Final Report Summary - BACCARA (Biodiversity and climate change, a risk analysis)
Based on a thorough analysis of forest inventories, rapid distribution shifts in tree species elevational optimum have been detected suggesting a fast and strong impact of climate change on tree species distribution and performance, which would be stronger for species already at the limit of their natural range. On the other hand, the functional diversity of tree assemblages shows a remarkable homeostasis across elevational and latitudinal gradients. With the review of the literature and the combination of data collected on many elevation gradients during the project, key processes and mechanisms underlying response of tree communities to climate change have been identified. First, individual tree species responses to climate change seem to be species-specific and often unpredictable. Second, responses to climate change differ between adults and juveniles so a well-balanced demographic structure of tree populations can mitigate negative impacts. Third positive species interactions involving facilitation of juveniles by established adults are important, particularly at range edge, so mixed forests are more likely to buffer negative impacts on key species than monospecific ones.
The analysis of past records of damage in forests indicates that climate change generally promotes pestilence in forest but not for all species of pests and pathogens. Drought is likely to increase damage by defoliators, foliar pathogens, bark beetles and endophytic fungi but may reduce the impact of root rot pathogens. Damage can be partly contained by a higher activity of insect natural enemies under warmer conditions, although this has been shown only for ectoparasitoids or parasitoids of ectophagous insect herbivores. Some plant defenses such as leaf toughness significantly increase with elevation, i.e. lower temperatures. A literature review on 61 different species (32 insects and 29 fungi) from European forests showed that increased temperature is directly associated with overwhelmingly positive response by insect pests while the trend is less clear in the case of pathogens. New empirical data from more than 40 altitudinal gradients, in several mountain areas of Europe, indicate that fungal and insect assemblages tend to simplify with altitude suggesting a potential increase in pest and pathogen damage with increasing temperatures. They also revealed either neutral or positive effect of increasing temperatures on insect herbivory on four main European tree species.
Analyses of European forest inventory data showed that mixed forests are on average 24 % more productive than monospecific stands and revealed a positive relationship between tree species richness and wood production. Extensive simulations with tree succession models have confirmed that tree species richness and functional diversity promote productivity in European temperate forests. The positive diversity - productivity relationship is likely to persist under climate change. Meta-analyses of scientific literature and data from manipulative experiments clearly demonstrate a positive effect of tree species diversity on resistance against specialist insect herbivores but not against polyphagous pests. Higher dilution, lower apparency and higher phylogenetic contrast of focal tree intermixed with non-host trees mainly explain such associational resistance.
The combined analysis of main results obtained in BACCARA revealed that it seems possible to predict the vulnerability to the biotic and abiotic factors involved in or amplified by climate change of the main European tree species on the basis of their functional traits. Multicriteria decision analyses also proved to be a promising tool to help foresters to integrate ecological and socio-economic issues in order to make a decision about converting mono-species into mixed-species forests.
Project context and objectives:
A considerable number of studies are being published on the possible effects of climate change on forest productivity. They suggest that global positive response of forest productivity to raising CO2 and temperatures may be impeded by large diebacks due to extreme climatic events such as severe droughts. These studies often dealt with large scale modelling to predict global forest response to climate change or, on the other hand, with possible changes in single tree species growth. However, they overlooked the response of the whole tree species community to climate change which is probably the most relevant scale to meet forest managers' expectations. Changes in the growth of individual tree species might affect biotic interactions, including competition, herbivory and symbiosis, leading to shifts in the species dominance. Together with single-tree species fitness, these interactions may determine which species will persist, go extinct or migrate to assemble new communities. These new tree species assemblages may in turn drive changes in forest productivity. Indeed, there is an increasing body of evidence to support the view that biomass production can increase with herbaceous plant species richness or diversity but results are less consistent in more complex ecosystems such as forests.
The main objective of BACCARA is therefore to develop tools allowing forest managers and policy makers to evaluate risk of European forest biodiversity loss under climate change and subsequent decrease in forest ecosystem productivity. The principle of the project is to construct a three-dimensional risk assessment model linking climate change, functional diversity, and forest productivity through a three step process:
1. effects of climate change on forest biodiversity are evaluated through better understanding of the influence of climatic conditions on the ecological processes that shape assemblages of forest tree species and associated insect, fungus and mycorrhizae species;
2. relationships between forest biodiversity and functioning are deciphered through better understanding of the role of forest species richness and composition on biomass production;
3. the information is eventually aggregated to predict the risk of forest productivity loss, considered as a function of climate change probability (hazard), susceptibility of forest to climate change according to its diversity (vulnerability), and effect of forest diversity on biomass productivity (exposure).
Project results:
Based on a thorough analysis of forest inventories, several studies have detected rapid distribution shifts in tree species altitudinal optimum thus suggesting a fast and strong impact of climate change on tree species distribution and performance, which would be stronger for species already at the limit of their natural range.
A translocation experiment of beech seedlings along an elevation gradient showed negative effects of the soil biota community on European beech survival. However, these negative effects decreased with elevation and disappeared in samples from the highest altitude. This is the first study to show variability in interactions between plants and the soil biota community across an elevation gradient. Many micro-organisms with rapid proliferation rates may have triggered the negative effects observed. For instance, Fagus sylvatica seedlings are known to host soil fungi which are responsible for root and collar rot symptoms. Hence, the trend observed was probably the consequence of a decrease in the soil pathogen pressure on F. sylvatica with increase in elevation. This suggests that global warming might enhance soil pathogen and then reduce the survival of some tree species.
A literature review of mechanisms underlying response of tree communities to climate change was undertaken. It highlighted that tree species have a high level of plasticity and genetic variation for phenological traits that could allow populations first to rapidly respond and second to adapt to new conditions. However, there are many uncertainties about the potential for acclimation to climate change (bud dormancy release for instance). Indeed, some studies suggest that this level of plasticity could be insufficient to adjust to expected climate change. Climate warming may increase the relative importance of chilling temperature in the timing of tree flushing in the next decades, which could alter the reaction norms to temperature. Global climate change is also projected to produce longer and more frequent droughts, which have the potential to trigger widespread tree die-off. Recently, several studies characterised the cavitation resistance on a broad range of species and reported a high level of variation between species, suggesting a species-specific response to increased drought severity. Ongoing climate change is therefore expected to have important impacts on tree species, for instance climate change will affect tree species distribution, but also species abundance and tree-population structure (i.e. size-distribution) within the entire species distribution. However, this review revealed the lack of understanding of the processes that drives climate related large scale pattern of species distribution. It is in particular necessary to better account for tree demography. Indeed, species distribution, species abundance and tree-population structure are inherently population level problems that should be analysed with a demographic framework. For instance a demographic analysis may allow identifying locations with positive population growth, where births are greater than deaths, and locations with negative population growth. This is clearly key to understand and define the species distribution edge, how and why species range boundaries will change but also how and why much more fine population characteristics such as the abundance of the species, its size or age structure, and it spatial structure will change throughout its entire distribution. The review further presents the state of knowledge of climate effect on three key demographic rates, growth, recruitment and survival. The overall pattern is a positive response of tree growth to increase in temperature and water availability. However, very few studies have explored how temperature and precipitation, or climate and light (crucial for competition) or climate and CO2 were interacting to control tree growth. Our understanding of recruitment response to climate is thus much more limited than for growth. The few studies documenting directly the response of fecundity, germination, or seedling growth and survival to climate have generally shown that tree recruitment was limited by low temperature and by water stress. Despite its great importance for forest dynamics the response of mortality to climate has been extremely poorly documented. Nevertheless, several studies have documented that climatic variables such as drought and frost were increasing tree mortality.
In line with the need to take into account tree demography to better understand the response of tree species to climate constraints, a thorough review of the literature was carried out on key demographic traits. The final data used for the analyses of tree responses to climate change included a total of 331 records: 144 for growth, 44 for recruitment, 98 for survival and 45 for abundance. Most studies reported a decreased growth, survival and recruitment for most of the 24 tree species in response to past climate change. In contrast, abundance was found to increase in most cases, mostly due to northward and upward range expansion. Phenological features such as leaf production and reproduction were in general found to take place earlier in the year in agreement with previous reviews. A small but significant fraction of studies reported no changes for certain species and response variables. Using these four traits for grouping of species according to their responses to climate change rendered three groups of eight species each. The grouping was highly consistent, with a perfect match after 500 iterations. In the three groupings most species exhibited a reduced growth and survival as a consequence of climate change. Differences among groups were mostly due to different responses in terms of abundance and regeneration. All species in group 1, with Picea abies as indicator species and many species from riparian and very humid sites (most of them short living), were the least vulnerable, exhibiting an increased abundance and regeneration. Group 3, the most vulnerable one, characterised by Abies alba and several pine and oak species and dominated by Gymnosperms, exhibited a decreased regeneration. Group 2, characterised by Quercus ilex was somewhat intermediate, with moderate decreases in abundance and little change in regeneration. Then 13 functional and life history traits were documented for the 24 European tree species. These traits altogether allowed separating three distinct groups of species. The grouping of the tree species exhibited a good agreement (100 % of matching) with the grouping with the 4 demographic traits. The main life traits explaining the separation between the three groups of European tree species were the drought tolerance and the wood density.
