Agrochemicals interact synergistically to increase bee mortality.

Global concern over widely documented declines in pollinators1-3 has led to the identification of anthropogenic stressors that, individually, are detrimental to bee populations4-7. Synergistic interactions between these stressors could substantially amplify the environmental effect of these stressors and could therefore have important implications for policy decisions that aim to improve the health of pollinators3,8,9. Here, to quantitatively assess the scale of this threat, we conducted a meta-analysis of 356 interaction effect sizes from 90 studies in which bees were exposed to combinations of agrochemicals, nutritional stressors and/or parasites. We found an overall synergistic effect between multiple stressors on bee mortality. Subgroup analysis of bee mortality revealed strong evidence for synergy when bees were exposed to multiple agrochemicals at field-realistic levels, but interactions were not greater than additive expectations when bees were exposed to parasites and/or nutritional stressors. All interactive effects on proxies of fitness, behaviour, parasite load and immune responses were either additive or antagonistic; therefore, the potential mechanisms that drive the observed synergistic interactions for bee mortality remain unclear. Environmental risk assessment schemes that assume additive effects of the risk of agrochemical exposure may underestimate the interactive effect of anthropogenic stressors on bee mortality and will fail to protect the pollinators that provide a key ecosystem service that underpins sustainable agriculture.

Tree diversity enhances predation by birds but not by arthropods across climate gradients.

Tree diversity can promote both predator abundance and diversity. However, whether this translates into increased predation and top-down control of herbivores across predator taxonomic groups and contrasting environmental conditions remains unresolved. We used a global network of tree diversity experiments (TreeDivNet) spread across three continents and three biomes to test the effects of tree species richness on predation across varying climatic conditions of temperature and precipitation. We recorded bird and arthropod predation attempts on plasticine caterpillars in monocultures and tree species mixtures. Both tree species richness and temperature increased predation by birds but not by arthropods. Furthermore, the effects of tree species richness on predation were consistent across the studied climatic gradient. Our findings provide evidence that tree diversity strengthens top-down control of insect herbivores by birds, underscoring the need to implement conservation strategies that safeguard tree diversity to sustain ecosystem services provided by natural enemies in forests.

Meta-analysis and the science of research synthesis.

Meta-analysis is the quantitative, scientific synthesis of research results. Since the term and modern approaches to research synthesis were first introduced in the 1970s, meta-analysis has had a revolutionary effect in many scientific fields, helping to establish evidence-based practice and to resolve seemingly contradictory research outcomes. At the same time, its implementation has engendered criticism and controversy, in some cases general and others specific to particular disciplines. Here we take the opportunity provided by the recent fortieth anniversary of meta-analysis to reflect on the accomplishments, limitations, recent advances and directions for future developments in the field of research synthesis.

Publication bias impacts on effect size, statistical power, and magnitude (Type M) and sign (Type S) errors in ecology and evolutionary biology.

Collaborative efforts to directly replicate empirical studies in the medical and social sciences have revealed alarmingly low rates of replicability, a phenomenon dubbed the 'replication crisis'. Poor replicability has spurred cultural changes targeted at improving reliability in these disciplines. Given the absence of equivalent replication projects in ecology and evolutionary biology, two inter-related indicators offer the opportunity to retrospectively assess replicability: publication bias and statistical power. This registered report assesses the prevalence and severity of small-study (i.e., smaller studies reporting larger effect sizes) and decline effects (i.e., effect sizes decreasing over time) across ecology and evolutionary biology using 87 meta-analyses comprising 4,250 primary studies and 17,638 effect sizes. Further, we estimate how publication bias might distort the estimation of effect sizes, statistical power, and errors in magnitude (Type M or exaggeration ratio) and sign (Type S). We show strong evidence for the pervasiveness of both small-study and decline effects in ecology and evolution. There was widespread prevalence of publication bias that resulted in meta-analytic means being over-estimated by (at least) 0.12 standard deviations. The prevalence of publication bias distorted confidence in meta-analytic results, with 66% of initially statistically significant meta-analytic means becoming non-significant after correcting for publication bias. Ecological and evolutionary studies consistently had low statistical power (15%) with a 4-fold exaggeration of effects on average (Type M error rates = 4.4). Notably, publication bias reduced power from 23% to 15% and increased type M error rates from 2.7 to 4.4 because it creates a non-random sample of effect size evidence. The sign errors of effect sizes (Type S error) increased from 5% to 8% because of publication bias. Our research provides clear evidence that many published ecological and evolutionary findings are inflated. Our results highlight the importance of designing high-power empirical studies (e.g., via collaborative team science), promoting and encouraging replication studies, testing and correcting for publication bias in meta-analyses, and adopting open and transparent research practices, such as (pre)registration, data- and code-sharing, and transparent reporting.

