María de los Ángeles Marcos-García

Saproxylic beetles (Coleoptera) and hoverflies (Diptera: Syrphidae) from a Mediterranean forest: towards a better understanding of their biology for species conservation

This report represents the first integrative study on saproxylic Coleoptera and Diptera Syrphidae from a representative Mediterranean forest in Cabañeros National Park in Central Spain. We collected 107 beetles, representing 32 families, and 25 species of hoverfly. Two undescribed and numerous rare beetle species were recorded, as were four hoverflies considered to be threatened species in Europe. We compiled biological information for all of the taxa encountered and recorded new data on their feeding habits, breeding microsites, and known tree associations. We found that the saproxylic biodiversity in this National Park was characterized by a significant number of Central European and North African species. Our results on the saproxylic assemblage, comprising many rare and poorly known species, of a typical Mediterranean forest represent a first step toward improved understanding of the saproxylic community and establishing the basis for conservation strategies in this region.

The “dehesa”, a key ecosystem in maintaining the diversity of Mediterranean saproxylic insects (Coleoptera and Diptera: Syrphidae)

The “dehesa” is a traditional Iberian agrosilvopastoral ecosystem characterized by the presence of old scattered trees that are considered as “keystone-structures”, which favor the presence of a wide range of biodiversity. We show the high diversity of saproxylic beetles and syrphids (Diptera) in this ecosystem, including red-listed species. We analyzed whether saproxylic species distribution in the “dehesa” was affected by tree density per hectare, dominant tree species or vegetation coverage. Species diversity did not correlate with tree density; however, it was affected by tree species and shrub coverage but in a different way for each taxon. The highest beetle diversity was linked to Quercus pyrenaica, the most managed tree species, with eight indicator species. In contrast, Q. rotundifolia hosted more species of saproxylic syrphids. Regarding vegetation coverage, shrub coverage was the only variable that affected insect richness, again in a different way for both taxa. In contrast, beetle species composition was only affected by dominant tree species whereas syrphid species composition was not affected by tree species or shrub coverage. We concluded that the high diversity of saproxylic insects in the “dehesa” is related to its long history of agrosilvopastoral management, which has generated landscape heterogeneity and preserved old mature trees. However, the richness and composition of different taxa of insects respond in different ways to tree species and vegetation coverage. Consequently, conservation strategies should try to maintain traditional management, and different saproxylic taxa should be used to monitor the effect of management on saproxylic diversity.

Unravelling Darwin's entangled bank: architecture and robustness of mutualistic networks with multiple interaction types.

Trying to unravel Darwins entangled bank further, we describe the architecture of a network involving multiple forms of mutualism (pollination by animals, seed dispersal by birds and plant protection by ants) and evaluate whether this multi-network shows evidence of a structure that promotes robustness. We found that species differed strongly in their contributions to the organization of the multi-interaction network, and that only a few species contributed to the structuring of these patterns. Moreover, we observed that the multi-interaction networks did not enhance community robustness compared with each of the three independent mutualistic networks when analysed across a range of simulated scenarios of species extinction. By simulating the removal of highly interacting species, we observed that, overall, these species enhance network nestedness and robustness, but decrease modularity. We discuss how the organization of interlinked mutualistic networks may be essential for the maintenance of ecological communities, and therefore the long-term ecological and evolutionary dynamics of interactive, species-rich communities. We suggest that conserving these keystone mutualists and their interactions is crucial to the persistence of species-rich mutualistic assemblages, mainly because they support other species and shape the network organization.

Influence of tree hollow characteristics on the diversity of saproxylic insect guilds in Iberian Mediterranean woodlands