Another, empirical study tackled the effect of climate conditions on the assemblages of tree species. The study was conducted on seven elevation gradients, from southern Spain to northern Sweden. Overall, species richness was higher for seedlings than for adults. This might be a consequence of seedlings colonising broader ranges of habitat conditions than the adults due to their small size and the spatial scale of resource variation. As a result, species richness does not seem to be compromised in the near future, at least due to increases in temperature, with the exception of sites where species richness in mature trees surpassed that of the seedlings at the highest temperatures, meaning that future richness could be reduced to climate change. Functional diversity was positively related to species richness in most sites, indicating that trait values are similar among species. In these sites, functional redundancy may buffer against the impact of climate change if species losses take place, because if one species gets extinct, functionally similar species can reduce the loss of functional diversity. However, in the Mediterranean sites a low a number of species was translated into high functional diversity. This is because the species present strong dissimilarities among traits. There species loss may have then serious consequences for functional diversity. When considering all sites and transects together, functional diversity was increasing with increasing temperatures. This means that in sites predicted to experience harsher conditions in the future (i.e. a decrease in productivity), the role of biodiversity on productivity will be more important. In other words if communities in those sites loose a species, the decrease in productivity will be on average stronger.
Predicting climate-driven changes in plant distribution is crucial for biodiversity conservation and management under recent climate change. Climate warming is expected to induce movement of species upslope and towards higher latitudes. However, the mechanisms and physiological processes behind the altitudinal and latitudinal distribution range of a tree species are complex and depend on each tree species features and vary over ontogenetic stages. We investigated the altitudinal distribution differences between juvenile and adult individuals of seven major European tree species along elevational transects covering a wide latitudinal range from southern Spain (37 degrees N) to northern Sweden (67 degrees N). By comparing juvenile and adult distributions (shifts on the optimum position and the range limits) we assessed the response of species to present climate conditions in relation to previous conditions that prevailed when adults were established. Mean temperature increased by 0.86 degrees Celsius on average at our sites during the last decade compared with previous 30-year period. Only one of the species studied, Abies alba, matched the expected predictions under the observed warming, with a maximum abundance of juveniles at higher altitudes than adults. Three species, Fagus sylvatica, Picea abies and Pinus sylvestris, showed an opposite pattern while for other three species, such as Quercus ilex, Acer pseudoplatanus and Quercus petraea, we were not able to detect changes in distribution. These findings are in contrast with theoretical predictions and show that tree responses to climate change are complex and are obscured not only by other environmental factors but also by internal processes related to ontogeny and demography.
With the review of the literature and the combination of data collected on many elevation gradients during the project, we have been able to identify key processes and mechanisms underlying response of tree communities to climate change. First, individual tree species responses to climate change seem to be idiosyncratic, i.e. unpredictable. Second, responses to climate change differ from adults and juveniles so a well-balanced demographic structure of tree populations can mitigate negative impacts. Third, positive species interactions involving facilitation of juveniles by established adults are important at limit range, both in elevation and latitude, so mixed forests are more likely to buffer negative impacts on key species than monospecific ones. Fourth, functional diversity of tree assemblages was assessed over elevational and latitudinal gradients showing a remarkable homeostasis, which is in contrast to the observed decrease in taxonomic diversity and species richness at increased elevation and latitudes.
At the beginning of the project, a theoretical review has been conducted to propose several mechanisms of response to climate change by pests and natural enemies of herbivores. It indicates that the direct effects on the herbivorous insect will be generally positive as a result of increased winter survival, faster development rates, and sometimes increased number of generations per year. Furthermore, some insect herbivores are likely to benefit from increased frequency of stressful events for plants. Insects that suffer from constitutive plant defences would tend to be favoured when conditions promote increased plant growth and associated declines in secondary metabolism. Insects that exploit young, nutritionally favourable foliage may be sensitive to climatically driven changes at the start of the growing season and to temperatures that influence the relative rates of leaf maturation and insect development after budburst. The nature of physiological controls on plant vs. insect phenology will influence the extent to which plant and insect phenology remains coupled under climate change. Increased activity in arthropod natural enemies could lead to increased strength of top-down control on the herbivorous insect. However, the magnitude of the effect will depend on attack strategy of predators and type of parasitism (endo versus ecto). Pathogens are likely to increase their infection rate under increased humidity and temperature. When forest pest outbreaks will occur within current distribution limits, we might expect shorter delays before negative feedbacks from natural enemies can act on population density. But outbreaks may well also occur outside range limits. In most cases, range limits tend to be a belt of recurrent colonisation and extinction events rather than a precise border. It is possible that many new outbreaks outside of the generally accepted range edge fall within this belt. The width of the belt would be defined by the dispersal potential of the species, including rare long-distance events. Climate change, however, may have an effect on dispersal per se and thus indirectly start outbreaks outside the range whenever conditions are suitable for insect herbivore performance. Climate-matching models frequently identify regions that seem suitable but are presently unoccupied - presumably because of dispersal limitation. Probably, the extent of such suitable but unoccupied regions is increasing under climate warming, which will increase the probability of outbreaks.
A first meta-analysis of the scientific literature was carried out to evaluate the effect of drought on forest pest and pathogen damage. The literature search yielded 100 comparisons of forest pest and disease damage on water stressed vs. unstressed trees, derived from 40 publications and reports that were published between 1975 and 2010. Overall water stress resulted in higher forest pest and disease damage. The type of trophic substrate used by forest pest and pathogens had a highly significant effect on the difference in damage between water stressed and unstressed trees. For pest insects and pathogens, the drought effect differed between the primary (those which can attack healthy trees) and the secondary agents (those which can only attack stressed trees). Primary damaging agents living on foliar organs caused higher damage in water stressed trees. Drought had negative effects on damage caused by primary agents developing on woody organs but significantly increased damage caused by secondary agents developing on woody organs. These results clearly indicate that the effect of water stress on the level of damage by forest pests and pathogens depends more on the type of substrate they use than on their feeding guild. We also tested the effect of water stress severity on level of damage for each functional group of forest pests and pathogens separately. We observed no significant effect of any water severity variables on level of damage in water stressed trees for any primary damaging agent. On the contrary, the effect of water stress severity significantly affected the level of damage caused by secondary agents living in woody organs. The variable best explaining damage variation was the ratio between observed predawn leaf water potential in stressed trees and the species - specific index of drought tolerance (P50). The level of damage increased linearly with this ratio. A threshold value of 30 % was detected below which damage in water stressed trees may be lower than in unstressed trees (negative effect size) whereas damage were consistently higher in stressed trees with predawn leaf water potential higher than 30 % of P50 (tree having a high native state of embolism). Drought is then likely to increase damage by defoliators, foliar pathogens, bark beetles and endophytic fungi but may reduce the impact of root rot pathogens.
A second meta-analysis was performed to test the effects of climate change on the top-down control of insect herbivores by insect parasitoids. Considering that elevation gradients can be used as analogues for global warming, we carried out meta-analyses of 27 correlations between parasitoid richness and elevation and 140 correlations between parasitism rate and elevation in natural and semi-natural environments. We also explored various covariates that may explain the observed responses. Both parasitism rates and parasitoid species richness significantly decreased with increasing elevation. The decrease was greater for ectoparasitoids and parasitoids of ectophagous insects than for endoparasitoids and parasitoids of endophagous hosts, possibly because these latter are better protected from adverse and extreme climatic conditions occurring at higher elevations. Although our results suggest an increase of parasitism with increasing temperature, other factors regulating herbivorous insects have to be considered before concluding that climate warming will lead to a decrease in pest density.
A third meta-analysis was carried out to evaluate the likely effects of climate change on the bottom-up regulation of insect damage, i.e. via plant defenses. We used again elevation gradients as analogues of temperature gradients. We also tested the effect of three covariates on the relationship between plant chemical defenses and altitude. First, we divided plant species into herbaceous and woody plants (including shrubs). Second, we divided plant chemicals into flavonoids and non-flavonoids secondary metabolites because flavonoids-based compounds can as well be involved in UV protection, or freezing tolerance in plants. Third, we distinguished between measures taken on reproductive (flowers, seeds, fruits) or vegetative organs of the plants (leaves, branches, trunks). Overall, we detected a significant increase in plant physical defense traits and flavonoids with elevation. Particularly, leaf toughness and flavonoids in the reproductive organs were increasing with elevation whereas we found no effect of elevation on other types of defenses (non-flavonoids in general and flavonoids in vegetative organs). These results suggest that, contrary to classical predictions, a reduction in herbivory pressure in harsher environments does not forcedly lead to a decrease in plant defenses. Along with climate selecting for physical and chemical protective traits, herbivores should also be expected to select for higher defense at high elevations. At low elevation, low defense may also be selected because species have fast growth rate and a high capacity to recover after damage. Indeed, high growth rate confers a competitive advantage against slower growing species with higher defense. Plant species from high elevation may have developed tougher leaves as an adaptation to severe climatic conditions, but this may indirectly confer increased resistance to herbivores. This suggests that selective forces of abiotic conditions (e.g. cold hardiness) might be stronger than biotic ones (e.g. resistance to herbivores) along elevation gradients, but this might be organ-specific depending on the trait analysed.
