauna such as dung beetles is an important process for nutrient cycling in pasturelands. Intensification of farming practices generally reduces species and functional diversity of terrestrial invertebrates, which may negatively affect ecosystem services. Here, we investigate the effects of cattle-grazing intensification on dung removal by dung beetles in field experiments replicated in 38 pastures around the world. Within each study site, we measured dung removal in pastures managed with low- and high-intensity regimes to assess between-regime differences in dung beetle diversity and dung removal, whilst also considering climate and regional variations. The impacts of intensification were heterogeneous, either diminishing or increasing dung beetle species richness, functional diversity, and dung removal rates. The effects of beetle diversity on dung removal were more variable across sites than within sites. Dung removal increased with species richness across sites, while functional diversity consistently enhanced dung removal within sites, independently of cattle grazing intensity or climate. Our findings indicate that, despite intensified cattle stocking rates, ecosystem services related to decomposition and nutrient cycling can be maintained when a functionally diverse dung beetle community inhabits the human-modified landscape.

A trait-based framework for dung beetle functional ecology.

Traits are key for understanding the environmental responses and ecological roles of organisms. Trait approaches to functional ecology are well established for plants, whereas consistent frameworks for animal groups are less developed. Here we suggest a framework for the study of the functional ecology of animals from a trait-based response-effect approach, using dung beetles as model system. Dung beetles are a key group of decomposers that are important for many ecosystem processes. The lack of a trait-based framework tailored to this group has limited the use of traits in dung beetle functional ecology. We review which dung beetle traits respond to the environment and affect ecosystem processes, covering the wide range of spatial, temporal and biological scales at which they are involved. Dung beetles show trait-based responses to variation in temperature, water, soil properties, trophic resources, light, vegetation structure, competition, predation and parasitism. Dung beetles' influence on ecosystem processes includes trait-mediated effects on nutrient cycling, bioturbation, plant growth, seed dispersal, other dung-based organisms and parasite transmission, as well as some cases of pollination and predation. We identify 66 dung beetle traits that are either response or effect traits, or both, pertaining to six main categories: morphology, feeding, reproduction, physiology, activity and movement. Several traits pertain to more than one category, in particular dung relocation behaviour during nesting or feeding. We also identify 136 trait-response and 77 trait-effect relationships in dung beetles. No response to environmental stressors nor effect over ecological processes were related with traits of a single category. This highlights the interrelationship between the traits shaping body-plans, the multi-functionality of traits, and their role linking responses to the environment and effects on the ecosystem. Despite current developments in dung beetle functional ecology, many knowledge gaps remain, and there are biases towards certain traits, functions, taxonomic groups and regions. Our framework provides the foundations for the thorough development of trait-based dung beetle ecology. It also serves as an example framework for other taxa.

Integrating thermal tolerance, water balance and morphology: An experimental study on dung beetles.

The impacts of extreme and rising mean temperatures due to climate change can pose significant physiological challenges for insects. An integrated approach that focuses on mechanisms of body temperature regulation, water balance and morphology may help to unravel the functional traits underpinning thermoregulation strategies and the most relevant trade-offs between temperature and water balance regulation. Here, we focused on four species of tunneler dung beetles as important providers of ecosystem services. In this experimental research, we first quantified two traits related to desiccation resistance and tolerance via experimental tests, and subsequently defined two levels of resistance and tolerance (i.e. low and high) according to significant differences among species. Second, we identified morphological traits correlated with water balance strategies, and we found that desiccation resistance and tolerance increased with small relative size of spiracles and wings. High levels of desiccation tolerance were also correlated with small body mass. Third, by integrating thermal tolerance with functional traits based on desiccation resistance and desiccation tolerance, we found that the species with the highest survival rates under elevated temperatures (Euoniticellus fulvus) was characterized by low desiccation resistance and high desiccation tolerance. Our results suggest shared physiological and morphological responses to temperature and desiccation, with potential conflicts between the need to regulate heat and water balance. They also highlighted the sensitivity of a large species such as Geotrupes stercorarius to warm and arid conditions with potential implications for its geographic distribution and the provisioning of ecosystem services under a climate change scenario.

Physiological, morphological and ecological traits drive desiccation resistance in north temperate dung beetles.

