Nontoxic effects of thymol, carvacrol, cinnamaldehyde, and garlic oil on dung beetles: A potential alternative to ecotoxic anthelmintics.

The sustainability of the traditional extensive livestock sector will only be possible if healthy dung-decomposing insect communities are preserved. However, many current pharmaceutical anthelmintics are harmful to dung beetles, their presence can have a negative impact on biological systems. Phytochemical anthelmintics are an alternative to ecotoxic synthetic pharmaceutical anthelmintics, although ecotoxicological tests of their possible indirect effects on dung beetles are required to demonstrate their viability. In this study, the potential ecotoxicity of thymol, carvacrol, cinnamaldehyde and garlic oil (diallyl disulfide and diallyl trisulfide) were tested for the first time. Inhibition of antennal response was measured as a relevant parameter by obtaining relevant toxicity thresholds derived from concentration‒response curves, such as the IC50. All phytochemical compounds tested were demonstrated to be suitable alternative candidates to the highly ecotoxic compound ivermectin, considering their non-toxicity to nontarget organisms. Residues of the phytochemical antiparasitics found in cattle droppings were extremely low, even undetectable in the case of diallyl disulfide and diallyl trisulfide. Furthermore, our results showed that none of the phytochemical compounds have ecotoxic effects, even at extremely high concentrations, including those almost 1000 times higher than what is most likely to be found in dung susceptible to ingestion by dung beetles in the field. We can conclude that the four selected phytochemical compounds meet the requirements to be considered reliable alternatives to ecotoxic veterinary medicinal products, such as ivermectin.

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.

Assessing the functional relationship between dung beetle traits and dung removal, burial, and seedling emergence.

The relationship between biodiversity and ecosystem functioning is often assessed through trait diversity. However, the relationship between traits and functions is typically assumed but seldom tested. We analyze the relationship between dung beetle traits and three ecological functions: dung removal, dung burial, and seedling emergence. We set up a laboratory experiment using nine Scarabaeidae species (three endocoprids, four paracoprids, and two telecoprids). We placed a sexual pair of beetles in each experimental unit, together with a mixture of dung and seeds, and measured the amount of dung removed and buried, burial depth, and the number of emerged seedlings. Sixteen morphological traits related to dung removal and burial were measured in each individual. Results indicate that these traits were related to dung beetle performance in dung removal and burial. Most traits were positively related to dung removal, indicating the existence of a general trait syndrome associated with dung manipulation and digging capability. Dung exploitation strategies did not provide further explanatory power. Seedling emergence showed a negative but weak relationship with dung burial amount and depth and species identity. This implies that specific differences in dung-soil interface activity may be important in secondary seed dispersal by dung beetles.

Biomagnification and body distribution of ivermectin in dung beetles.

A terrestrial test system to investigate the biomagnification potential and tissue-specific distribution of ivermectin, a widely used parasiticide, in the non-target dung beetle Thorectes lusitanicus (Jekel) was developed and validated. Biomagnification kinetics of ivermectin in T. lusitanicus was investigated by following uptake, elimination, and distribution of the compound in dung beetles feeding on contaminated faeces. Results showed that ivermectin was biomagnified in adults of T. lusitanicus when exposed to non-lethal doses via food uptake. Ivermectin was quickly transferred from the gut to the haemolymph, generating a biomagnification factor (BMFk) three times higher in the haemolymph than in the gut after an uptake period of 12 days. The fat body appeared to exert a major role on the biomagnification of ivermectin in the insect body, showing a BMFk 1.6 times higher than in the haemolymph. The results of this study highlight that the biomagnification of ivermectin should be investigated from a global dung-based food web perspective and that the use of these antiparasitic substances should be monitored and controlled on a precautionary basis. Thus, we suggest that an additional effort be made in the development of standardised regulatory recommendations to guide biomagnification studies in terrestrial organisms, but also that it is necessary to adapt existing methods to assess the effects of such veterinary medical products.

Author Correction: First assessment of the comparative toxicity of ivermectin and moxidectin in adult dung beetles: Sub-lethal symptoms and pre-lethal consequences.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has been fixed in the paper.

First assessment of the comparative toxicity of ivermectin and moxidectin in adult dung beetles: Sub-lethal symptoms and pre-lethal consequences.

