Brice Giffard

Plant apparency, an overlooked driver of associational resistance to insect herbivory

Summary Herbivore regulation is one of the services provided by plant diversity in terrestrial ecosystems. It has been suggested that tree diversity decreases insect herbivory in forests, but recent studies have reported opposite patterns, indicating that tree diversity can trigger associational resistance or susceptibility. The mechanisms underlying the tree diversity–resistance relationship thus remain a matter of debate. We assessed insect herbivory on pedunculate oak saplings (Quercus robur) in a large-scale experiment in which we manipulated tree diversity and identity by mixing oaks, birch and pine species. Tree diversity at the plot scale had no effect on damage due to leaf chewers, but abundance of leaf miners decreased with increasing tree diversity. The magnitude of this associational resistance increased with host dilution, consistent with the ‘resource concentration hypothesis’. At a smaller scale, we estimated tree apparency as the difference in total height between focal oak saplings and their nearest neighbouring trees. Levels of oak infestation with leaf miners decreased significantly with decreasing tree apparency. As the probability of having taller neighbours increased with tree diversity, notably due to the increase in the proportion of faster growing nonhost trees, such as birches and pines, tree apparency may be seen as a ‘hidden’, sampling effect of tree diversity. Synthesis. These findings suggest that greater host dilution and lower tree apparency contribute to associational resistance in young trees. They also highlight the importance of taking plant size into account as a covariate, to avoid misleading interpretations about the biodiversity–resistance relationship.

Genetic Diversity Increases Insect Herbivory on Oak Saplings

A growing body of evidence from community genetics studies suggests that ecosystem functions supported by plant species richness can also be provided by genetic diversity within plant species. This is not yet true for the diversity-resistance relationship as it is still unclear whether damage by insect herbivores responds to genetic diversity in host plant populations. We developed a manipulative field experiment based on a synthetic community approach, with 15 mixtures of one to four oak (Quercus robur) half-sib families. We quantified genetic diversity at the plot level by genotyping all oak saplings and assessed overall damage caused by ectophagous and endophagous herbivores along a gradient of increasing genetic diversity. Damage due to ectophagous herbivores increased with the genetic diversity in oak sapling populations as a result of higher levels of damage in mixtures than in monocultures for all families (complementarity effect) rather than because of the presence of more susceptible oak genotypes in mixtures (selection effect). Assemblages of different oak genotypes would benefit polyphagous herbivores via improved host patch location, spill over among neighbouring saplings and diet mixing. By contrast, genetic diversity was a poor predictor of the abundance of endophagous herbivores, which increased with individual sapling apparency. Plant genetic diversity may not provide sufficient functional contrast to prevent tree sapling colonization by specialist herbivores while enhancing the foraging of generalist herbivores. Long term studies are nevertheless required to test whether the effect of genetic diversity on herbivory change with the ontogeny of trees and local adaptation of specialist herbivores.

Dispersal capacity of Monochamus galloprovincialis, the European vector of the pine wood nematode, on flight mills

The pine wood nematode (Bursaphelenchus xylophilus), which causes the symptoms of pine wilt disease, is recognized worldwide as a major forest pest. It was introduced into Portugal in 1999. It is transmitted between trees almost exclusively by longhorn beetles of the genus Monochamus, including, in particular, M. galloprovincialis (Coleoptera: Cerambycidae) in maritime pine forests. Accurate estimates of the flight capacity of this insect vector are required if we are to understand and predict the spread of pine wilt disease in Europe. Using computer‐linked flight mills, we evaluated the distance flown, the flight probability and speed of M. galloprovincialis throughout adulthood and investigated the effects of age, sex and body weight on these flight performances, which are proxies for dispersal capacity. The within‐population variability of flight performance in M. galloprovincialis was high, with a mean distance of 16 km flown over the lifetime of the beetle. Age and body weight had a significant positive effect on flight capacity, but there was no difference in performance between males and females. These findings have important implications for managing the spread of the pine wood nematode in European forests.

Bird predation enhances tree seedling resistance to insect herbivores in contrasting forest habitats

According to the associational resistance hypothesis, neighbouring plants are expected to influence both the insect herbivore communities and their natural enemies. However, this has rarely been tested for the effects of canopy trees on herbivory of seedlings. One possible mechanism responsible for associational resistance is the indirect impact of natural enemies on insect herbivory, such as insectivorous birds. But it remains unclear to what extent such trophic cascades are influenced by the composition of plant associations (i.e. identity of ‘associated’ plants). Here, we compared the effect of bird exclusion on insect leaf damage for seedlings of three broadleaved tree species in three different forest habitats. Exclusion of insectivorous birds affected insect herbivory in a species-specific manner: leaf damage increased on Betula pendula seedlings whereas bird exclusion had no effect for two oaks (Quercus robur and Q. ilex). Forest habitat influenced both the extent of insect herbivory and the effect of bird exclusion. Broadleaved seedlings had lower overall leaf damage within pine plantations than within broadleaved stands, consistent with the resource concentration hypothesis. The indirect effect of bird exclusion on leaf damage was only significant in pine plantations, but not in exotic and native broadleaved woodlands. Our results support the enemies hypothesis, which predicts that the effects of insectivorous birds on insect herbivory on seedlings are greater beneath non-congeneric canopy trees. Although bird species richness and abundance were greater in broadleaved woodlands, birds were unable to regulate insect herbivory on seedlings in forests of more closely related tree species.