BACKGROUND: Increasing temperatures and changes in precipitation patterns threaten the existence of many organisms. It is therefore informative to identify the functional traits that underlie differences in desiccation resistance to understand the response of different species to changes in water availability resulting from climate change. We used adult dung beetles as model species due to their importance to ecosystem services. We investigated: (i) the effect of physiological (water loss rate, water loss tolerance, body water content), morphological (body mass) and ecological (nesting behaviour) traits on desiccation resistance; (ii) the role of phylogenetic relatedness in the above associations; and, (iii) whether relatively large or small individuals within a species have similar desiccation resistance and whether these responses are consistent across species. RESULTS: Desiccation resistance decreased with increasing water loss rate and increased with increasing water loss tolerance (i.e. proportion of initial water content lost at the time of death). A lack of consistent correlation between these traits due to phylogenetic relatedness suggests that the relationship is not determined by a shared evolutionary history. The advantage of a large body size in favouring desiccation resistance depended on the nesting behaviour of the dung beetles. In rollers (one species), large body sizes increased desiccation resistance, while in tunnelers and dwellers, desiccation resistance seemed not to be dependent on body mass. The phylogenetic correlation between desiccation resistance and nesting strategies was significant. Within each species, large individuals showed greater resistance to desiccation, and these responses were consistent across species. CONCLUSIONS: Resistance to desiccation was explained mainly by the dung beetles' ability to reduce water loss rate (avoidance) and to tolerate water loss (tolerance). A reduction in water availability may impose a selection pressure on body size that varies based on nesting strategies, even though these responses may be phylogenetically constrained. Changes in water availability are more likely to affect dweller species, and hence the ecosystem services they provide.

Dung beetles as drivers of ecosystem multifunctionality: Are response and effect traits interwoven?

Rapid biodiversity loss has emphasized the need to understand how biodiversity affects the provisioning of ecological functions. Of particular interest are species and communities with versatile impacts on multiple parts of the environment, linking processes in the biosphere, lithosphere, and atmosphere to human interests in the anthroposphere (in this case, cattle farming). In this study, we examine the role of a specific group of insects - beetles feeding on cattle dung - on multiple ecological functions spanning these spheres (dung removal, soil nutrient content and greenhouse gas emissions). We ask whether the same traits which make species prone to extinction (i.e. response traits) may also affect their functional efficiency (as effect traits). To establish the link between response and effect traits, we first evaluated whether two traits (body mass and nesting strategy, the latter categorized as tunnelers or dwellers) affected the probability of a species being threatened. We then tested for a relationship between these traits and ecosystem functioning. Across Scandinavian dung beetle species, 75% of tunnelers and 30% of dwellers are classified as threatened. Hence, nesting strategy significantly affects the probability of a species being threatened, and constitutes a response trait. Effect traits varied with the ecological function investigated: density-specific dung removal was influenced by both nesting strategy and body mass, whereas methane emissions varied with body mass and nutrient recycling with nesting strategy. Our findings suggest that among Scandinavian dung beetles, nesting strategy is both a response and an effect trait, with tunnelers being more efficient in providing several ecological functions and also being more sensitive to extinction. Consequently, functionally important tunneler species have suffered disproportionate declines, and species not threatened today may be at risk of becoming so in the near future. This linkage between effect and response traits aggravates the consequences of ongoing biodiversity loss.

Greenhouse gas emissions from dung pats vary with dung beetle species and with assemblage composition.

Cattle farming is a major source of greenhouse gases (GHGs). Recent research suggests that GHG fluxes from dung pats could be affected by biotic interactions involving dung beetles. Whether and how these effects vary among beetle species and with assemblage composition is yet to be established. To examine the link between GHGs and different dung beetle species assemblages, we used a closed chamber system to measure fluxes of carbon dioxide (CO2), methane (CH4) and nitrous oxide (N2O) from cattle dung pats. Targeting a total of four dung beetle species (a pat-dwelling species, a roller of dung balls, a large and a small tunnelling species), we ran six experimental treatments (four monospecific and two mixed) and two controls (one with dung but without beetles, and one with neither dung nor beetles). In this setting, the overall presence of beetles significantly affected the gas fluxes, but different species contributed unequally to GHG emissions. When compared to the control with dung, we detected an overall reduction in the total cumulative CO2 flux from all treatments with beetles and a reduction in N2O flux from the treatments with the three most abundant dung beetle species. These reductions can be seen as beneficial ecosystem services. Nonetheless, we also observed a disservice provided by the large tunneler, Copris lunaris, which significantly increased the CH4 flux-an effect potentially traceable to the species' nesting strategy involving the construction of large brood balls. When fluxes were summed into CO2-equivalents across individual GHG compounds, dung with beetles proved to emit less GHGs than did beetle-free dung, with the mix of the three most abundant species providing the highest reduction (-32%). As the mix of multiple species proved the most effective in reducing CO2-equivalents, the conservation of diverse assemblages of dung beetles emerges as a priority in agro-pastoral ecosystems.

Ecological functions provided by dung beetles are interlinked across space and time: evidence from 15 N isotope tracing.

