Ecological relationships between coprophagous insects and livestock production: a review.

The ecological function played by the coprophagous insects is an important issue in livestock production contexts. The role of this fauna, specially dung beetles, provides benefits to both rangelands and production performance. This interaction has been studied and reported in many scientific articles, in very different places and with diverse production contexts. However, a comprehensive review of the relationship between coprophagous insects and livestock production is still lacking. We reviewed the research studies on this topic during the past five decades, with a focus in Scarabaeidae taxon and livestock production, in order to identify further research priorities. We analysed 435 research articles. The main results were: (I) studies were mostly located in temperate broadleaf forest biome, whereas arid environments were less studied; (II) Production practices impacts category was the most studied, for which the effects produced by antiparasitic products on the coprophagous insects (n = 93; 21% of total revised articles) was the topics with major number of articles. Followed was Biology category (n = 69; 16%), then in Ecosystem function category the most frequent studies were on dung removal (n = 40; 9%), whereas in the Ecosystem Services category the most frequent studies were on biological control (n = 28; 6%); (III) Australia, Mexico, Brazil, and United States were the countries with most research articles. We identified some knowledge gaps on relevant ecological functions of this fauna, in relation to benefits to livestock production. There is a need for future research on nutrient cycling, bioturbation, effects on primary production and vegetation diversity.

Linking functional group richness and ecosystem functions of dung beetles: an experimental quantification.

Dung beetles form an insect group that fulfils important functions in terrestrial ecosystems throughout the world. These include nutrient cycling through dung removal, soil bioturbation, plant growth, secondary seed dispersal and parasite control. We conducted field experiments at two sites in the northern hemisphere temperate region in which dung removal and secondary seed dispersal were assessed. Dung beetles were classified in three functional groups, depending on their size and dung manipulation method: dwellers, large and small tunnelers. Other soil inhabiting fauna were included as a fourth functional group. Dung removal and seed dispersal by each individual functional group and combinations thereof were estimated in exclusion experiments using different dung types. Dwellers were the most diverse and abundant group, but tunnelers were dominant in terms of biomass. All dung beetle functional groups had a clear preference for fresh dung. The ecosystem services in dung removal and secondary seed dispersal provided by dung beetles were significant and differed between functional groups. Although in absolute numbers more dwellers were found, large tunnelers were disproportionally important for dung burial and seed removal. In the absence of dung beetles, other soil inhabiting fauna, such as earthworms, partly took over the dung decomposing role of dung beetles while most dung was processed when all native functional groups were present. Our results, therefore, emphasize the need to conserve functionally complete dung ecosystems to maintain full ecosystem functioning.

Functional identity and diversity of animals predict ecosystem functioning better than species-based indices.

Drastic biodiversity declines have raised concerns about the deterioration of ecosystem functions and have motivated much recent research on the relationship between species diversity and ecosystem functioning. A functional trait framework has been proposed to improve the mechanistic understanding of this relationship, but this has rarely been tested for organisms other than plants. We analysed eight datasets, including five animal groups, to examine how well a trait-based approach, compared with a more traditional taxonomic approach, predicts seven ecosystem functions below- and above-ground. Trait-based indices consistently provided greater explanatory power than species richness or abundance. The frequency distributions of single or multiple traits in the community were the best predictors of ecosystem functioning. This implies that the ecosystem functions we investigated were underpinned by the combination of trait identities (i.e. single-trait indices) and trait complementarity (i.e. multi-trait indices) in the communities. Our study provides new insights into the general mechanisms that link biodiversity to ecosystem functioning in natural animal communities and suggests that the observed responses were due to the identity and dominance patterns of the trait composition rather than the number or abundance of species per se.

Density-dependent ecosystem service delivery under shifting temperatures by dung beetles.

Increases in the frequency and magnitude of suboptimal temperatures as a result of climate change are subjecting insects to unprecedented stresses. This may negatively affect their fitness and the efficiency of their ecosystem service provision. Dung beetles are ecosystem service providers: through feeding on and burying dung, they facilitate nutrient recycling, secondary seed dispersal, parasite control, soil bioturbation and dung decomposition. As such, prediction of how dung beetles respond to multiple anthropogenic environmental changes is critical for the conservation of ecosystem services. Here, we quantified ecosystem services via dung utilisation and dung ball production in three telecoprid species: Allogymnopleurus indigaceous, Scarabaeus zambezianus and Khepher prodigiosus. We examined ecosystem service efficiency factorially under different beetle densities towards different dung masses and under three temperature treatments (21 °C, 28 °C and 35 °C). Khepher prodigiosus, exhibited greatest dung utilisation efficiency overall across dung masses, compared to both S. zambezianus and A. indigaceous. Dung removal was exhibited under all the tested temperatures by all tested species, and therefore the sub-optimal temperatures employed here did not fully inhibit ecosystem service delivery. However, emergent effects among temperatures, beetle species and beetle density further affected removal efficiency: S. zambezianus and A. indigaceous utilisation increased with both warming and beetle density, whereas K. prodigiosus performance was less temperature- and density-dependent. Beetles also tended to exhibit positive density-dependence as dung supply increased. The numbers of dung balls produced differed across species, and increased with temperature and densities, with S. zambezianus producing significantly most balls overall. Our study provides novel evidence for differential density-dependent ecosystem service delivery among species across stressful temperature regimes and emergent effects for dung mass utilisation. This information is essential for biodiversity-ecosystem-function and is critical for the conservation of functionally efficacious species, with implications for natural capital conservation policy in rapidly changing environments.