A fourth literature review on 61 different species (32 insects and 29 fungi) from European forests showed that increased temperature is directly associated with overwhelmingly positive response by insect pests while the trend is less clear in the case of pathogens. We collected 90 cases involving 61 different species (32 insects and 29 pathogens) from European forests for which data were available about the effect of climate-associated driver such as elevated temperatures, drought, storm and fire on their abundance or damage. The most abundant tree species in Europe were considered according to ICP Forest (2005) and enlarged to other tree species for which there was information available. Six tree genera were particularly concerned (Betula, Fagus, Picea, Pinus, Populus, Quercus) but several pests / pathogens were polyphagous on conifer and broadleaved trees. Increased temperature is directly associated with overwhelmingly positive response by insect pests. The trends are less clear in the case of pathogens, with relatively few cases of responses reported, and in most cases without known underlying mechanisms. Diplodia pinea and Gremmeniella abietina are benefiting from the temperature increase whereas Crumenulopsis sororia, Melampsora larici-populina, and Phloeosporella padi are negatively affected. Other frost-sensitive fungi, such as Phytophthora spp., may also benefit from the increase of temperature especially in winter. Increased frequency and intensity of drought is indirectly associated with damage by pests and pathogens, acting mainly through changes in the host plant traits and in the soil conditions. In contrast to their responses to temperature, insects appear to respond more equivocally to drought, with a similar number of cases of positive and negative responses. The responses of pathogens to drought vary as well, but those cases for which responses are known tend to be primarily via host plants (indirect) and, notably, positive, in contrast to those of insects. Responses of insects to increased fire frequency are rather poorly documented. A number of pathogen species, on the other hand, show a positive response indirectly mediated by an increase in host susceptibility or availability of an alternative host. All the insects and pathogens species that have been reported to be affected by storms show a consistent positive response to increased storm (wind) frequency, related to a higher availability of suitable breeding substrate. The type of host, i.e. broadleaved or coniferous tree species, does not seem to affect the responses of insect pests and pathogens to the four climatic drivers. The comparison of three major functional guilds of insect pests and pathogens allows identifying different types of responses. The primary foliar insects and pathogens respond positively to temperature and fire while the response to drought is either positive or negative. The primary wood pests and pathogens show a positive answer to all drivers but for drought, with a majority of negative response to increasing water stress. Secondary wood pests and pathogens respond in an overall positive way to all climatic drivers.
More than 40 transects have been set up along elevational gradients, in several mountain areas of Europe, as spatial analogues of climatic gradients to decipher ecological and physiological mechanisms underlying climate-driven changes in tree and insect herbivores performance. We quantified endemic insect herbivory by four guilds (sap feeders, chewers, miners and gall makers) feeding on four major European tree species (Beech, Norway spruce, Scots pine, and European larch) on each elevation gradient. The average level of insect herbivory was generally below 10 %. Within each tree species and feeding guilds there was relatively high variability in the level of herbivory between the various regions. We observed a neutral effect of temperature for all the host tree species except for European larch that exhibited a positive temperature-herbivory relationship. However, for beech, Norway spruce and European larch we found a significant interaction between feeding guild and temperature, i.e. the effect of temperature was different for the different guilds. For beech we found a negative association for sap-feeders, while chewers showed an opposite pattern. Miners and gall-makers exhibited a neutral response. For Norway spruce we found a stronger positive effect for gall-makers than for the other guilds. For Scots pine we found a non-significant trend for all the guilds. For larch, we generally found a tighter herbivory-temperature relationship than for the other host tree species. We found a strong positive relationship for miners, a less steep positive trend for sap-feeders and a negative relationship for chewers. Against the general expectation of an overall positive effect of warmer temperatures on insect herbivory, we therefore observed a more complex response depending on the herbivore feeding guild and the host species. The large variability in the herbivore response emphasised the need to evaluate simultaneously the responses of multiple host and herbivore species to predict the net effects of climate change on insect herbivory along elevational gradients.
We tested whether tree wood production is positively related to tree species richness while controlling for climatic factors, by analysing 55 265 forest inventory plots in 11 forest types across five European countries. Wood production was higher in mixed compared to monospecific forests of the same European forest type (except in acidophilous oak forests for which values were lower). On average, wood production was 24.38 % higher in mixed than in monospecific forests. Taken alone, wood production increased with tree species richness, at least from monospecific to mixed plots with 3-4 species, and then the relationship reached an asymptote. In alpine forests, wood production increased up to six species, while in non-riverine pioneer forests maximum wood production was already reached in two species forests. In acidophilous forests, wood production decreased from monospecific to mixed plots with 3-5 species, while productivity in plots with 6-8 species was not significantly different from the monospecific ones. Overall, climatic variables were stronger determinants of wood production compared to tree species richness. Tree species richness had a low but positive direct effect on wood production. However, in almost all forest types, stand basal area increased with tree species richness, and stand basal area was the variable with the largest positive effect on wood production. Therefore, the effect of tree species richness on wood production is mainly indirect by increasing stand basal area.
Extensive simulations were also performed with a forest succession model (ForClim), differing in species richness and composition (from 1 to 30 European tree species) and covering a time period of 2000 years, at 11 sites in central Europe located along a strong climatic gradient. Forest productivity increased strongly with both realised species richness and functional trait diversity, but it varied significantly across sites, ranging from 1.1 to 2.97 t ha-1 year-1 for simulations with 30 species (i.e. the highest richness tested). A positive biodiversity-productivity relationship was also evident when considering initial species richness. The shape of the relationship varied across sites, but it consistently reached an asymptote at high species richness. Saturation, defined as 90 % of the productivity obtained in the simulation with 30 species, occurred at lower richness at sites with low maximum productivity. The positive trend between species richness and productivity was strongly related to an increase in functional diversity. In 93 % of the simulations, mixtures showed higher productivity than the average of the monoculture productivities (non-transgressive overyielding). Nevertheless, diverse forests achieved greater productivity than the most productive monospecific forest (transgressive overyielding) in only 11 % of simulations. The net biodiversity effect (i.e. the difference between the simulated productivity of a multi-species forest and its expected productivity based on the simulated monospecific forests, under the null hypothesis that there is no selection or complementarity effect) calculated with realised abundance at the end of the simulation was positive in 85 % of simulations, increasing with realised species richness. Thus a strong overyielding pattern was present in most cases. To explain it, we partitioned the selection and complementarity components of the net biodiversity effect, which showed striking results: both effects range from positive to negative, but the selection effect was negative in 36 % of simulations across all sites whereas the complementarity effect was negative in 11 % of simulations only; the complementarity effect was stronger than the selection effect in 80 % of simulations. The selection effect increased weakly with realised species richness. In contrast, complementarity increased 2.5 times more strongly with realised species richness. Also, the net biodiversity was strongly positively related to functional diversity across sites as well as within sites. The complementarity and selection effects were also related to functional diversity. Overall, this confirms the strong importance of functional diversity for explaining why productivity increases with increasing species richness. These biodiversity effects emerged because increasing species richness promotes higher diversity in shade tolerance and growth ability, which resulted in forests responding faster to small-scale mortality events. The same study revealed that the temporal stability of biomass production increases with increasing species richness and functional diversity, mostly because of the asynchrony of species fluctuations in the forest.
Further simulations have been undertaken in conditions representative of core and margins of tree species ranges, under three regional climate models, and revealed the persistence of the diversity - productivity relationship under climate change. Under new climate conditions (temperature warmer by + 3 to 4 degrees Celsius) on average, the mean productivity of the monocultures is still lower than the productivity of the mixture. However, the difference between mixture and monocultures diminishes in comparison with simulation run under current conditions. Overall, the most northerly located EFTs (Boreal and Hemi-Boreal) and the Alpine EFT are those predicted to experience the strongest positive impact of diversity under future conditions. Boreal and Hemi-Boreal EFTs are located in regions that will be the more likely to be colonised by species migrating northwards according to recent projections. Our simulation results comfort this view as future conditions will allow more species from the defined species pool to better perform in those areas. The biodiversity effect is weaker in EFTs with larger species pool. In these richer communities, even if future conditions are more favourable for more species, high competition levels may temper the diversity effect. In other words as the diversity effect is already strong in these EFTs under current conditions, it might not increase much further under future conditions.
The quantitative effects of tree diversity on resistance against pest insects have been evaluated through meta-analyses and also investigated in three 'manipulative forest diversity experiments' in Finland, Germany and France.
First we hypothesised that in mixed forests, resistance of a tree species to insect herbivores results from the interaction between three factors: density of the focal tree species (main resource concentration), the phylogenetic distance between this species and its neighbours, and the degree of insect feeding specialisation. To test this hypothesis, we compared herbivory (assessed via abundance or damage) by a given insect type (species or feeding guild) on a focal tree species grown as a monoculture (hereafter referred as the main host species) with herbivory on the same tree species when grown in a mixed stand, by performing a meta-analysis. Increase in tree species richness within a stand generally coincides with a decrease in the density of each individual tree species. To separate effects of tree species richness from those of resource dilution, we retained only case studies that compared single-species stands with two-species mixtures, which constituted the majority of available data. The final dataset was composed of 85 case studies from 22 different publications, with 28, 24 and 22 case studies for monophagous, oligophagous and polyphagous herbivores, respectively. Associational resistance (i.e. lower damage in mixed stands) occurred in 80 % of case studies. On average we observed a 30 % decrease in herbivory in mixed stands as compared to monocultures. Monophagous herbivores showed the strongest negative response to tree diversity with a 42 % decrease in herbivore abundance and damage in two-species mixtures as compared to pure stands. Oligophagous herbivores showed a weaker but still significant 15 % decrease in herbivory in mixed stands. Responses of polyphagous herbivores to tree diversity were not significant. The magnitude of associational resistance to monophagous herbivores increased with increasing dilution of the main host species in the mixed stands. Damage by oligophagous herbivores in mixed forest significantly decreased with increasing host dilution and phylogenetic distance between the main host and the associated species. For polyphagous herbivores, we observed a switch from associational susceptibility (more damage in mixed stands) when the phylogenetic distance between the host and the associated species was low to associational resistance (lower damage in mixed stands) when the phylogenetic distance was high.
In the experimental plantations, tree species diversity overall had positive effects (lower damage in mixtures, i.e. associational resistance) on specialist herbivores (leaf miners, leaf rollers, gall makers, sap feeders), probably because non host plant neighbours can disrupt visual or olfactory cues used by insect specialists to locate and colonise their host plants. In contrast, tree diversity had a negative effect (higher damage in mixtures, i.e. associational susceptibility) on generalists (chewers and skeletonisers), probably due to spill-over among host plants, or increased fitness provided by mixing diet.