Introducing our series: research synthesis and meta-research in biology.

Research synthesis is the process of bringing together findings and attributes from different publications, for example, to give a more complete description of phenomena than is usually possible in a single work. We bring the Research Synthesis Series to BMC Biology to promote meta-analyses, other research syntheses including meta-research studies, and research synthesis methodologies in biology, facilitating their dissemination to broader communities.

Biotic predictors complement models of bat and bird responses to climate and tree diversity in European forests.

Bats and birds are key providers of ecosystem services in forests. How climate and habitat jointly shape their communities is well studied, but whether biotic predictors from other trophic levels may improve bird and bat diversity models is less known, especially across large bioclimatic gradients. Here, we achieved multi-taxa surveys in 209 mature forests replicated in six European countries from Spain to Finland, to investigate the importance of biotic predictors (i.e. the abundance or activity of defoliating insects, spiders, earthworms and wild ungulates) for bat and bird taxonomic and functional diversity. We found that nine out of 12 bird and bat diversity metrics were best explained when biotic factors were added to models including climate and habitat variables, with a mean gain in explained variance of 38% for birds and 15% for bats. Tree functional diversity was the most important habitat predictor for birds, while bats responded more to understorey structure. The best biotic predictors for birds were spider abundance and defoliating insect activity, while only bat functional evenness responded positively to insect herbivory. Accounting for potential biotic interactions between bats, birds and other taxa of lower trophic levels will help to understand how environmental changes along large biogeographical gradients affect higher-level predator diversity in forest ecosystems.

Meta-analysis of the role of entomopathogenic and unspecialized fungal endophytes as plant bodyguards.

Herbaceous plants harbour species-rich communities of asymptomatic endophytic fungi. Although some of these endophytes are entomopathogenic, many are not, and remarkably little is known about how the presence of these fungi in plant tissues affects phytophagous insects. Here we show through a meta-analysis that both entomopathogenic and nonentomopathogenic endophytes have a negative effect on insect herbivores. Growth and performance of polyphagous and sucking insects are reduced by nonentomopathogenic endophytes, but monophages are unaffected, likely because the latter are better adapted to secondary metabolites produced or induced by the fungi. Furthermore, studies using excised leaves report weaker effects than those with intact plants, likely caused by chemical changes being masked by leaf excision. Most surprisingly, endophyte infection of seeds produces the greatest effect on insect herbivores in subsequent mature plants, even though the usual mode of fungal transmission is infection of leaves by airborne spores. We conclude that these ubiquitous hidden fungi may be important bodyguards of plants. However, in order to fully understand their roles in plant protection, we must be aware that minor differences in experimental design can lead to contradictory results.

Forest diversity effects on insect herbivores: do leaf traits matter?

Insect herbivore damage and abundance are often reduced in diverse plant stands. However, few studies have explored whether this phenomenon is a result of plant diversity effects on host plant traits. We explored indirect effects of tree species diversity on herbivory via changes in leaf traits in a long-term forest diversity experiment in Finland. We measured 16 leaf traits and leaf damage by four insect guilds (chewers, gall formers, leaf miners and rollers) on silver birch (Betula pendula) trees growing in one-, two-, three- and five-species mixtures. A decline in the frequency of birch in mixed stands resulted in reduced leaf area. This, in turn, mediated the reduction in chewing damage in mixed stands. In contrast, associational resistance of birch to leaf miners was not trait-mediated but driven directly by concurrent declines in birch frequency as tree species richness increased. Our results show that leaf trait variation across the diversity gradient might promote associational resistance, but these patterns are driven by an increase in the relative abundance of heterospecifics rather than by tree species richness per se. Therefore, accounting for concurrent changes in stand structure and key foliar traits is important for the interpretation of plant diversity effects and predictions of associational patterns.

Contrasting effects of tree species and genetic diversity on the leaf-miner communities associated with silver birch.