Saproxylic diversity assessment is a major goal for conservation strategies in woodlands and it should consider woodland composition and configuration at site and tree level as key modelling factors. However, in Mediterranean woodlands little is known about the relation with the environmental factors that structure their assemblages, especially those linked to tree hollow microhabitats. We assessed the diversity of Syrphidae (Diptera) and Coleoptera saproxylic guilds that co-occurred in tree hollows located in three different Iberian Mediterranean woodlands in the Cabañeros National Park (Spain). Furthermore, we evaluated how differences in tree hollow microenvironmental variables (understood as the physical and biotic characteristics of a hollow and tree individual) influenced saproxylic guild diversity both within and among woodland sites. We found that woodland sites that provided greater heterogeneity of trees and hollow microhabitats determined higher saproxylic guild diversity. Nevertheless, certain species or even complete guilds can be favoured in woodlands where some hollow microhabitats predominate as a consequence of historical tree management. In general, hollow volume was the main determining factor for saproxylic guild richness and abundance in woodland sites, and large hollow volume was usually related to higher diversity, which highlighted the importance of multi-habitat hollow trees. Moreover, saproxylic guilds also responded to other different microenvironmental variables, which indicated different ecological preferences among guilds. The conservation of saproxylic insects in Iberian Mediterranean areas must be addressed to protect woodland sites that provide high diversity and large numbers of tree hollow microhabitats, and practices to enhance microhabitat heterogeneity should even be encouraged.

Facilitation among Saproxylic Insects Inhabiting Tree Hollows in a Mediterranean Forest: The Case of Cetonids (Coleoptera: Cetoniidae) and Syrphids (Diptera: Syrphidae)

ABSTRACT Tree hollows offer an ideal niche for saproxylic insects in mature Mediterranean forests, where Diptera and Coleoptera are the richest groups. Co-occurrence is frequently observed among many species of both groups in these microhabitats, and some of these species have been considered to facilitate the presence of other species by acting as ecosystem engineers. One of the systems that is found in Mediterranean tree hollows is formed by cetonid (Coleoptera: Cetoniidae) and syrphid (Diptera: Syrphidae) larvae. Here, cetonid larvae feed on wood and litter and produce a substrate that is easier to decompose. To assess the possible role of these larvae as facilitating agents for the saproxylic guild, we studied whether the presence of saprophagous Syrphidae inside tree hollows is associated with the activity of cetonid larvae. Furthermore, in laboratory conditions, we tested whether cetonid larvae activity can improve the development and fitness of the saprophagous syrphid species. Our results show that “cetonid activity” was the variable that best explained the presence of saprophagous syrphid species in natural conditions. Myathropa florea (L., 1758) was one of the species most influenced by this activity. The laboratory experiment gave similar results, demonstrating that an enriched substrate with Cetonia aurataeformis Curti, 1913 larval feces improves syrphid larval growth rate and fitness of adults (measured as longer wing length) of M. florea.

Bacteria associated with Copestylum (Diptera, Syrphidae) larvae and their cactus host Isolatocereus dumortieri

We describe the gut bacterial diversity inhabiting two saprophagous syrphids and their breeding substrate (decayed tissues of the columnar cactus Isolatocereus dumortieri). We analyzed the gut microbiota of Copestylum latum (scooping larvae that feed on decayed cactus tissues) and Copestylum limbipenne (whose larvae can also feed on semiliquid tissues) using molecular techniques. DNA was extracted from larval guts and cactus tissues. The V1-V3 region of the 16S rRNA genes was amplified and sequenced. A total of 31079 sequences were obtained. The main findings are: C. limbipenne is dominated by several Enterobacteriaceae, including putative nitrogen-fixing genera and pectinolitic species and some denitrifying species, whereas in C. latum unclassified Gammaproteobacteria predominate. Decayed tissues have a dominant lactic acid bacterial community. The bacterial communities were more similar between larval species than between each larva and its breeding substrate. The results suggest that the gut bacterial community in these insects is not strongly affected by diet and must be dependent on other factors, such as vertical transmission, evolutionary history and host innate immunity.

Landscape configurational heterogeneity by small-scale agriculture, not crop diversity, maintains pollinators and plant reproduction in western Europe

Agricultural intensification is one of the main causes for the current biodiversity crisis. While reversing habitat loss on agricultural land is challenging, increasing the farmland configurational heterogeneity (higher field border density) and farmland compositional heterogeneity (higher crop diversity) has been proposed to counteract some habitat loss. Here, we tested whether increased farmland configurational and compositional heterogeneity promote wild pollinators and plant reproduction in 229 landscapes located in four major western European agricultural regions. High-field border density consistently increased wild bee abundance and seed set of radish (Raphanus sativus), probably through enhanced connectivity. In particular, we demonstrate the importance of crop–crop borders for pollinator movement as an additional experiment showed higher transfer of a pollen analogue along crop–crop borders than across fields or along semi-natural crop borders. By contrast, high crop diversity reduced bee abundance, probably due to an increase of crop types with particularly intensive management. This highlights the importance of crop identity when higher crop diversity is promoted. Our results show that small-scale agricultural systems can boost pollinators and plant reproduction. Agri-environmental policies should therefore aim to halt and reverse the current trend of increasing field sizes and to reduce the amount of crop types with particularly intensive management.