In particular, in the ORPHEE experiment, we focussed on oak trees and found that herbivory by leaf chewers (generalist herbivores) was not significantly affected by tree diversity at the plot scale. By contrast, the abundance of leaf miners decreased significantly with increasing tree diversity. The dilution of deciduous oak species was the best explanatory variable. Thus, the mean abundance of leaf miners per plot decreased significantly with tree diversity, due to the greater dilution of host trees in more diverse plots. The insect herbivory response to tree diversity variables at the neighbourhood scale was similar to that observed at the plot scale. For leaf chewers, both tree height and tree apparency (i.e. difference between focal oak tree height and the height of its eight neighbours) had a significant positive effect on herbivory, with taller and more apparent saplings being more prone to damage than less apparent ones. Taller oak saplings consistently experienced more chewing damage than smaller saplings, regardless of the diversity of the surrounding trees. Leaf miner infestation also increased significantly with increasing oak sapling apparency. This suggests that the abundance of leaf miners was not related to tree diversity per se, but to the local structural heterogeneity generated by tree diversity. This experimental study provides new evidence for the existence of a relationship between diversity and resistance, with lower levels of damage by leaf miners in more diverse tree species assemblages. However, the main contribution of this work was the breaking down of the diversity effect mainly into two interacting mechanisms acting at two different spatial scales. The first of these mechanisms is based on host dilution among non-host plants, which increases with increasing tree species richness. The second is based on tree apparency being lower due to the presence of taller trees, when the non-host trees grow more rapidly than the host trees. Both mechanisms may have resulted in the disruption of host location and colonisation and both are dependent on the presence of particular non-host species (sampling effect). In addition, the above two mechanisms (host dilution and tree apparency) did interact. Leaf miners responded more strongly to tree apparency when their host species were concentrated but became less selective about host tree size when their feeding resource was diluted and more difficult to find, suggesting changes in host searching patterns depending on local resource availability. These findings highlight the fact that insufficient consideration of plant size as a covariate may lead to misleading interpretations about the existence of such effects of biodiversity, particularly during forest regeneration. They also have implications for the design of new planted forests, which are mostly managed as monocultures. The complementation between tree species grown for wood production and more rapidly growing pioneer species may provide effective protection against pest insects through visual or olfactory disruption of host finding while producing additional biomass. However, long-term studies are required to determine the consequences of decreasing herbivory for forest productivity throughout the entire forest rotation.
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 therefore 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 colonisation 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.
It is important to better understand the response of tree species to biotic and abiotic disturbances associated with climate change, in order to predict the shifts in tree species dominance in mixed forests. For that we developed a risk analysis, based on a large literature review and expert knowledge, to estimate the vulnerability of 24 common European tree species. We developed a cluster analysis to identify functional tree species groups of response to biotic and abiotic stresses and rated their relative vulnerability. This clustering produced four groups of species according to their relative vulnerability to climate and biotic stressors. The group with species less vulnerable included Quercus robur, Betula pubescens, Populus tremula and Betula pendula. The group with species vulnerable to abiotic stressors but not to biotic agents comprised Acer pseudoplatanus, Fagus sylvatica, Juniperus communis, Pinus halepensis, Quercus faginea, Quercus ilex, Quercus petraea, Quercus pubescens, Sorbus aucuparia and Tilia cordata. The group with species less vulnerable to abiotic stressors but more to biotic agents comprised Alnus glutinosa, Castanea sativa, Picea abies, and Ulmus glabra. The group with tree species highly vulnerable to both biotic and abiotic stressors included Abies alba, Fraxinus excelsior, Pinus nigra, Pinus pinaster, Pinus sylvestris and Quercus suber. We also documented 13 key functional traits for these species. The 4 response groups of tree species were significantly discriminated using the 13 life trait values and the matrix of confusion revealed a rate of good classification (right allocation of species to a priori groups) equal to 100 % for the four groups. The groups of species highly vulnerable to abiotic stresses were mainly characterised by low water stress tolerance whereas the groups of species vulnerable to biotic stresses are mainly characterised by high leaf nitrogen content, i.e. high leaf palatability for forest insects and pathogens. The least vulnerable group (low-low) combines high stress tolerance and low leaf nitrogen content. Our analysis has demonstrated that it seems possible to predict the vulnerability to biotic and abiotic agents of the main European tree species on the basis of their functional traits. The construction of such functional groups of tree species response to climate and pest and pathogens stressors provides forest managers with new tools to better anticipate the effect of climate change on the functioning of their forests according to their composition. It also gives some useful indication about the response of any other tree species, e.g. exotic, not included in our analysis, but for which the same life traits are known and quantified. By projecting these values in the same plan defined by the 13 traits or by drought tolerance and leaf nitrogen content, one might be able to evaluate the relative vulnerability of this additional tree species.
A growing body of evidence, including those produced by the project, suggests a positive relationship between tree species diversity and forest productivity. Within the BACCARA project we have also shown that tree species diversity can provide other ecosystem services. Using a meta-analysis of the scientific literature, we have demonstrated a consistent and positive relationship between tree species diversity and species richness of mammals, birds and arthropods, thus substantiating the 'biodiversity for biodiversity' concept. We have also shown that mixed forests are overall more resistant to pest insects than pure forests However a majority of these studies have pointed out the importance of species composition which is often more relevant than the number of species per se to explain the relationship between biodiversity and ecosystem functioning. Some tree species assemblages can be 'unlucky', being less productive or more vulnerable due to the 'wrong' assemblage of individual tree species. Furthermore, mixed forests are often considered as more complicate to manage than pure forests due to different requirement by different tree species or different growth phenology. The cost of establishment and maintenance of mixed forests might be also higher. There are therefore a large number of criteria to take into account when it comes to decide about growing trees as pure vs. mixed forest stands. Some of these criteria will have to be maximised, some other minimised. These criteria are also quantified in different manners, with different units. Criteria may also have different importance or relevance and thus not account with the same weight in the decision. It is therefore very difficult to integrate all these information to find the best compromise and make the right decision about converting pure to mixed forests. This is where multi criteria decision analysis (MCDA) tools can be useful. MCDA has been developed to help rank several alternatives from the worst to the best based on multiple, often conflicting criteria. One of the main advantages of MCDA is that it allows consideration of a large number of criteria that may be measured on completely different scales. We developed a pilot study using this approach. We focused on Scots pine (Pinus sylvestris), Norway spruce (Picea abies) and birch (Betula pendula) in the boreal, hemiboreal and alpine coniferous European forest types because we had the requisite information about their functioning in pure vs. mixed stands. We considered three criteria related to productivity (wood productivity, resistance to pest damage, stability of primary production), two criteria related to biodiversity conservation (species richness of birds and arthropods) and one criterion related to financial risk (standard deviation of the net present value). We could document these 6 criteria for the seven possible combinations of one, two and three of these tree species. Giving similar weight to the six criteria we found that overall mixed stands were preferred to pure stands, notably those composed of a mixture of broadleaved and coniferous species. The objective of this analysis was not to provide forest owners with the ultimate forest composition to be grown in northern Europe in the climate change context. The aim of this pilot study was rather to propose a method to integrate different criteria in order to make a decision about converting mono-species into mixed-species forests. It will be the choice and the responsibility of the user to add or delete some criteria, change their values and reduce the list of possible tree species, depending for example on local site conditions and wood market demand. Then forest advisors will also have the possibility to test the effect of changing the weights of criteria, first to see whether the forest type ranking is consistent or not (a sensitivity test), and second to consider different forest ecosystem services.
Potential impact:
Based on empirical data collected along elevation gradients in Europe and also on literature reviews, several features have been identified about forest pest insects and pathogens that can explain and then predict their response to increasing temperature and drought. According to this classification, 'What-to-combat'? guidelines have been produced in the form of an electronic database. In total, 83 data sheets on the main European forest pests and disease will be soon available where are presented a brief description of the biology, symptoms, identification key and an assessment of the actual and potential effects of climate change on distribution, abundance and damage.
A thorough review of the literature together with the empirical knowledge accumulated during the project made it possible to classify the 24 most abundant European forest species according to four levels of vulnerability to biotic and abiotic stressors triggered by climate change. In addition, several tree attributes (life traits and response patterns) were identified that could explain this categorisation. Furthermore we propose 'what-to-grow'? guidelines explaining how to integrate these characteristics and other socio-economic features in a MCDA tool in order to help forest managers identifying the tree species to introduce, maintain or abandon, in the current climate change context.
The analysis of forest inventory data from all around Europe clearly showed that mixed forests are more productive than monocultures in most European forest types. These results are confirmed by simulations run with forest succession models. Converging results have been also obtained from meta-analyses of the scientific literature and empirical data of experiments demonstrating associational resistance (i.e. lower damage in mixed forests) against forest insect specialists. Forest mixtures would be also more able to buffer negative impacts of climate change on key tree species. All these outcomes strongly suggest enhancing tree species diversity at the stand level to sustain forest ecosystem productivity in the context of climate change. In the line with this recommendation, we propose a decision analysis tool that integrates multiple ecological and socio-economic criteria in order to help forest managers making decision when they want to convert tree monocultures in mixed forests.
Analysis of the publications
Until now the project has produced 44 scientific publications in peer reviewed journals, four are currently submitted and many are still in preparation. The target review are mainly in the field of ecology, including two papers already published in Ecology Letters which ranks first in terms of impact factor. Papers have also been published in entomology, pathology and forestry journals.