Maintaining multiple ecological functions ("multifunctionality") is crucial to sustain viable ecosystems. To date most studies on biodiversity-ecosystem functioning (BEF) have focused on single or few ecological functions and services. However, there is a critical need to evaluate how species and species assemblages affect multiple processes at the same time, and how these functions are interconnected. Dung beetles represent excellent model organisms because they are key contributors to several ecosystem functions. Using a novel method based on the application of 15 N-enriched dung in a mesocosm field experiment, we assessed the role of dung beetles in regulating multiple aspects of nutrient cycling in alpine pastures over appropriate spatial (up to a soil depth of 20 cm) and temporal (up to 1 yr after dung application) scales. 15 N isotope tracing allowed the evaluation of multiple interrelated ecosystem functions responsible for the cycling of dung-derived nitrogen (DDN) in the soil and vegetation. We also resolved the role of functional group identity and the importance of interactions among co-occurring species for sustaining multiple functions by focusing on two different dung beetle nesting strategies (tunnelers and dwellers). Species interactions were studied by contrasting mixed-species to single-species assemblages, and asking whether the former performed multiple functions better than the latter. Dung beetles influenced at least seven ecological functions by facilitating dung removal, transport of DDN into the soil, microbial ammonification and nitrification processes, uptake of DDN by plants, herbage growth, and changes in botanical composition. Tunnelers and dwellers were found to be similarly efficient for most functions, with differences based on the spatial and temporal scales over which the functions operated. Although mixed-species assemblages seemed to perform better than single-species, this outcome may be dependent on the context. Most importantly though, the different functions were found to be interconnected sequentially as reveled by analyzing 15 N content in dung, soil and vegetation. Taken together, our current findings offer strong support for the contention that the link between biodiversity and ecosystem functions should be examined not function by function, but in terms of understanding multiple functions and how they interact with each other.

The effects of body mass on dung removal efficiency in dung beetles.

Understanding of the role of body mass in structural-functional relationships is pressing, particularly because species losses often occur non-randomly with respect to body size. Our study examined the effects of dung beetle body mass on dung removal at two levels. First, we used the lab experiment to evaluate the efficiency of eight dung beetle species belonging to two functional groups (tunnelers, dwellers) on dung removal. Second, the same species employed in the lab were used in field mesocosms to examine the effects of the two functional groups on dung removal maintaining realistic differences in the total body mass between tunneler and dweller assemblages. Furthermore, the experimental assemblages contained one and four species within each functional group, so the effect of body mass heterogeneity was examined. We used a statistical approach (offset method) which took into account a priori constraints due to the study design allowing us to analyse the effect of larger species in mesocosm style experiments. Body size played a crucial role in dung removal: large beetles were more efficient than small ones and the percentage of removed dung increased with higher body mass heterogeneity. Tunnelers were more efficient than dwellers over both short and long time periods (one month and one year). Significant effects of dwellers were found only after one year. Moreover, our study showed that not including the body mass as an offset in the model resulted in sometimes different results, as the offset expresses dung removal independently of the body mass. This approach confirmed that body size is likely a pivotal factor controlling dung removal efficiency at multiple levels, from single species to overall dung beetle assemblages. Even though other specific traits should be examined, this study has begun to address the consequences of losing individuals with specific traits that are especially sensitive to perturbations.

Pastoral practices to reverse shrub encroachment of sub-alpine grasslands: dung beetles (coleoptera, scarabaeoidea) respond more quickly than vegetation.

In recent decades, pastoral abandonment has produced profound ecological changes in the Alps. In particular, the reduction in grazing has led to extensive shrub encroachment of semi-natural grasslands, which may represent a threat to open habitat biodiversity. To reverse shrub encroachment, we assessed short-term effects of two different pastoral practices on vegetation and dung beetles (Coleoptera, Scarabaeoidea). Strategic placement of mineral mix supplements (MMS) and arrangement of temporary night camp areas (TNCA) for cattle were carried out during summer 2011 in the Val Troncea Natural Park, north-western Italian Alps. In 2012, one year after treatment, a reduction in shrub cover and an increase in bare ground cover around MMS sites was detected. A more intense effect was detected within TNCA through increases in forage pastoral value, and in the cover and height of the herbaceous layer. Immediately after treatment, changes in dung beetle diversity (total abundance, species richness, Shannon diversity, taxonomic and functional diversity) showed a limited disturbance effect caused by high cattle density. In contrast, dung beetle diversity significantly increased one year later both at MMS and TNCA sites, with a stronger effect within TNCA. Multivariate Regression Trees and associated Indicator Value analyses showed that some ecologically relevant dung beetle species preferred areas deprived of shrub vegetation. Our main conclusions are: i) TNCA are more effective than MMS in terms of changes to vegetation and dung beetles, ii) dung beetles respond more quickly than vegetation to pastoral practices, and iii) the main driver of the rapid response by dung beetles is the removal of shrubs. The resulting increase in dung beetle abundance and diversity, which are largely responsible for grassland ecosystem functioning, may have a positive effect on meso-eutrophic grassland restoration. Shrub encroachment in the Alps may therefore be reversed, and restoration of grassland enhanced, by using appropriate pastoral practices.