Effects of different pastures management on dung beetle communities in a sub-mountainous landscape of central Italy: a multicomponent biodiversity and ecological process analysis

Dung beetles are an important group of insects in terms of diversity and biomass in grassland habitats in the Mediterranean Basin. Using dung during feeding and nesting they are linked to numerous ecosystem services dependent on dung degradation and burying. Dung removal from the pasture surface and its reincorporation into the soil supporting nutrient cycles improve the physical structure of the soil, reduce greenhouse gas emissions from dung and the livestock’s ecto and endoparasites and improve secondary seed dispersal and germination. Despite their ecological importance, dung beetles are globally threatened. Among the principal threats to dung beetles in the Mediterranean Basin changes in livestock grazing management is one of the most important. Indeed, in the last few decades, extensive livestock management has undergone a rapid process of modification. Italy has seen the progressive abandonment of traditional extensive grazing systems in favour of more intensive versions. This has led to a situation where marginal areas are abandoned, but more productive locations can suffer from overgrazing. Another relevant factor related to intensification is the use/abuse of veterinary medical products (VMPs). VMP molecules such as ivermectin are poorly metabolized by cattle and are voided as unchanged residues in faeces. These residues have been demonstrated to have negative sub-lethal effects and ultimate lethal consequences on non-target dung fauna and, particularly, dung beetles. Due to the potential impacts of these three factors (grazing abandonment, grazing extensification and grazing intensification) on dung beetle, the aims of this thesis was to analyze the effects of grazing intensity and the use of VMPs on dung beetle diversity and their ecological processes in the sub-mountainous landscape of Central Italy. Moreover, I investigated the relationships among some indices of “classic” diversity and functional diversity, and the relationships between these last and the ecological process (dung removal capacity). During this work 156.936 specimens belonging to 58 species were collected (3 Geotrupinae; 16 Scarabaeinae; 39 Aphodiinae). Our results report that an historical use of VMPs may affect negatively all the species of the community as shown by the absence of indicator species. It is likely that VMPs affect all the species by decreasing their abundance, with consequent loss of rare species, but maintaining the structure of the community. This is confirmed by the fact that the dung beetle composition between areas with use or not use of VMPs is different only for the rare species, whereas the common and dominant ones maintain a comparable composition. The loss of species, abundance and biomass are consistent with other studies, but unlike our results, some authors found an impact on Shannon diversity index. As probably different impacts depend on factors that have not been considered in our study, such as the frequency of treatment, the dosage, the type of molecules, the way of administration, the period of application and climatic conditions there is a high necessity to essay more in depth the usage of VMPs. From a functional standpoint, the use of VMPs leads to a loss of the number of functional roles (FD), even though the functional structure of the community was maintained, probably because the usage of VMPs do not affect specific functional traits, fostering the homogeneous distribution of the abundance of the functional roles into the functional space. Hence, in our region, VMPs use appears to indistinctly impacts all the dung beetle functional niches, with no reason that specific traits were more affected than others. Finally, the impact of VMPs use on dung beetle communities is reflected in the loss of about 70% of the dung burial capacity, which is of concern considering the possible over-accumulation of dung piles in the pastures. This result may be due to two mechanisms: a) alterations of dung beetle community attributes (abundance and biomass, number of species, number of functional niches) and b) intoxication of the dung beetles, making them unable to carry out their activities. Low grazing intensity can be considered one of the step of grazing extensification that leads progressively to a total abandonment. In our studies we found that even a simple reduction of grazing intensity implies negative effects on dung beetle community. This grazing extensification leads to a loss of alpha diversity (species richness, 1D and 2D) and in the number of favored species (indicator species). Moreover, we observed a shift in the community composition that fostered more opportunistic species (r-strategy reproduction) and those adopting particular behavioral strategies to avoid competition with other dung-feeder insects (saprophagous larvae or cleptoparasitim). Although our results are consistent with other studies, new surveys that consider more intervals of grazing intensity are needed, as dung beetle diversity appears to be very sensitive even to small differences in the availability of trophic resources. From a functional point of view, grazing extensification leads to a loss of functional diversity in terms of both functional richness and functional structure. Indeed, it is likely that even the loss of a little amount of trophic resource may act as a filter, allowing only species with particular functional traits to maintain viable populations in this area. The loss of large body size species, and the advantages for the opportunistic ones, which increase the functional redundancy of the community, seem to support these findings. Generally, the changes in the dung beetle community caused by grazing extensification, produced a loss of dung burial capacity of about 30-40% in the low grazing area compared to those with moderate grazing activity. From a management point of view, this result appears to be of little concern compared to the impact of VMPs use. Indeed, the dung burial capacity of the community occurring in the low grazing areas, seems to be proportional to the amount of dung produced by the cattle. Domestic grazing abandonment leads to a loss of species richness, total abundance and biomass, number of favored species (indicator species), loss of large body size beetles and loss of no nesting species. All these results are consistent with those obtained by other authors. However, the domestic grazing abandonment maintains a well-structured community, which is demonstrated by the high level of 1D and 2D that emphasize the importance of the wild fauna excrements to maintain a diverse assemblage. Generally, abandonment leads to the impoverishment of the communities where only medium sized beetles, which perform food relocation for nesting, can maintain viable populations. Moreover, a shift toward a fauna which prefer closed habitat was found, which might be indication of an incipient tree and shrub encroachment due to grazing abandonment. From a functional standpoint, grazing abandonment caused a loss in the number of functional roles (FD), but the functional structure was maintained because the abundances of each functional role are evenly distributed. This is probably due to a mechanism of limiting similarity triggered by the scarcity of resources. Furthermore, the functional uniqueness of abandoned sites, as showed by the FSpe measure, corroborates the idea that the loss of trophic resource act as a filter that impoverishes and changes the composition of the community. Compared with low and moderate grazing intensity sites, the community occurring in the abandoned areas showed a low dung burial performance that vary from about -27% to -47%. These results seem to be a consequence of the qualitative and quantitative changes in the community attributes. We found a robust correlation between species richness and FD, and between 1D and wFD, and this is in accord with other studies. Although several methodological or context dependent factor can interfere with this relationship (e.g. number of traits, types of traits, intensity and type of environmental disturb, number of species), we suggest that our results can be interpreted as a real absence of functional redundancy in the dung beetle community. This is because we selected the functional traits on biological basis, using a similar number of quantitative and qualitative traits, and tested this relationship for two dung beetle assemblages that suffered different environmental stressors. However, we would like to stress the usefulness of the functional diversity metrics for two reasons: firstly, some of them are little related with other measures and can provide complementary information (i.e. FEve and FSpe); and secondly, for some metrics, the correlation is context dependent (e.g. FEve). Hence, for every study that intends to evaluate the functional diversity, it is recommended to always test its relationships with classical biodiversity measures. While several studies suggest that functional diversity is more related to ecological processes than classical biodiversity metrics (e.g. species richness, total abundance, Shannon index etc.), we cannot generalize this statement. Indeed, the patterns of variation of functional diversity do not always follow the patterns of variation of the ecological processes. For example, ‘VMPs use areas’ and ‘abandoned areas’, have a well-developed functional structure, but they have a low capacity of dung burial compared with ‘VMPs free areas’ and ‘Moderate grazing intensity’ areas. Although more analyses are needed in order to evaluate the relative importance of each community variable on ecological process, we suggest to empirically evaluate this relationship than extrapolating it from community biodiversity patterns.