Five Master students and eight Doctor of Philosophy (PhD) students will or have successfully defended their work with the full help of the BACCARA project (in total 25 were partially helped by the project).
More than 100 communications (oral and poster) have been presented in national and international scientific conference to disseminate the outcomes of the project.
Furthermore, 23 interviews in the radio and television media have been given to explain the objectives and findings of the project to the large public audience.
Project website: http://www.baccara-project.eu/
The analysis of past records of damage in forests indicates that climate change generally promotes pestilence in forest but not for all species of pests and pathogens. Drought is likely to increase damage by defoliators, foliar pathogens, bark beetles and endophytic fungi but may reduce the impact of root rot pathogens. Damage can be partly contained by a higher activity of insect natural enemies under warmer conditions, although this has been shown only for ectoparasitoids or parasitoids of ectophagous insect herbivores. Some plant defenses such as leaf toughness significantly increase with elevation, i.e. lower temperatures. A literature review on 61 different species (32 insects and 29 fungi) from European forests showed that increased temperature is directly associated with overwhelmingly positive response by insect pests while the trend is less clear in the case of pathogens. New empirical data from more than 40 altitudinal gradients, in several mountain areas of Europe, indicate that fungal and insect assemblages tend to simplify with altitude suggesting a potential increase in pest and pathogen damage with increasing temperatures. They also revealed either neutral or positive effect of increasing temperatures on insect herbivory on four main European tree species.
Analyses of European forest inventory data showed that mixed forests are on average 24 % more productive than monospecific stands and revealed a positive relationship between tree species richness and wood production. Extensive simulations with tree succession models have confirmed that tree species richness and functional diversity promote productivity in European temperate forests. The positive diversity - productivity relationship is likely to persist under climate change. Meta-analyses of scientific literature and data from manipulative experiments clearly demonstrate a positive effect of tree species diversity on resistance against specialist insect herbivores but not against polyphagous pests. Higher dilution, lower apparency and higher phylogenetic contrast of focal tree intermixed with non-host trees mainly explain such associational resistance.
The combined analysis of main results obtained in BACCARA revealed that it seems possible to predict the vulnerability to the biotic and abiotic factors involved in or amplified by climate change of the main European tree species on the basis of their functional traits. Multicriteria decision analyses also proved to be a promising tool to help foresters to integrate ecological and socio-economic issues in order to make a decision about converting mono-species into mixed-species forests.
Project context and objectives:
A considerable number of studies are being published on the possible effects of climate change on forest productivity. They suggest that global positive response of forest productivity to raising CO2 and temperatures may be impeded by large diebacks due to extreme climatic events such as severe droughts. These studies often dealt with large scale modelling to predict global forest response to climate change or, on the other hand, with possible changes in single tree species growth. However, they overlooked the response of the whole tree species community to climate change which is probably the most relevant scale to meet forest managers' expectations. Changes in the growth of individual tree species might affect biotic interactions, including competition, herbivory and symbiosis, leading to shifts in the species dominance. Together with single-tree species fitness, these interactions may determine which species will persist, go extinct or migrate to assemble new communities. These new tree species assemblages may in turn drive changes in forest productivity. Indeed, there is an increasing body of evidence to support the view that biomass production can increase with herbaceous plant species richness or diversity but results are less consistent in more complex ecosystems such as forests.
The main objective of BACCARA is therefore to develop tools allowing forest managers and policy makers to evaluate risk of European forest biodiversity loss under climate change and subsequent decrease in forest ecosystem productivity. The principle of the project is to construct a three-dimensional risk assessment model linking climate change, functional diversity, and forest productivity through a three step process:
1. effects of climate change on forest biodiversity are evaluated through better understanding of the influence of climatic conditions on the ecological processes that shape assemblages of forest tree species and associated insect, fungus and mycorrhizae species;
2. relationships between forest biodiversity and functioning are deciphered through better understanding of the role of forest species richness and composition on biomass production;
3. the information is eventually aggregated to predict the risk of forest productivity loss, considered as a function of climate change probability (hazard), susceptibility of forest to climate change according to its diversity (vulnerability), and effect of forest diversity on biomass productivity (exposure).
Project results:
Based on a thorough analysis of forest inventories, several studies have detected rapid distribution shifts in tree species altitudinal optimum thus suggesting a fast and strong impact of climate change on tree species distribution and performance, which would be stronger for species already at the limit of their natural range.
A translocation experiment of beech seedlings along an elevation gradient showed negative effects of the soil biota community on European beech survival. However, these negative effects decreased with elevation and disappeared in samples from the highest altitude. This is the first study to show variability in interactions between plants and the soil biota community across an elevation gradient. Many micro-organisms with rapid proliferation rates may have triggered the negative effects observed. For instance, Fagus sylvatica seedlings are known to host soil fungi which are responsible for root and collar rot symptoms. Hence, the trend observed was probably the consequence of a decrease in the soil pathogen pressure on F. sylvatica with increase in elevation. This suggests that global warming might enhance soil pathogen and then reduce the survival of some tree species.
A literature review of mechanisms underlying response of tree communities to climate change was undertaken. It highlighted that tree species have a high level of plasticity and genetic variation for phenological traits that could allow populations first to rapidly respond and second to adapt to new conditions. However, there are many uncertainties about the potential for acclimation to climate change (bud dormancy release for instance). Indeed, some studies suggest that this level of plasticity could be insufficient to adjust to expected climate change. Climate warming may increase the relative importance of chilling temperature in the timing of tree flushing in the next decades, which could alter the reaction norms to temperature. Global climate change is also projected to produce longer and more frequent droughts, which have the potential to trigger widespread tree die-off. Recently, several studies characterised the cavitation resistance on a broad range of species and reported a high level of variation between species, suggesting a species-specific response to increased drought severity. Ongoing climate change is therefore expected to have important impacts on tree species, for instance climate change will affect tree species distribution, but also species abundance and tree-population structure (i.e. size-distribution) within the entire species distribution. However, this review revealed the lack of understanding of the processes that drives climate related large scale pattern of species distribution. It is in particular necessary to better account for tree demography. Indeed, species distribution, species abundance and tree-population structure are inherently population level problems that should be analysed with a demographic framework. For instance a demographic analysis may allow identifying locations with positive population growth, where births are greater than deaths, and locations with negative population growth. This is clearly key to understand and define the species distribution edge, how and why species range boundaries will change but also how and why much more fine population characteristics such as the abundance of the species, its size or age structure, and it spatial structure will change throughout its entire distribution. The review further presents the state of knowledge of climate effect on three key demographic rates, growth, recruitment and survival. The overall pattern is a positive response of tree growth to increase in temperature and water availability. However, very few studies have explored how temperature and precipitation, or climate and light (crucial for competition) or climate and CO2 were interacting to control tree growth. Our understanding of recruitment response to climate is thus much more limited than for growth. The few studies documenting directly the response of fecundity, germination, or seedling growth and survival to climate have generally shown that tree recruitment was limited by low temperature and by water stress. Despite its great importance for forest dynamics the response of mortality to climate has been extremely poorly documented. Nevertheless, several studies have documented that climatic variables such as drought and frost were increasing tree mortality.
In line with the need to take into account tree demography to better understand the response of tree species to climate constraints, a thorough review of the literature was carried out on key demographic traits. The final data used for the analyses of tree responses to climate change included a total of 331 records: 144 for growth, 44 for recruitment, 98 for survival and 45 for abundance. Most studies reported a decreased growth, survival and recruitment for most of the 24 tree species in response to past climate change. In contrast, abundance was found to increase in most cases, mostly due to northward and upward range expansion. Phenological features such as leaf production and reproduction were in general found to take place earlier in the year in agreement with previous reviews. A small but significant fraction of studies reported no changes for certain species and response variables. Using these four traits for grouping of species according to their responses to climate change rendered three groups of eight species each. The grouping was highly consistent, with a perfect match after 500 iterations. In the three groupings most species exhibited a reduced growth and survival as a consequence of climate change. Differences among groups were mostly due to different responses in terms of abundance and regeneration. All species in group 1, with Picea abies as indicator species and many species from riparian and very humid sites (most of them short living), were the least vulnerable, exhibiting an increased abundance and regeneration. Group 3, the most vulnerable one, characterised by Abies alba and several pine and oak species and dominated by Gymnosperms, exhibited a decreased regeneration. Group 2, characterised by Quercus ilex was somewhat intermediate, with moderate decreases in abundance and little change in regeneration. Then 13 functional and life history traits were documented for the 24 European tree species. These traits altogether allowed separating three distinct groups of species. The grouping of the tree species exhibited a good agreement (100 % of matching) with the grouping with the 4 demographic traits. The main life traits explaining the separation between the three groups of European tree species were the drought tolerance and the wood density.
Another, empirical study tackled the effect of climate conditions on the assemblages of tree species. The study was conducted on seven elevation gradients, from southern Spain to northern Sweden. Overall, species richness was higher for seedlings than for adults. This might be a consequence of seedlings colonising broader ranges of habitat conditions than the adults due to their small size and the spatial scale of resource variation. As a result, species richness does not seem to be compromised in the near future, at least due to increases in temperature, with the exception of sites where species richness in mature trees surpassed that of the seedlings at the highest temperatures, meaning that future richness could be reduced to climate change. Functional diversity was positively related to species richness in most sites, indicating that trait values are similar among species. In these sites, functional redundancy may buffer against the impact of climate change if species losses take place, because if one species gets extinct, functionally similar species can reduce the loss of functional diversity. However, in the Mediterranean sites a low a number of species was translated into high functional diversity. This is because the species present strong dissimilarities among traits. There species loss may have then serious consequences for functional diversity. When considering all sites and transects together, functional diversity was increasing with increasing temperatures. This means that in sites predicted to experience harsher conditions in the future (i.e. a decrease in productivity), the role of biodiversity on productivity will be more important. In other words if communities in those sites loose a species, the decrease in productivity will be on average stronger.