Association patterns in saproxylic insect networks in three Iberian Mediterranean woodlands and their resistance to microhabitat loss.

The assessment of the relationship between species diversity, species interactions and environmental characteristics is indispensable for understanding network architecture and ecological distribution in complex networks. Saproxylic insect communities inhabiting tree hollow microhabitats within Mediterranean woodlands are highly dependent on woodland configuration and on microhabitat supply they harbor, so can be studied under the network analysis perspective. We assessed the differences in interacting patterns according to woodland site, and analysed the importance of functional species in modelling network architecture. We then evaluated their implications for saproxylic assemblages’ persistence, through simulations of three possible scenarios of loss of tree hollow microhabitat. Tree hollow-saproxylic insect networks per woodland site presented a significant nested pattern. Those woodlands with higher complexity of tree individuals and tree hollow microhabitats also housed higher species/interactions diversity and complexity of saproxylic networks, and exhibited a higher degree of nestedness, suggesting that a higher woodland complexity positively influences saproxylic diversity and interaction complexity, thus determining higher degree of nestedness. Moreover, the number of insects acting as key interconnectors (nodes falling into the core region, using core/periphery tests) was similar among woodland sites, but the species identity varied on each. Such differences in insect core composition among woodland sites suggest the functional role they depict at woodland scale. Tree hollows acting as core corresponded with large tree hollows near the ground and simultaneously housing various breeding microsites, whereas core insects were species mediating relevant ecological interactions within saproxylic communities, e.g. predation, competitive or facilitation interactions. Differences in network patterns and tree hollow characteristics among woodland sites clearly defined different sensitivity to microhabitat loss, and higher saproxylic diversity and woodland complexity showed positive relation with robustness. These results highlight that woodland complexity goes hand in hand with biotic and ecological complexity of saproxylic networks, and together exhibited positive effects on network robustness.

Bacteria and Hoverflies (Diptera: Syrphidae) in Tree Hollows From the Iberian Mediterranean Forest

Abstract Saproxylic insect communities inhabiting tree hollows in Mediterranean forests depend on a combination of physical characteristics and interactions occurring between community member species. Despite the need to preserve these organisms, little is known about their interrelationships, in particular those relationships between saproxylic insects and microbiota occurring in these microhabitats. In tree hollows of Quercus rotundifolia Lamark that hold water and contain dead leaves, abundant microbial populations can be found. Developing on them are the larvae of Mallota dusmeti Andréu, 1926 (Diptera: Syrphidae), a vulnerable species (IUCN category: Marcos-García and Quinto 2011). This study provides the first data on the microbiota living inside the gut of the larvae of M. dusmeti, as well as the microbiota in the hollow where these larvae develop. Bacteria were identified by amplification and partial sequencing of the V1–V3 regions and the complete nucleotide sequence of 16S rRNA genes. We found eight species of bacteria living in tree hollows and three species in the gut of M. dusmeti larvae: Bacillus cereus, Bacillus toyonensis, and Lysinibacillus sphaericus. The filter-feeding mechanism characteristic of M. dusmeti larvae is selective in enabling ingestion of bacteria only above 2.1 µm in diameter.

Correction to ‘Unravelling Darwin's entangled bank: architecture and robustness of mutualistic networks with multiple interaction types’

[ Proc. R. Soc. B 283 , 20161564 (Published 23 November 2016). ([doi:10.1098/rspb.2016.1564][2])][2] Field data on ants were supported by a CONACYT grant (no. 903579). P.R.G. and J.N.T. were supported by FAPESP and NSF, respectively. L.P.M. was supported by FAPESP (2015/12956-7). R.O.-P. was