Both species and genetic diversity of plant communities can affect insect herbivores, but a few studies have compared the effects of both diversity levels within the same experimental context. We compared the effects of tree species and genetic diversity on abundance, species richness, and ß-diversity of leaf-miner communities associated with silver birch using two long-term forest diversity experiments in Finland where birch trees were planted in monocultures and mixtures of birch genotypes or other trees species. Although both abundance and species richness of leaf miners differed among birch genotypes at the tree level, birch genetic diversity had no significant effect on miner abundance and species richness at the plot level. Instead, birch genetic diversity affected leaf-miner ß-diversity with species turnover being higher among trees within genotypic mixtures than among trees within monoclonal plots. In contrast, tree species diversity had a significant negative effect on both leaf-miner abundance and species richness at plot level, but no effect on miner ß-diversity. Significant tree species diversity effects on leaf-miner abundance and species richness were found only in plots with high tree density. We have demonstrated that plant species and genetic diversity play important but contrasting roles in structuring associated herbivore communities. Tree species diversity largely affects miner abundance and species richness, whereas tree genetic diversity affects miner ß-diversity. These results have important implications for conservation and management of woodlands.

Biotic homogenization can decrease landscape-scale forest multifunctionality.

Many experiments have shown that local biodiversity loss impairs the ability of ecosystems to maintain multiple ecosystem functions at high levels (multifunctionality). In contrast, the role of biodiversity in driving ecosystem multifunctionality at landscape scales remains unresolved. We used a comprehensive pan-European dataset, including 16 ecosystem functions measured in 209 forest plots across six European countries, and performed simulations to investigate how local plot-scale richness of tree species (α-diversity) and their turnover between plots (ß-diversity) are related to landscape-scale multifunctionality. After accounting for variation in environmental conditions, we found that relationships between α-diversity and landscape-scale multifunctionality varied from positive to negative depending on the multifunctionality metric used. In contrast, when significant, relationships between ß-diversity and landscape-scale multifunctionality were always positive, because a high spatial turnover in species composition was closely related to a high spatial turnover in functions that were supported at high levels. Our findings have major implications for forest management and indicate that biotic homogenization can have previously unrecognized and negative consequences for large-scale ecosystem multifunctionality.

Continental mapping of forest ecosystem functions reveals a high but unrealised potential for forest multifunctionality.

Humans require multiple services from ecosystems, but it is largely unknown whether trade-offs between ecosystem functions prevent the realisation of high ecosystem multifunctionality across spatial scales. Here, we combined a comprehensive dataset (28 ecosystem functions measured on 209 forest plots) with a forest inventory dataset (105,316 plots) to extrapolate and map relationships between various ecosystem multifunctionality measures across Europe. These multifunctionality measures reflected different management objectives, related to timber production, climate regulation and biodiversity conservation/recreation. We found that trade-offs among them were rare across Europe, at both local and continental scales. This suggests a high potential for 'win-win' forest management strategies, where overall multifunctionality is maximised. However, across sites, multifunctionality was on average 45.8-49.8% below maximum levels and not necessarily highest in protected areas. Therefore, using one of the most comprehensive assessments so far, our study suggests a high but largely unrealised potential for management to promote multifunctional forests.

Biodiversity and ecosystem functioning relations in European forests depend on environmental context.

The importance of biodiversity in supporting ecosystem functioning is generally well accepted. However, most evidence comes from small-scale studies, and scaling-up patterns of biodiversity-ecosystem functioning (B-EF) remains challenging, in part because the importance of environmental factors in shaping B-EF relations is poorly understood. Using a forest research platform in which 26 ecosystem functions were measured along gradients of tree species richness in six regions across Europe, we investigated the extent and the potential drivers of context dependency of B-EF relations. Despite considerable variation in species richness effects across the continent, we found a tendency for stronger B-EF relations in drier climates as well as in areas with longer growing seasons and more functionally diverse tree species. The importance of water availability in driving context dependency suggests that as water limitation increases under climate change, biodiversity may become even more important to support high levels of functioning in European forests.

Do birds see the forest for the trees? Scale-dependent effects of tree diversity on avian predation of artificial larvae.