Predicting climate-driven changes in plant distribution is crucial for biodiversity conservation and management under recent climate change. Climate warming is expected to induce movement of species upslope and towards higher latitudes. However, the mechanisms and physiological processes behind the altitudinal and latitudinal distribution range of a tree species are complex and depend on each tree species features and vary over ontogenetic stages. We investigated the altitudinal distribution differences between juvenile and adult individuals of seven major European tree species along elevational transects covering a wide latitudinal range from southern Spain (37 degrees N) to northern Sweden (67 degrees N). By comparing juvenile and adult distributions (shifts on the optimum position and the range limits) we assessed the response of species to present climate conditions in relation to previous conditions that prevailed when adults were established. Mean temperature increased by 0.86 degrees Celsius on average at our sites during the last decade compared with previous 30-year period. Only one of the species studied, Abies alba, matched the expected predictions under the observed warming, with a maximum abundance of juveniles at higher altitudes than adults. Three species, Fagus sylvatica, Picea abies and Pinus sylvestris, showed an opposite pattern while for other three species, such as Quercus ilex, Acer pseudoplatanus and Quercus petraea, we were not able to detect changes in distribution. These findings are in contrast with theoretical predictions and show that tree responses to climate change are complex and are obscured not only by other environmental factors but also by internal processes related to ontogeny and demography.
With the review of the literature and the combination of data collected on many elevation gradients during the project, we have been able to identify key processes and mechanisms underlying response of tree communities to climate change. First, individual tree species responses to climate change seem to be idiosyncratic, i.e. unpredictable. Second, responses to climate change differ from adults and juveniles so a well-balanced demographic structure of tree populations can mitigate negative impacts. Third, positive species interactions involving facilitation of juveniles by established adults are important at limit range, both in elevation and latitude, so mixed forests are more likely to buffer negative impacts on key species than monospecific ones. Fourth, functional diversity of tree assemblages was assessed over elevational and latitudinal gradients showing a remarkable homeostasis, which is in contrast to the observed decrease in taxonomic diversity and species richness at increased elevation and latitudes.
At the beginning of the project, a theoretical review has been conducted to propose several mechanisms of response to climate change by pests and natural enemies of herbivores. It indicates that the direct effects on the herbivorous insect will be generally positive as a result of increased winter survival, faster development rates, and sometimes increased number of generations per year. Furthermore, some insect herbivores are likely to benefit from increased frequency of stressful events for plants. Insects that suffer from constitutive plant defences would tend to be favoured when conditions promote increased plant growth and associated declines in secondary metabolism. Insects that exploit young, nutritionally favourable foliage may be sensitive to climatically driven changes at the start of the growing season and to temperatures that influence the relative rates of leaf maturation and insect development after budburst. The nature of physiological controls on plant vs. insect phenology will influence the extent to which plant and insect phenology remains coupled under climate change. Increased activity in arthropod natural enemies could lead to increased strength of top-down control on the herbivorous insect. However, the magnitude of the effect will depend on attack strategy of predators and type of parasitism (endo versus ecto). Pathogens are likely to increase their infection rate under increased humidity and temperature. When forest pest outbreaks will occur within current distribution limits, we might expect shorter delays before negative feedbacks from natural enemies can act on population density. But outbreaks may well also occur outside range limits. In most cases, range limits tend to be a belt of recurrent colonisation and extinction events rather than a precise border. It is possible that many new outbreaks outside of the generally accepted range edge fall within this belt. The width of the belt would be defined by the dispersal potential of the species, including rare long-distance events. Climate change, however, may have an effect on dispersal per se and thus indirectly start outbreaks outside the range whenever conditions are suitable for insect herbivore performance. Climate-matching models frequently identify regions that seem suitable but are presently unoccupied - presumably because of dispersal limitation. Probably, the extent of such suitable but unoccupied regions is increasing under climate warming, which will increase the probability of outbreaks.
A first meta-analysis of the scientific literature was carried out to evaluate the effect of drought on forest pest and pathogen damage. The literature search yielded 100 comparisons of forest pest and disease damage on water stressed vs. unstressed trees, derived from 40 publications and reports that were published between 1975 and 2010. Overall water stress resulted in higher forest pest and disease damage. The type of trophic substrate used by forest pest and pathogens had a highly significant effect on the difference in damage between water stressed and unstressed trees. For pest insects and pathogens, the drought effect differed between the primary (those which can attack healthy trees) and the secondary agents (those which can only attack stressed trees). Primary damaging agents living on foliar organs caused higher damage in water stressed trees. Drought had negative effects on damage caused by primary agents developing on woody organs but significantly increased damage caused by secondary agents developing on woody organs. These results clearly indicate that the effect of water stress on the level of damage by forest pests and pathogens depends more on the type of substrate they use than on their feeding guild. We also tested the effect of water stress severity on level of damage for each functional group of forest pests and pathogens separately. We observed no significant effect of any water severity variables on level of damage in water stressed trees for any primary damaging agent. On the contrary, the effect of water stress severity significantly affected the level of damage caused by secondary agents living in woody organs. The variable best explaining damage variation was the ratio between observed predawn leaf water potential in stressed trees and the species - specific index of drought tolerance (P50). The level of damage increased linearly with this ratio. A threshold value of 30 % was detected below which damage in water stressed trees may be lower than in unstressed trees (negative effect size) whereas damage were consistently higher in stressed trees with predawn leaf water potential higher than 30 % of P50 (tree having a high native state of embolism). Drought is then likely to increase damage by defoliators, foliar pathogens, bark beetles and endophytic fungi but may reduce the impact of root rot pathogens.
A second meta-analysis was performed to test the effects of climate change on the top-down control of insect herbivores by insect parasitoids. Considering that elevation gradients can be used as analogues for global warming, we carried out meta-analyses of 27 correlations between parasitoid richness and elevation and 140 correlations between parasitism rate and elevation in natural and semi-natural environments. We also explored various covariates that may explain the observed responses. Both parasitism rates and parasitoid species richness significantly decreased with increasing elevation. The decrease was greater for ectoparasitoids and parasitoids of ectophagous insects than for endoparasitoids and parasitoids of endophagous hosts, possibly because these latter are better protected from adverse and extreme climatic conditions occurring at higher elevations. Although our results suggest an increase of parasitism with increasing temperature, other factors regulating herbivorous insects have to be considered before concluding that climate warming will lead to a decrease in pest density.
A third meta-analysis was carried out to evaluate the likely effects of climate change on the bottom-up regulation of insect damage, i.e. via plant defenses. We used again elevation gradients as analogues of temperature gradients. We also tested the effect of three covariates on the relationship between plant chemical defenses and altitude. First, we divided plant species into herbaceous and woody plants (including shrubs). Second, we divided plant chemicals into flavonoids and non-flavonoids secondary metabolites because flavonoids-based compounds can as well be involved in UV protection, or freezing tolerance in plants. Third, we distinguished between measures taken on reproductive (flowers, seeds, fruits) or vegetative organs of the plants (leaves, branches, trunks). Overall, we detected a significant increase in plant physical defense traits and flavonoids with elevation. Particularly, leaf toughness and flavonoids in the reproductive organs were increasing with elevation whereas we found no effect of elevation on other types of defenses (non-flavonoids in general and flavonoids in vegetative organs). These results suggest that, contrary to classical predictions, a reduction in herbivory pressure in harsher environments does not forcedly lead to a decrease in plant defenses. Along with climate selecting for physical and chemical protective traits, herbivores should also be expected to select for higher defense at high elevations. At low elevation, low defense may also be selected because species have fast growth rate and a high capacity to recover after damage. Indeed, high growth rate confers a competitive advantage against slower growing species with higher defense. Plant species from high elevation may have developed tougher leaves as an adaptation to severe climatic conditions, but this may indirectly confer increased resistance to herbivores. This suggests that selective forces of abiotic conditions (e.g. cold hardiness) might be stronger than biotic ones (e.g. resistance to herbivores) along elevation gradients, but this might be organ-specific depending on the trait analysed.
A fourth literature review on 61 different species (32 insects and 29 fungi) from European forests showed that increased temperature is directly associated with overwhelmingly positive response by insect pests while the trend is less clear in the case of pathogens. We collected 90 cases involving 61 different species (32 insects and 29 pathogens) from European forests for which data were available about the effect of climate-associated driver such as elevated temperatures, drought, storm and fire on their abundance or damage. The most abundant tree species in Europe were considered according to ICP Forest (2005) and enlarged to other tree species for which there was information available. Six tree genera were particularly concerned (Betula, Fagus, Picea, Pinus, Populus, Quercus) but several pests / pathogens were polyphagous on conifer and broadleaved trees. Increased temperature is directly associated with overwhelmingly positive response by insect pests. The trends are less clear in the case of pathogens, with relatively few cases of responses reported, and in most cases without known underlying mechanisms. Diplodia pinea and Gremmeniella abietina are benefiting from the temperature increase whereas Crumenulopsis sororia, Melampsora larici-populina, and Phloeosporella padi are negatively affected. Other frost-sensitive fungi, such as Phytophthora spp., may also benefit from the increase of temperature especially in winter. Increased frequency and intensity of drought is indirectly associated with damage by pests and pathogens, acting mainly through changes in the host plant traits and in the soil conditions. In contrast to their responses to temperature, insects appear to respond more equivocally to drought, with a similar number of cases of positive and negative responses. The responses of pathogens to drought vary as well, but those cases for which responses are known tend to be primarily via host plants (indirect) and, notably, positive, in contrast to those of insects. Responses of insects to increased fire frequency are rather poorly documented. A number of pathogen species, on the other hand, show a positive response indirectly mediated by an increase in host susceptibility or availability of an alternative host. All the insects and pathogens species that have been reported to be affected by storms show a consistent positive response to increased storm (wind) frequency, related to a higher availability of suitable breeding substrate. The type of host, i.e. broadleaved or coniferous tree species, does not seem to affect the responses of insect pests and pathogens to the four climatic drivers. The comparison of three major functional guilds of insect pests and pathogens allows identifying different types of responses. The primary foliar insects and pathogens respond positively to temperature and fire while the response to drought is either positive or negative. The primary wood pests and pathogens show a positive answer to all drivers but for drought, with a majority of negative response to increasing water stress. Secondary wood pests and pathogens respond in an overall positive way to all climatic drivers.