Ecosystem Services from Small Forest Patches in Agricultural Landscapes

In Europe, like in many temperate lowlands worldwide, forest has a long history of fragmentation and land use change. In many places, forest landscapes consist of patches of different quality, age, size and isolation, embedded in a more or less intensively managed agricultural matrix. As potential biodiversity islets, small forest patches (SFP) may deliver several crucial ecosystem services to human society, but they receive little attention compared to large, relatively intact forest patches. Beyond their role as a biodiversity reservoir, SFP provide important in situ services such as timber and wild food (game, edible plants and mushrooms) production. At the landscape scale, SFP may enhance the crop production via physical (obstacle against wind and floods) and biological (sources of pollinators and natural enemies) regulation, but may, on the other hand, also be involved in the spread of infectious diseases. Depending on their geographic location, SFP can also greatly influence the water cycle and contribute to supply high-quality water to agriculture and people. Globally, SFP are important carbon sinks and are involved in nutrient cycles, thus play a role in climate change mitigation. Cultural services are more related to landscape values than to SFP per se, but the latter may contribute to the construction of community identity. We conclude that SFP, as local biodiversity hotspots in degraded landscapes, have the potential to deliver a wide range of ecosystem services and may even be crucial for the ecological intensification of agro-ecosystems. There is thus an urgent need to increase our knowledge about the relationships between biodiversity and ecosystem services delivered by these SFP in agricultural landscapes.

Plant neighbours mediate bird predation effects on arthropod abundance and herbivory

Tritrophic interactions among plants, herbivores and predators are expected to be influenced by the surrounding vegetation. Neighbouring plants can influence focal plant colonisation by herbivorous insects and the foraging behaviour of natural enemies, such as insectivorous birds. The aim of the experiment was to disentangle the interactive effects of neighbouring plants and avian predation on arthropod abundance and insect leaf damage in oak tree seedlings, using exclusion cages and vegetation removal. The presence or removal of surrounding herbaceous vegetation differentially mediated top‐down effects of insectivorous birds on distinct arthropod guilds and herbivore damage in seedlings. Avian predation reduced sawfly larval abundance regardless of the presence of plant neighbours; lepidopteran larval abundance only when plant neighbours were removed; and spider abundance only when plant neighbours were left intact. The removal of plant neighbours increased prey accessibility for foraging insectivorous birds and decreased chewer damage on seedlings. The density of concealed‐feeder insects (leaf miners) increased with plant neighbour removal and when seedlings were less damaged by chewer guild, suggesting intraguild competition. These results highlight the strong indirect effects of neighbouring vegetation on tritrophic interactions involving a focal plant species, its associated herbivores and the upper trophic level of predators.

Potential effects of climate warming on the survivorship of adult Monochamus galloprovincialis

Ecologists have explored widely the consequences of climate change on insect species distribution and fitness. Although most studies have assessed the effect of increasing mean temperatures on individual performances, the response to temporal thermal variations, including the magnitude and frequency of extreme temperatures, has often been overlooked. In the present study, we hypothesized that insect performances increase with increasing mean temperatures but decrease under more variable thermal conditions. We used a manipulative experiment to compare the longevity and weight variation of Monochamus galloprovincialis (Coleoptera: Cerambycidae) under three climatic conditions in which the mean and variance of daily temperatures were both controlled. This insect is vector of the invasive nematode, Bursapheluncus xylophilus, which is the causal agent of the pine wilt disease, one of the major threats to pine forests in Europe. Our results showed that an increase of 2.5 °C in average temperature had no effect on the survivorship and weight variations of the beetle. By contrast, larger fluctuating variations of temperature across year resulted in significantly lower longevity, whereas weight remained unchanged. The results of the present study suggest that the effect of global warming on the survival of M. galloprovincialis is likely to be driven by change in temperature stability rather than by change in mean temperature.