Among macrocyclic lactones (ML), ivermectin (IVM) and moxidectin (MOX) potentially affect all Ecdysozoan species, with dung beetles being particularly sensitive. The comparative effects of IVM and MOX on adult dung beetles were assessed for the first time to determine both the physiological sub-lethal symptoms and pre-lethal consequences. Inhibition of antennal response and ataxia were tested as two intuitive and ecologically relevant parameters by obtaining the lowest observed effect concentration (LOEC) values and interpolating other relevant toxicity thresholds derived from concentration-response curves (IC50, as the concentration of each ML where the antennal response is inhibited by half; and pLC50, as the quantity of ingested ML where partial paralysis was observed by half of treated individuals) from concentration-response curves. Both sub-lethal and pre-lethal symptoms obtained in this study coincided in that IVM was six times more toxic than MOX for adult dung beetles. Values of LOEC, IC50 and pLC50 obtained for IVM and MOX evaluated in an environmental context indicate that MOX, despite needing more time for tis elimination in the faeces, would be twice as harmful to dung beetles as IVM. This approach will be valuable to clarify the real impact of MLs on dung beetle health and to avoid the subsequent environmental consequences.

Spatial and temporal variations of aridity shape dung beetle assemblages towards the Sahara desert.

BACKGROUND: Assemblage responses to environmental gradients are key to understand the general principles behind the assembly and functioning of communities. The spatially and temporally uneven distribution of water availability in drylands creates strong aridity gradients. While the effects of spatial variations of aridity are relatively well known, the influence of the highly-unpredictable seasonal and inter-annual precipitations on dryland communities has been seldom addressed. AIMS: Here, we study the seasonal and inter-annual responses of dung beetle (Coleoptera, Scarabaeidae) communities to the variations of water availability along a semiarid region of the Mediterranean. METHODS: We surveyed a 400 km linear transect along a strong aridity gradient from the Mediterranean coast to the Sahara (Eastern Morocco), during four sampling campaigns: two in the wet season and two in the dry season. We measured species richness, abundance and evenness. Variations in community composition between sites, seasons and years were assessed through beta diversity partitioning of dissimiliarity metrics based on species occurrences and abundances. The effects of climate, soil, vegetation and dung availability were evaluated using Spearman-rank correlations, general linear regressions and partial least-squares generalized linear regressions for community structure, and non-metric multi-dimensional scaling, Permutational Analysis of Variance (PERMANOVA) and distance-based RDA variation partitioning for compositional variations. RESULTS: Dung beetle abundance and species richness showed large seasonal variations, but remained relatively similar between years. Indeed, aridity and its interaction with season and year were the strongest correlates of variations in species richness and composition. Increasing aridity resulted in decreasing species richness and an ordered replacement of species, namely the substitution of the Mediterranean fauna by desert assemblages dominated by saprophagous and generalist species both in space towards the Sahara and in the dry season. DISCUSSION: Our study shows that aridity determines composition in dung beetle communities, filtering species both in space and time. Besides the expected decrease in species richness, such environmental filtering promotes a shift towards generalist and saprophagous species in arid conditions, probably related to changes in resource quality along the transect and through the year. Our results highlight the importance of considering the effects of the highly-unpredictable seasonal and inter-annual variations in precipitation when studying dryland communities.

Ivermectin residues disrupt dung beetle diversity, soil properties and ecosystem functioning: An interdisciplinary field study.

Ivermectin is the most common endectocide used to control parasites affecting livestock. Short-term physiological and behavioural effects of ivermectin on dung beetles may have long-term consequences for beetle populations and ecosystem functioning. Long-term effects of the use of ivermectin can be estimated by comparing dung assemblages and ecosystem functions in areas with conventional ivermectin-treated livestock and environmentally similar areas in which livestock are not treated with veterinary medical products (organic farming). In this study, we investigated both short-term and long-term effects of the administration of ivermectin on the characteristics of dung beetle assemblages and the services they provided in a protected area (Doñana National Park, SW Spain). We examined short-term dung colonization, dwelling, relocation, and disaggregation rates and the associations between these processes and the key assemblage parameters of species richness, abundance, biomass and functional diversity. Furthermore, we analysed changes in soil physical-chemical properties and processes. Short-term differences were observed in the total amount of dung relocated by dung beetles at different colonization vs. emigration stages, suggesting that dung beetles in this area were affected by the recent treatments of livestock with ivermectin. Moreover, short-term effects could also be responsible for the significant differences in dung spreading rates between sites. Conventional use of ivermectin disrupted ecosystem functioning by affecting species richness, abundance and biomass. The decrease in diversity parameters was related to a reduction in the functional efficiency, which resulted in the long-term accumulation of dung on the ground and considerable changes in soil functionality.