More than 40 transects have been set up along elevational gradients, in several mountain areas of Europe, as spatial analogues of climatic gradients to decipher ecological and physiological mechanisms underlying climate-driven changes in tree and insect herbivores performance. We quantified endemic insect herbivory by four guilds (sap feeders, chewers, miners and gall makers) feeding on four major European tree species (Beech, Norway spruce, Scots pine, and European larch) on each elevation gradient. The average level of insect herbivory was generally below 10 %. Within each tree species and feeding guilds there was relatively high variability in the level of herbivory between the various regions. We observed a neutral effect of temperature for all the host tree species except for European larch that exhibited a positive temperature-herbivory relationship. However, for beech, Norway spruce and European larch we found a significant interaction between feeding guild and temperature, i.e. the effect of temperature was different for the different guilds. For beech we found a negative association for sap-feeders, while chewers showed an opposite pattern. Miners and gall-makers exhibited a neutral response. For Norway spruce we found a stronger positive effect for gall-makers than for the other guilds. For Scots pine we found a non-significant trend for all the guilds. For larch, we generally found a tighter herbivory-temperature relationship than for the other host tree species. We found a strong positive relationship for miners, a less steep positive trend for sap-feeders and a negative relationship for chewers. Against the general expectation of an overall positive effect of warmer temperatures on insect herbivory, we therefore observed a more complex response depending on the herbivore feeding guild and the host species. The large variability in the herbivore response emphasised the need to evaluate simultaneously the responses of multiple host and herbivore species to predict the net effects of climate change on insect herbivory along elevational gradients.
We tested whether tree wood production is positively related to tree species richness while controlling for climatic factors, by analysing 55 265 forest inventory plots in 11 forest types across five European countries. Wood production was higher in mixed compared to monospecific forests of the same European forest type (except in acidophilous oak forests for which values were lower). On average, wood production was 24.38 % higher in mixed than in monospecific forests. Taken alone, wood production increased with tree species richness, at least from monospecific to mixed plots with 3-4 species, and then the relationship reached an asymptote. In alpine forests, wood production increased up to six species, while in non-riverine pioneer forests maximum wood production was already reached in two species forests. In acidophilous forests, wood production decreased from monospecific to mixed plots with 3-5 species, while productivity in plots with 6-8 species was not significantly different from the monospecific ones. Overall, climatic variables were stronger determinants of wood production compared to tree species richness. Tree species richness had a low but positive direct effect on wood production. However, in almost all forest types, stand basal area increased with tree species richness, and stand basal area was the variable with the largest positive effect on wood production. Therefore, the effect of tree species richness on wood production is mainly indirect by increasing stand basal area.
Extensive simulations were also performed with a forest succession model (ForClim), differing in species richness and composition (from 1 to 30 European tree species) and covering a time period of 2000 years, at 11 sites in central Europe located along a strong climatic gradient. Forest productivity increased strongly with both realised species richness and functional trait diversity, but it varied significantly across sites, ranging from 1.1 to 2.97 t ha-1 year-1 for simulations with 30 species (i.e. the highest richness tested). A positive biodiversity-productivity relationship was also evident when considering initial species richness. The shape of the relationship varied across sites, but it consistently reached an asymptote at high species richness. Saturation, defined as 90 % of the productivity obtained in the simulation with 30 species, occurred at lower richness at sites with low maximum productivity. The positive trend between species richness and productivity was strongly related to an increase in functional diversity. In 93 % of the simulations, mixtures showed higher productivity than the average of the monoculture productivities (non-transgressive overyielding). Nevertheless, diverse forests achieved greater productivity than the most productive monospecific forest (transgressive overyielding) in only 11 % of simulations. The net biodiversity effect (i.e. the difference between the simulated productivity of a multi-species forest and its expected productivity based on the simulated monospecific forests, under the null hypothesis that there is no selection or complementarity effect) calculated with realised abundance at the end of the simulation was positive in 85 % of simulations, increasing with realised species richness. Thus a strong overyielding pattern was present in most cases. To explain it, we partitioned the selection and complementarity components of the net biodiversity effect, which showed striking results: both effects range from positive to negative, but the selection effect was negative in 36 % of simulations across all sites whereas the complementarity effect was negative in 11 % of simulations only; the complementarity effect was stronger than the selection effect in 80 % of simulations. The selection effect increased weakly with realised species richness. In contrast, complementarity increased 2.5 times more strongly with realised species richness. Also, the net biodiversity was strongly positively related to functional diversity across sites as well as within sites. The complementarity and selection effects were also related to functional diversity. Overall, this confirms the strong importance of functional diversity for explaining why productivity increases with increasing species richness. These biodiversity effects emerged because increasing species richness promotes higher diversity in shade tolerance and growth ability, which resulted in forests responding faster to small-scale mortality events. The same study revealed that the temporal stability of biomass production increases with increasing species richness and functional diversity, mostly because of the asynchrony of species fluctuations in the forest.
Further simulations have been undertaken in conditions representative of core and margins of tree species ranges, under three regional climate models, and revealed the persistence of the diversity - productivity relationship under climate change. Under new climate conditions (temperature warmer by + 3 to 4 degrees Celsius) on average, the mean productivity of the monocultures is still lower than the productivity of the mixture. However, the difference between mixture and monocultures diminishes in comparison with simulation run under current conditions. Overall, the most northerly located EFTs (Boreal and Hemi-Boreal) and the Alpine EFT are those predicted to experience the strongest positive impact of diversity under future conditions. Boreal and Hemi-Boreal EFTs are located in regions that will be the more likely to be colonised by species migrating northwards according to recent projections. Our simulation results comfort this view as future conditions will allow more species from the defined species pool to better perform in those areas. The biodiversity effect is weaker in EFTs with larger species pool. In these richer communities, even if future conditions are more favourable for more species, high competition levels may temper the diversity effect. In other words as the diversity effect is already strong in these EFTs under current conditions, it might not increase much further under future conditions.
The quantitative effects of tree diversity on resistance against pest insects have been evaluated through meta-analyses and also investigated in three 'manipulative forest diversity experiments' in Finland, Germany and France.
First we hypothesised that in mixed forests, resistance of a tree species to insect herbivores results from the interaction between three factors: density of the focal tree species (main resource concentration), the phylogenetic distance between this species and its neighbours, and the degree of insect feeding specialisation. To test this hypothesis, we compared herbivory (assessed via abundance or damage) by a given insect type (species or feeding guild) on a focal tree species grown as a monoculture (hereafter referred as the main host species) with herbivory on the same tree species when grown in a mixed stand, by performing a meta-analysis. Increase in tree species richness within a stand generally coincides with a decrease in the density of each individual tree species. To separate effects of tree species richness from those of resource dilution, we retained only case studies that compared single-species stands with two-species mixtures, which constituted the majority of available data. The final dataset was composed of 85 case studies from 22 different publications, with 28, 24 and 22 case studies for monophagous, oligophagous and polyphagous herbivores, respectively. Associational resistance (i.e. lower damage in mixed stands) occurred in 80 % of case studies. On average we observed a 30 % decrease in herbivory in mixed stands as compared to monocultures. Monophagous herbivores showed the strongest negative response to tree diversity with a 42 % decrease in herbivore abundance and damage in two-species mixtures as compared to pure stands. Oligophagous herbivores showed a weaker but still significant 15 % decrease in herbivory in mixed stands. Responses of polyphagous herbivores to tree diversity were not significant. The magnitude of associational resistance to monophagous herbivores increased with increasing dilution of the main host species in the mixed stands. Damage by oligophagous herbivores in mixed forest significantly decreased with increasing host dilution and phylogenetic distance between the main host and the associated species. For polyphagous herbivores, we observed a switch from associational susceptibility (more damage in mixed stands) when the phylogenetic distance between the host and the associated species was low to associational resistance (lower damage in mixed stands) when the phylogenetic distance was high.
In the experimental plantations, tree species diversity overall had positive effects (lower damage in mixtures, i.e. associational resistance) on specialist herbivores (leaf miners, leaf rollers, gall makers, sap feeders), probably because non host plant neighbours can disrupt visual or olfactory cues used by insect specialists to locate and colonise their host plants. In contrast, tree diversity had a negative effect (higher damage in mixtures, i.e. associational susceptibility) on generalists (chewers and skeletonisers), probably due to spill-over among host plants, or increased fitness provided by mixing diet.