Effects of Land-Use Change on the Community Structure of the Dung Beetle (Scarabaeinae) in an Altered Ecosystem in Southern Ecuador.

This study evaluated the effects of land-use change (L-UCH) on dung beetle community structure (Scarabaeinae) in a disturbed dry ecosystem in southern Ecuador. Five different L-UCH classes were analyzed by capturing the dung beetle species at each site using 120 pitfall traps in total. To determine dung beetle abundance and diversity at each L-UCH, a general linear model (GLM) and a redundancy analysis (RDA) were applied, which correlated environmental and edaphic conditions to the community structure. Furthermore, changes in dung-producing vertebrate fauna were examined, which varied significantly between the different L-UCH classes due to the specific anthropogenic use or level of ecosystem disturbance. The results indicated that soil organic matter, pH, potassium, and phosphorus (RDA: component 1), as well as temperature and altitude (RDA: component 2) significantly affect the abundance of beetles (GLM: p value < 0.001), besides the food availability (dung). The highest abundance and diversity (Simpson's index > 0.4, Shannon-Wiener index > 1.10) was found in highly disturbed sites, where soils were generally more compacted, but with a greater food supply due to the introduced farm animals. At highly disturbed sites, the species Canthon balteatus, Dichotomius problematicus, and Onthphagus confuses were found specifically, which makes them useful as bio-indicators for disturbed dry forest ecosystems in southern Ecuador.

Animal-Mediated Ecosystem Process Rates in Forests and Grasslands are Affected by Climatic Conditions and Land-Use Intensity.

Decomposition, vegetation regeneration, and biological control are essential ecosystem functions, and animals are involved in the underlying processes, such as dung removal, seed removal, herbivory, and predation. Despite evidence for declines of animal diversity and abundance due to climate change and land-use intensification, we poorly understand how animal-mediated processes respond to these global change drivers. We experimentally measured rates of four ecosystem processes in 134 grassland and 149 forest plots in Germany and tested their response to climatic conditions and land-use intensity, that is, grazing, mowing, and fertilization in grasslands and the proportion of harvested wood, non-natural trees, and deadwood origin in forests. For both climate and land use, we distinguished between short-term effects during the survey period and medium-term effects during the preceding years. Forests had significantly higher process rates than grasslands. In grasslands, the climatic effects on the process rates were similar or stronger than land-use effects, except for predation; land-use intensity negatively affected several process rates. In forests, the land-use effects were more pronounced than the climatic effects on all processes except for predation. The proportion of non-natural trees had the greatest impact on the process rates in forests. The proportion of harvested wood had negative effects, whereas the proportion of anthropogenic deadwood had positive effects on some processes. The effects of climatic conditions and land-use intensity on process rates mirror climatic and habitat effects on animal abundance, activity, and resource quality. Our study demonstrates that land-use changes and interventions affecting climatic conditions will have substantial impacts on animal-mediated ecosystem processes.

Exposure to low concentrations of pesticide stimulates ecological functioning in the dung beetle Onthophagus nuchicornis.

Body-size is an important trait for predicting how species contribute to ecosystem functions and respond to environmental stress. Using the dung beetle Onthophagus nuchicornis (Coleoptera: Scarabaeidae), we explored how variation in body-size affected ecosystem functioning (dung burial) and sensitivity to an environmental stressor (exposure to the veterinary anthelmintic ivermectin). We found that large beetles buried nearly 1.5-fold more dung than small beetles, but that mortality from exposure to a range of concentrations of ivermectin did not differ between large and small beetles. Unexpectedly, we found that exposure to low concentrations of ivermectin (0.01⁠-1 mg ivermectin per kg dung) stimulated dung burial in both small and large beetles. Our results provide evidence of ecological functioning hormesis stemming from exposure to low amounts of a chemical stressor that causes mortality at high doses.

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.