Watch Out for Your Neighbor: Climbing onto Shrubs Is Related to Risk of Cannibalism in the Scorpion Buthus cf. occitanus.

The distribution and behavior of foraging animals usually imply a balance between resource availability and predation risk. In some predators such as scorpions, cannibalism constitutes an important mortality factor determining their ecology and behavior. Climbing on vegetation by scorpions has been related both to prey availability and to predation (cannibalism) risk. We tested different hypotheses proposed to explain climbing on vegetation by scorpions. We analyzed shrub climbing in Buthus cf. occitanus with regard to the following: a) better suitability of prey size for scorpions foraging on shrubs than on the ground, b) selection of shrub species with higher prey load, c) seasonal variations in prey availability on shrubs, and d) whether or not cannibalism risk on the ground increases the frequency of shrub climbing. Prey availability on shrubs was compared by estimating prey abundance in sticky traps placed in shrubs. A prey sample from shrubs was measured to compare prey size. Scorpions were sampled in six plots (50 m x 10 m) to estimate the proportion of individuals climbing on shrubs. Size difference and distance between individuals and their closest scorpion neighbor were measured to assess cannibalism risk. The results showed that mean prey size was two-fold larger on the ground. Selection of particular shrub species was not related to prey availability. Seasonal variations in the number of scorpions on shrubs were related to the number of active scorpions, but not with fluctuations in prey availability. Size differences between a scorpion and its nearest neighbor were positively related with a higher probability for a scorpion to climb onto a shrub when at a disadvantage, but distance was not significantly related. These results do not support hypotheses explaining shrub climbing based on resource availability. By contrast, our results provide evidence that shrub climbing is related to cannibalism risk.

Low doses of ivermectin cause sensory and locomotor disorders in dung beetles.

Ivermectin is a veterinary pharmaceutical generally used to control the ecto- and endoparasites of livestock, but its use has resulted in adverse effects on coprophilous insects, causing population decline and biodiversity loss. There is currently no information regarding the direct effects of ivermectin on dung beetle physiology and behaviour. Here, based on electroantennography and spontaneous muscle force tests, we show sub-lethal disorders caused by ivermectin in sensory and locomotor systems of Scarabaeus cicatricosus, a key dung beetle species in Mediterranean ecosystems. Our findings show that ivermectin decreases the olfactory and locomotor capacity of dung beetles, preventing them from performing basic biological activities. These effects are observed at concentrations lower than those usually measured in the dung of treated livestock. Taking into account that ivermectin acts on both glutamate-gated and GABA-gated chloride ion channels of nerve and muscle cells, we predict that ivermectin's effects at the physiological level could influence many members of the dung pat community. The results indicate that the decline of dung beetle populations could be related to the harmful effects of chemical contamination in the dung.

Effects of brood parasitism on host reproductive success: evidence from larval interactions among dung beetles.

This paper investigates the effect of brood parasitism in a dung beetle assemblage in an arid region of Spain. The study was conducted during the spring season (March-May 1994-1998) using mesh cylinders buried into the ground, filled with sand and with sheep dung on top. We quantified the proportion of nests containing larvae of parasitic beetles and their effect on host larvae survival. Experiments on the effect of parasitic larvae on host-larvae survival were conducted by placing scarab brood masses (raised from captive scarabs in the laboratory) in containers with and without aphodiid larvae. During the spring, dung desiccation is rapid, preventing aphodiids nesting in the dung, and forcing these species to adopt brood parasitism as a nesting strategy. Parasitic aphodiids were found in 12-47% of scarab nests of three species. The incidence of brood parasitization was positively related with the number of brood masses contained in the nests, being also higher in the most abundant species. Field data and experiments showed that brood parasites significantly reduced host larvae survival from 74.8% in non-parasitized nests to 8.8% in parasitized nests. Because different rates of nest parasitization and mortality were caused by parasites, brood parasitism had a differential effect on different host species. Thus, brood parasitism constitutes an important mortality factor reducing the reproductive success of the host species and potentially affecting the beetle abundance in the area.