The enemies hypothesis states that reduced insect herbivory in mixed-species stands can be attributed to more effective top-down control by predators with increasing plant diversity. Although evidence for this mechanism exists for invertebrate predators, studies on avian predation are comparatively rare and have not explicitly tested the effects of diversity at different spatial scales, even though heterogeneity at macro- and micro-scales can influence bird foraging selection. We studied bird predation in an established forest diversity experiment in SW Finland, using artificial larvae installed on birch, alder and pine trees. Effects of tree species diversity and densities on bird predation were tested at two different scales: between plots and within the neighbourhood around focal trees. At the neighbourhood scale, birds preferentially foraged on focal trees surrounded by a higher diversity of neighbours. However, predation rates did not increase with tree species richness at the plot level and were instead negatively affected by tree height variation within the plot. The highest probability of predation was observed on pine, and rates of predation increased with the density of pine regardless of scale. Strong tree species preferences observed may be due to a combination of innate bird species preferences and opportunistic foraging on profitable-looking artificial prey. This study therefore finds partial support for the enemies hypothesis and highlights the importance of spatial scale and focal tree species in modifying trophic interactions between avian predators and insect herbivores in forest ecosystems.

Assessment of temporal instability in the applied ecology and conservation evidence base.

Outcomes of meta-analyses are increasingly used to inform evidence-based decision making in various research fields. However, a number of recent studies have reported rapid temporal changes in magnitude and significance of the reported effects which could make policy-relevant recommendations from meta-analyses to quickly go out of date. We assessed the extent and patterns of temporal trends in magnitude and statistical significance of the cumulative effects in meta-analyses in applied ecology and conservation published between 2004 and 2018. Of the 121 meta-analyses analysed, 93% showed a temporal trend in cumulative effect magnitude or significance with 27% of the datasets exhibiting temporal trends in both. The most common trend was the early study effect when at least one of the first 5 years effect size estimates exhibited more than 50% magnitude difference to the subsequent estimate. The observed temporal trends persisted in majority of datasets once moderators were accounted for. Only 5 datasets showed significant changes in sample size over time which could potentially explain the observed temporal change in the cumulative effects. Year of publication of meta-analysis had no significant effect on presence of temporal trends in cumulative effects. Our results show that temporal changes in magnitude and statistical significance in applied ecology are widespread and represent a serious potential threat to use of meta-analyses for decision-making in conservation and environmental management. We recommend use of cumulative meta-analyses and call for more studies exploring the causes of the temporal effects.

Effects of plant diversity on productivity strengthen over time due to trait-dependent shifts in species overyielding.

Plant diversity effects on community productivity often increase over time. Whether the strengthening of diversity effects is caused by temporal shifts in species-level overyielding (i.e., higher species-level productivity in diverse communities compared with monocultures) remains unclear. Here, using data from 65 grassland and forest biodiversity experiments, we show that the temporal strength of diversity effects at the community scale is underpinned by temporal changes in the species that yield. These temporal trends of species-level overyielding are shaped by plant ecological strategies, which can be quantitatively delimited by functional traits. In grasslands, the temporal strengthening of biodiversity effects on community productivity was associated with increasing biomass overyielding of resource-conservative species increasing over time, and with overyielding of species characterized by fast resource acquisition either decreasing or increasing. In forests, temporal trends in species overyielding differ when considering above- versus belowground resource acquisition strategies. Overyielding in stem growth decreased for species with high light capture capacity but increased for those with high soil resource acquisition capacity. Our results imply that a diversity of species with different, and potentially complementary, ecological strategies is beneficial for maintaining community productivity over time in both grassland and forest ecosystems.

Effects of tree species richness and composition on moose winter browsing damage and foraging selectivity: an experimental study.

The optimal foraging theory, the nutrient balance hypothesis, and the plant association theories predict that foraging decisions and resulting tree damage by large mammalian browsers may be influenced by the species richness and species composition of forest stands. This may lead to either associational susceptibility (increased damage on a focal plant in a mixed stand) or associational resistance (reduced damage in a mixed stand). Better understanding of the mechanisms and the relative importance of tree species richness and composition effects on foraging by mammalian browsers is needed to support sustainable management of forests and mammal populations. However, existing knowledge of forest diversity effects on foraging by large mammalian browsers comes largely from observational studies while experimental evidence is limited. We analysed winter browsing by moose (Alces alces L.) in a long-term, large-scale experiment in Finland, which represents a tree species richness gradient from monocultures to 2-, 3- and 5-species mixtures composed of Scots pine (Pinus sylvestris L.), Norway spruce (Picea abies L.), Siberian larch (Larix sibirica Ledeb.), silver birch (Betula pendula Roth.) and black alder (Alnus glutinosa L.). The intensity of browsing per plot increased with tree species richness while browsing selectivity decreased with tree species being targeted more equally in species-rich mixtures. Tree species composition of a plot was also an important determinant of intensity of browsing. The greatest browsing occurred in plots containing preferred species (pine and birch) while intermediate preference species (larch and alder) experienced associational susceptibility when growing with pine and birch compared with their monocultures or mixtures without pine and birch. In contrast, we found no evidence of associational resistance; the presence of a least preferred species (spruce) in a mixture had no significant effect on moose browsing on other tree species. We demonstrate that the presence of alternative forage species allows moose to spend longer opportunistically foraging in a plot, resulting in increased level of damage in species-rich stands and stands containing preferred tree species. Our results highlight the limitations of the optimal foraging theory in predicting browsing patterns and demonstrate the importance of associational effects within mixed stands.

