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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.

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 e

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 e

The Mediterranean Red List assessment is a review of the regional conservation status of approximately 6,000 species (amphibians, mammals, reptiles, birds, fishes, butterflies, dragonflies, beetles, corals and plants) according to the IUCN Red List Categories and Criteria. It identifies those species that are threatened with extinction at the regional level to guide appropriate conservation actions for improving their status. This report summarises the results for Mediterranean dung beetles. All the dung beetles that are endemic or nearly endemic to the Mediterranean region – 200 species – are included. The geographical scope is the Mediterranean region according to the Mediterranean Basin Biodiversity Hotspot (Mittermeier et al., 2004), with the exception of the Macaronesian islands, which have not been included in this study. Of the 644 species of dung beetles inhabiting the Mediterranean region, 200 (32%) have at least 75% of their distribution range within the borders of the region. The other 444 species, which occur over a wider area, were excluded from this assessment. Of the 200 species analysed, 150 are considered endemic as they cannot be found anywhere else in the world.

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.

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 (BMF) 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 BMF 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.

Correction to: Scientific Reports https://doi.org/10.1038/s41598-018-33241-0, published online 05 October 2018

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.

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.

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 its elimination in the faeces, would be half 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.

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.

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.

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.