Effects of soil erosion on agro-ecosystem services and soil functions: A multidisciplinary study in nineteen organically farmed European and Turkish vineyards

This multidisciplinary research work evaluated the effects of soil erosion on grape yield and quality and on different soil functions, namely water and nutrient supply, carbon sequestration, organic matter recycling, and soil biodiversity, with the aim to understand the causes of soil malfunctioning and work out a proper strategy of soil remediation. Degraded areas in nineteen organically farmed European and Turkish vineyards resulted in producing significantly lower amounts of grapes and excessive concentrations of sugar. Plants suffered from decreased water nutrition, due to shallower rooting depth, compaction, and reduced available water capacity, lower chemical fertility, as total nitrogen and cation exchange capacity, and higher concentration of carbonates. Carbon storage and organic matter recycling were also depressed. The general trend of soil enzyme activity mainly followed organic matter stock. Specific enzymatic activities suggested that in degraded soils, alongside a general slowdown in organic matter cycling, there was a greater reduction in decomposition capacity of the most recalcitrant forms. The abundance of Acari Oribatida and Collembola resulted the most sensitive indicator of soil degradation among the considered microarthropods. No clear difference in overall microbial richness and evenness were observed. All indices were relatively high and indicative of rich occurrence of many and rare microbial species. Dice cluster analyses indicated slight qualitative differences in Eubacterial and fungal community compositions in rhizosphere soil and roots in degraded soils. This multidisciplinary study indicates that the loss of soil fertility caused by excessive earth movement before planting, or accelerated erosion, mainly affects water nutrition and chemical fertility. Biological soil fertility is also reduced, in particular the ability of biota to decompose organic matter, while biodiversity is less affected, probably because of the organic management. Therefore, the restoration of the eroded soils requires site-specific and intensive treatments, including accurately chosen organic matrices for fertilization, privileging the most easily decomposable. Restoring soil fertility in depth, however, remain an open question, which needs further investigation.

Ecology for Sustainable and Multifunctional Agriculture

The Green Revolution and the introduction of chemical fertilizers, synthetic pesticides and high yield crops had enabled to increase food production in the mid and late 20th. The benefits of this agricultural intensification have however reached their limits since yields are no longer increasing for many crops, negative externalities on the environment and human health are now recognized and economic inequality between farmers have increased. Agroecology has been proposed to secure food supply with fewer or lower negative environmental and social impacts than intensive agriculture. Agroecology principles are based on the recognition that biodiversity in agroecosystems can provide more than only food, fibre and timber. Hence, biodiversity and its associated functions, such as pollination, pest control, and mechanisms that maintain or improve soil fertility, may improve production efficiency and sustainability of agroecosystems. Although appealing, promoting ecological-based agricultural production is not straightforward since agroecosystems are socio-ecosystems with complex interactions between the ecological and social systems that act at different spatial and temporal scales. To be operational, agroecology thus requires understanding the relationships between biodiversity, functions and management, as well as to take into account the links between agriculture, ecology and the society. Here we review current knowledge on (i) the effect of landscape context on biodiversity and ecosystem functions and (ii) trophic and non-trophic interactions in ecological networks in agroecosystems. In particular, many insights have been made these two previous decades on (i) the interacting effects of management and landscape characteristics on biodiversity, (ii) the crucial role of plant diversity in delivering multiple services and (iii) the variety of ecological belowground mechanisms determining soil fertility in interaction with aboveground processes. However, we also pinpointed the absence of consensus on the effects of landscape heterogeneity on biodiversity and the need for a better mechanistic understanding of the effects of landscape and agricultural variables on farmland food webs and related services. We end by proposing new research avenues to fill knowledge gaps and implement agroecological principles within operational management strategies.

Linking macrodetritivore distribution to desiccation resistance in small forest fragments embedded in agricultural landscapes in Europe

PurposeMost of the agricultural landscape in Europe, and elsewhere, consists of mosaics with scattered fragments of semi-natural habitat like small forest fragments. Mutual interactions between forest fragments and agricultural areas influence ecosystem processes such as nutrient cycling, a process strongly mediated by the macrodetritivore community, which is however, poorly studied. We investigated macrodetritivore distribution patterns at local and landscape-level and used a key functional trait (desiccation resistance) to gain mechanistic insights of the putative drivers.MethodsMacrodetritivores were sampled in forest edges-centres of 224 European forest fragments across 14 landscapes opposing in land use intensity. We used a multilevel analysis of variance to assess the relative contribution of different spatial scales in explaining activity-density and Shannon-diversity of woodlice and millipedes, together with a model-based analysis of the multivariate activity-density data testing the effect on species composition. Secondly, we tested if desiccation resistance of macrodetritivores varied across communities at different spatial scales using linear mixed effect models.ResultsForest edge-centre and landscape use intensity determined activity-density and community composition of macrodetritivores in forest fragments, while fragment characteristics like size and continuity were relatively unimportant. Forest edges and higher intensity landscapes supported higher activity-density of macrodetritivores and determined species composition. Forest edges sustained woodlouse communities dominated by more drought tolerant species.ConclusionsLandscape use intensity and forest edges are main drivers in macrodetritivore distribution in forest fragments with desiccation resistance a good predictor of macrodetritivore distribution. Key functional traits can help us to predict changes in community structure in changing landscapes.