Plant neighbourhood diversity effects on leaf traits: A meta-analysis.

Leaf traits often vary with plant neighbourhood composition, which in turn may mediate plant susceptibility to herbivory. However, it is unknown whether there are any common patterns of change in leaf trait expression in response to neighbourhood diversity, and whether these responses confer increased resistance or susceptibility to herbivores.We used meta-analysis to combine data from 43 studies that examined the influence of neighbourhood diversity on eight physical and chemical leaf traits that could affect herbivory. All leaf traits apart from leaf thickness were highly plastic and exhibited significant differences between plant monocultures and species mixtures, but the direction of effect was variable. Leaf toughness was the only trait that displayed a significant decrease with plant diversity, whereas specific leaf area (SLA) and leaf nitrogen were both marginally increased in species mixtures.The magnitude and direction of leaf trait responses to neighbourhood diversity were independent of plant density and phylogenetic diversity, but changes in SLA correlated positively with plant species richness. SLA was also significantly increased in experimental studies, but not in observational studies, while neighbourhoods containing nitrogen-fixers were associated with increased leaf nitrogen and reduced phenolics. When studies on the over-represented species Betula pendula were removed from the analysis, the effect of neighbourhood diversity on leaf toughness became nonsignificant, but phenolics were significantly reduced in diverse neighbourhoods composed of mature trees, and marginally reduced in species mixtures across all studies.Increases in plant neighbourhood diversity are often associated with reductions of herbivory, although in some cases, the reverse occurs, and plants growing in species mixtures are found to suffer greater herbivory than those in monocultures. This study offers a potential explanation for the latter phenomenon, as our results show that leaf trait expression is highly plastic in response to neighbourhood diversity, and in certain cases could lead to increased leaf quality, which in turn could promote greater rates of herbivory. Read the free Plain Language Summary for this article on the Journal blog.

Aboveground-belowground herbivore interactions: a meta-analysis.

Research investigating interactions between aboveground (AG) and below-ground (BG) herbivores has been central to characterizing AG-BG linkages in terrestrial ecosystems, with many of these interactions forming the basis of complex food webs spanning the two subsystems. Despite the growing literature on the effects of AG and BG herbivores on each other, underlying patterns have been difficult to identify due to a high degree of context dependency. In this study, we present the first quantitative meta-analysis of AG and BG herbivore interactions. Previous global predictions, specifically that BG herbivores normally promoted AG herbivore performance and AG herbivores normally reduced BG herbivore performance, were not supported. Instead, the meta-analysis identified four factors that determined the outcome of AG-BG interactions. (1) Sequence of herbivore arrival on host plants was important, with BG herbivores promoting AG herbivore performance only when introduced to the plant simultaneously, whereas AG herbivores had negative effects on BG herbivores only when introduced first. (2) AG herbivores negatively affected BG herbivore survival but tended to increase population growth rates. (3) AG herbivores negatively affected BG herbivore performance on annual plants, but not on perennials, and these effects were observed more consistently in laboratory than field studies. (4) The type of herbivore was also important, with BG insect herbivores belonging to the order Diptera (i.e., true flies) having the strongest negative effects on AG herbivores. Coleoptera (i.e., beetles) species were the most widely investigated BG herbivores and had positive impacts on AG Homoptera (e.g., aphids), but negative effects on AG Hymenoptera (e.g., sawflies). The strongest negative outcomes for BG herbivores were seen when the AG herbivore was a Coleoptera species. We found no evidence for publication bias in AG-BG herbivore interaction literature and conclude that several biological and experimental factors are important for predicting the outcome of AG-BG herbivore interactions. The sequence of herbivore arrival on the host plant was among the most influential.