Efecto de la cobertura vegetal en escarabajos coprófagos (Coleoptera: Scarabaeinae) y sus funciones ecológicas en un bosque andino de Colombia / Effect of vegetation cover on dung beetles (Coleoptera: Scarabaeinae) and their ecological functions in an Andean forest of Colombia

Resumen Introducción: Los escarabajos coprófagos cumplen funciones importantes en los ecosistemas terrestres, pero las presiones antrópicas los afectan negativamente. Estos efectos están bien documentados en los bosques neotropicales de tierras bajas, pero se han estudiado poco en los bosques andinos. Objetivo: Evaluar cómo los atributos de los ensambles de escarabajos coprófagos y tres de sus funciones ecológicas difieren en tres tipos de cobertura vegetal, y determinar las relaciones entre atributos y funciones, y entre funciones. Métodos: Los escarabajos coprófagos se capturaron con trampas pitfall y se midieron las funciones ecológicas a través de un experimento de campo en la hacienda "El Ocaso" (Colombia), en tres tipos de cobertura vegetal: bosque secundario, bosque mixto y pastos para ganado (tres sitios independientes por cobertura). Los atributos del ensamble que se evaluaron fueron: abundancia, número de especies, biomasa y longitud corporal media ponderada; las funciones medidas fueron: remoción de estiércol, excavación del suelo y dispersión secundaria de semillas. Resultados: Se encontró que tanto los atributos del ensamble como las funciones ecológicas se vieron afectados negativamente en las coberturas vegetales más alteradas, particularmente en los pastos ganaderos. La mayoría de los atributos de ensamblaje se correlacionaron positivamente con las funciones; la excavación del suelo y la dispersión secundaria de semillas tuvieron una fuerte correlación positiva con la remoción de estiércol. Conclusiones: Los ensambles de escarabajos coprófagos juegan importantes funciones ecológicas y son sensibles a las alteraciones del ecosistema. Este estudio muestra cómo los escarabajos coprófagos y sus funciones se ven afectados negativamente cuando el bosque se transforma en pastizales para ganado en los ecosistemas forestales andinos poco estudiados y altamente fragmentados.

Abstract Introduction: Dung beetles perform important functions in terrestrial ecosystems, but anthropic pressures affect them negatively. These effects are well documented in neotropical lowland forests but have been studied little in Andean forests. Objective: To evaluate how the attributes of the dung beetle assemblages and three of their ecological functions differ in three types of vegetation cover, and to determine the relationships between attributes and functions, and among functions. Methods: Dung beetles were captured with pitfall traps, and ecological functions were measured through a field experiment in the farm "El Ocaso" (Colombia), in three types of vegetation cover: secondary forest, mixed forest and cattle pasture (three independent sites per cover). The assemblage attributes that were evaluated were abundance, number of species, biomass, and weighted mean body length; functions measured were dung removal, soil excavation, and secondary seed dispersal. Results: It was found that both the assemblage attributes and the ecological functions were negatively affected in the more disturbed vegetation covers, particularly in cattle pastures. Most of the assemblage attributes correlated positively with functions; soil excavation and secondary seed dispersal had a strong positive correlation with dung removal. Conclusions: Dung beetle assemblages play important ecological functions and they are sensitive to ecosystem disturbances. This study shows how dung beetles and their functions are affected negatively when forest is transformed to cattle pasture in the understudied and highly fragmented Andean forest ecosystems.

Lethal and Sublethal Effects of Ivermectin on Onthophagus landolti (Coleoptera: Scarabaeidae).

Previous work has documented toxic effects of ivermectin (IVM) on dung beetles from the Old World, but very little is known about this drug's effect on Neotropical dung beetles. Accordingly, we conducted a bioassay with dung spiked with IVM to assess its lethal and sublethal effects on the Neotropical dung beetle Onthophagus landolti Harold. The experimental design consisted of five treated groups G1, G2, G3, G4, and G5 receiving 0.001, 0.01, 0.1, 1.0, and 10 mg IVM/kg dung fresh weight, respectively, and two control groups (solvent control [CGA] and untreated control [CGU]). Adult survival and fecundity were measured throughout a 10-d period, and subsequent egg development and survival were monitored. Adult survival was only affected for treatment groups G4 and G5 groups (70 and 30%, respectively); groups G1, G2, G3 and both controls exhibited 100% survival. Fecundity was completely suppressed under treatment groups G4 and G5. Group G3 only had 1.7 and 2.1% brood mass production relative to CGA and CGU, respectively. Additionally, for groups G1 and G2 the proportion of adults emerging from brood masses was lower relative to CGA. Furthermore, development time for the second generation in groups G1 and G2 was 12.5% slower relative to control groups. Finally, dung removal by beetles from groups G3, G4, and G5 was significantly lower relative to control groups. In conclusion, toxic effects of IVM on O. landolti are associated mainly with reduced fecundity and lower dung-removal by adult beetles as well as reduced survival and slower development of offspring.