In particular, in the ORPHEE experiment, we focussed on oak trees and found that herbivory by leaf chewers (generalist herbivores) was not significantly affected by tree diversity at the plot scale. By contrast, the abundance of leaf miners decreased significantly with increasing tree diversity. The dilution of deciduous oak species was the best explanatory variable. Thus, the mean abundance of leaf miners per plot decreased significantly with tree diversity, due to the greater dilution of host trees in more diverse plots. The insect herbivory response to tree diversity variables at the neighbourhood scale was similar to that observed at the plot scale. For leaf chewers, both tree height and tree apparency (i.e. difference between focal oak tree height and the height of its eight neighbours) had a significant positive effect on herbivory, with taller and more apparent saplings being more prone to damage than less apparent ones. Taller oak saplings consistently experienced more chewing damage than smaller saplings, regardless of the diversity of the surrounding trees. Leaf miner infestation also increased significantly with increasing oak sapling apparency. This suggests that the abundance of leaf miners was not related to tree diversity per se, but to the local structural heterogeneity generated by tree diversity. This experimental study provides new evidence for the existence of a relationship between diversity and resistance, with lower levels of damage by leaf miners in more diverse tree species assemblages. However, the main contribution of this work was the breaking down of the diversity effect mainly into two interacting mechanisms acting at two different spatial scales. The first of these mechanisms is based on host dilution among non-host plants, which increases with increasing tree species richness. The second is based on tree apparency being lower due to the presence of taller trees, when the non-host trees grow more rapidly than the host trees. Both mechanisms may have resulted in the disruption of host location and colonisation and both are dependent on the presence of particular non-host species (sampling effect). In addition, the above two mechanisms (host dilution and tree apparency) did interact. Leaf miners responded more strongly to tree apparency when their host species were concentrated but became less selective about host tree size when their feeding resource was diluted and more difficult to find, suggesting changes in host searching patterns depending on local resource availability. These findings highlight the fact that insufficient consideration of plant size as a covariate may lead to misleading interpretations about the existence of such effects of biodiversity, particularly during forest regeneration. They also have implications for the design of new planted forests, which are mostly managed as monocultures. The complementation between tree species grown for wood production and more rapidly growing pioneer species may provide effective protection against pest insects through visual or olfactory disruption of host finding while producing additional biomass. However, long-term studies are required to determine the consequences of decreasing herbivory for forest productivity throughout the entire forest rotation.
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 therefore 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 colonisation 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.
It is important to better understand the response of tree species to biotic and abiotic disturbances associated with climate change, in order to predict the shifts in tree species dominance in mixed forests. For that we developed a risk analysis, based on a large literature review and expert knowledge, to estimate the vulnerability of 24 common European tree species. We developed a cluster analysis to identify functional tree species groups of response to biotic and abiotic stresses and rated their relative vulnerability. This clustering produced four groups of species according to their relative vulnerability to climate and biotic stressors. The group with species less vulnerable included Quercus robur, Betula pubescens, Populus tremula and Betula pendula. The group with species vulnerable to abiotic stressors but not to biotic agents comprised Acer pseudoplatanus, Fagus sylvatica, Juniperus communis, Pinus halepensis, Quercus faginea, Quercus ilex, Quercus petraea, Quercus pubescens, Sorbus aucuparia and Tilia cordata. The group with species less vulnerable to abiotic stressors but more to biotic agents comprised Alnus glutinosa, Castanea sativa, Picea abies, and Ulmus glabra. The group with tree species highly vulnerable to both biotic and abiotic stressors included Abies alba, Fraxinus excelsior, Pinus nigra, Pinus pinaster, Pinus sylvestris and Quercus suber. We also documented 13 key functional traits for these species. The 4 response groups of tree species were significantly discriminated using the 13 life trait values and the matrix of confusion revealed a rate of good classification (right allocation of species to a priori groups) equal to 100 % for the four groups. The groups of species highly vulnerable to abiotic stresses were mainly characterised by low water stress tolerance whereas the groups of species vulnerable to biotic stresses are mainly characterised by high leaf nitrogen content, i.e. high leaf palatability for forest insects and pathogens. The least vulnerable group (low-low) combines high stress tolerance and low leaf nitrogen content. Our analysis has demonstrated that it seems possible to predict the vulnerability to biotic and abiotic agents of the main European tree species on the basis of their functional traits. The construction of such functional groups of tree species response to climate and pest and pathogens stressors provides forest managers with new tools to better anticipate the effect of climate change on the functioning of their forests according to their composition. It also gives some useful indication about the response of any other tree species, e.g. exotic, not included in our analysis, but for which the same life traits are known and quantified. By projecting these values in the same plan defined by the 13 traits or by drought tolerance and leaf nitrogen content, one might be able to evaluate the relative vulnerability of this additional tree species.
A growing body of evidence, including those produced by the project, suggests a positive relationship between tree species diversity and forest productivity. Within the BACCARA project we have also shown that tree species diversity can provide other ecosystem services. Using a meta-analysis of the scientific literature, we have demonstrated a consistent and positive relationship between tree species diversity and species richness of mammals, birds and arthropods, thus substantiating the 'biodiversity for biodiversity' concept. We have also shown that mixed forests are overall more resistant to pest insects than pure forests However a majority of these studies have pointed out the importance of species composition which is often more relevant than the number of species per se to explain the relationship between biodiversity and ecosystem functioning. Some tree species assemblages can be 'unlucky', being less productive or more vulnerable due to the 'wrong' assemblage of individual tree species. Furthermore, mixed forests are often considered as more complicate to manage than pure forests due to different requirement by different tree species or different growth phenology. The cost of establishment and maintenance of mixed forests might be also higher. There are therefore a large number of criteria to take into account when it comes to decide about growing trees as pure vs. mixed forest stands. Some of these criteria will have to be maximised, some other minimised. These criteria are also quantified in different manners, with different units. Criteria may also have different importance or relevance and thus not account with the same weight in the decision. It is therefore very difficult to integrate all these information to find the best compromise and make the right decision about converting pure to mixed forests. This is where multi criteria decision analysis (MCDA) tools can be useful. MCDA has been developed to help rank several alternatives from the worst to the best based on multiple, often conflicting criteria. One of the main advantages of MCDA is that it allows consideration of a large number of criteria that may be measured on completely different scales. We developed a pilot study using this approach. We focused on Scots pine (Pinus sylvestris), Norway spruce (Picea abies) and birch (Betula pendula) in the boreal, hemiboreal and alpine coniferous European forest types because we had the requisite information about their functioning in pure vs. mixed stands. We considered three criteria related to productivity (wood productivity, resistance to pest damage, stability of primary production), two criteria related to biodiversity conservation (species richness of birds and arthropods) and one criterion related to financial risk (standard deviation of the net present value). We could document these 6 criteria for the seven possible combinations of one, two and three of these tree species. Giving similar weight to the six criteria we found that overall mixed stands were preferred to pure stands, notably those composed of a mixture of broadleaved and coniferous species. The objective of this analysis was not to provide forest owners with the ultimate forest composition to be grown in northern Europe in the climate change context. The aim of this pilot study was rather to propose a method to integrate different criteria in order to make a decision about converting mono-species into mixed-species forests. It will be the choice and the responsibility of the user to add or delete some criteria, change their values and reduce the list of possible tree species, depending for example on local site conditions and wood market demand. Then forest advisors will also have the possibility to test the effect of changing the weights of criteria, first to see whether the forest type ranking is consistent or not (a sensitivity test), and second to consider different forest ecosystem services.
Potential impact:
Based on empirical data collected along elevation gradients in Europe and also on literature reviews, several features have been identified about forest pest insects and pathogens that can explain and then predict their response to increasing temperature and drought. According to this classification, 'What-to-combat'? guidelines have been produced in the form of an electronic database. In total, 83 data sheets on the main European forest pests and disease will be soon available where are presented a brief description of the biology, symptoms, identification key and an assessment of the actual and potential effects of climate change on distribution, abundance and damage.
A thorough review of the literature together with the empirical knowledge accumulated during the project made it possible to classify the 24 most abundant European forest species according to four levels of vulnerability to biotic and abiotic stressors triggered by climate change. In addition, several tree attributes (life traits and response patterns) were identified that could explain this categorisation. Furthermore we propose 'what-to-grow'? guidelines explaining how to integrate these characteristics and other socio-economic features in a MCDA tool in order to help forest managers identifying the tree species to introduce, maintain or abandon, in the current climate change context.
The analysis of forest inventory data from all around Europe clearly showed that mixed forests are more productive than monocultures in most European forest types. These results are confirmed by simulations run with forest succession models. Converging results have been also obtained from meta-analyses of the scientific literature and empirical data of experiments demonstrating associational resistance (i.e. lower damage in mixed forests) against forest insect specialists. Forest mixtures would be also more able to buffer negative impacts of climate change on key tree species. All these outcomes strongly suggest enhancing tree species diversity at the stand level to sustain forest ecosystem productivity in the context of climate change. In the line with this recommendation, we propose a decision analysis tool that integrates multiple ecological and socio-economic criteria in order to help forest managers making decision when they want to convert tree monocultures in mixed forests.
Analysis of the publications
Until now the project has produced 44 scientific publications in peer reviewed journals, four are currently submitted and many are still in preparation. The target review are mainly in the field of ecology, including two papers already published in Ecology Letters which ranks first in terms of impact factor. Papers have also been published in entomology, pathology and forestry journals.
Five Master students and eight Doctor of Philosophy (PhD) students will or have successfully defended their work with the full help of the BACCARA project (in total 25 were partially helped by the project).
More than 100 communications (oral and poster) have been presented in national and international scientific conference to disseminate the outcomes of the project.
Furthermore, 23 interviews in the radio and television media have been given to explain the objectives and findings of the project to the large public audience.
Project website: http://www.baccara-project.eu/