Temperature and water availability drive insect seasonality across a temperate and a tropical region.

The more insects there are, the more food there is for insectivores and the higher the likelihood for insect-associated ecosystem services. Yet, we lack insights into the drivers of insect biomass over space and seasons, for both tropical and temperate zones. We used 245 Malaise traps, managed by 191 volunteers and park guards, to characterize year-round flying insect biomass in a temperate (Sweden) and a tropical (Madagascar) country. Surprisingly, we found that local insect biomass was similar across zones. In Sweden, local insect biomass increased with accumulated heat and varied across habitats, while biomass in Madagascar was unrelated to the environmental predictors measured. Drivers behind seasonality partly converged: In both countries, the seasonality of insect biomass differed between warmer and colder sites, and wetter and drier sites. In Sweden, short-term deviations from expected season-specific biomass were explained by week-to-week fluctuations in accumulated heat, rainfall and soil moisture, whereas in Madagascar, weeks with higher soil moisture had higher insect biomass. Overall, our study identifies key drivers of the seasonal distribution of flying insect biomass in a temperate and a tropical climate. This knowledge is key to understanding the spatial and seasonal availability of insects-as well as predicting future scenarios of insect biomass change.

The effect of local habitat and spatial connectivity on urban seed predation.

PREMISE: During the last centuries, the area covered by urban landscapes is increasing all over the world. Urbanization can change local habitats and decrease connectivity among these habitats, with important consequences for species interactions. While several studies have found a major imprint of urbanization on plant-insect interactions, the effects of urbanization on seed predation remain largely unexplored. METHODS: We investigated the relative impact of sunlight exposure, leaf litter, and spatial connectivity on predation by moth and weevil larvae on acorns of the pedunculate oak across an urban landscape during 2018 and 2020. We also examined whether infestations by moths and weevils were independent of each other. RESULTS: While seed predation varied strongly among trees, seed predation was not related to differences in sunlight exposure, leaf litter, or spatial connectivity. Seed predation by moths and weevils was negatively correlated at the level of individual acorns in 2018, but positively correlated at the acorn and the tree level in 2020. CONCLUSIONS: Our study sets the baseline expectation that urban seed predators are unaffected by differences in sunlight exposure, leaf litter, and spatial connectivity. Overall, our findings suggest that the impact of local and spatial factors on insects within an urban context may depend on the species guild. Understanding the impact of local and spatial factors on biodiversity, food web structure, and ecosystem functioning can provide valuable insights for urban planning and management strategies aimed at promoting urban insect diversity.

Genetic composition and diversity of Arabica coffee in the crop's centre of origin and its impact on four major fungal diseases.

Conventional wisdom states that genetic variation reduces disease levels in plant populations. Nevertheless, crop species have been subject to a gradual loss of genetic variation through selection for specific traits during breeding, thereby increasing their vulnerability to biotic stresses such as pathogens. We explored how genetic variation in Arabica coffee sites in southwestern Ethiopia was related to the incidence of four major fungal diseases. Sixty sites were selected along a gradient of management intensity, ranging from nearly wild to intensively managed coffee stands. We used genotyping-by-sequencing of pooled leaf samples (pool-GBS) derived from 16 individual coffee shrubs in each of the 60 sites to assess the variation in genetic composition (multivariate: reference allele frequency) and genetic diversity (univariate: mean expected heterozygosity) between sites. We found that genetic composition had a clear spatial pattern and that genetic diversity was higher in less managed sites. The incidence of the four fungal diseases was related to the genetic composition of the coffee stands, but in a specific way for each disease. In contrast, genetic diversity was only related to the within-site variation of coffee berry disease, but not to the mean incidence of any of the four diseases across sites. Given that fungal diseases are major challenges of Arabica coffee in its native range, our findings that genetic composition of coffee sites impacted the major fungal diseases may serve as baseline information to study the molecular basis of disease resistance in coffee. Overall, our study illustrates the need to consider both host genetic composition and genetic diversity when investigating the genetic basis for variation in disease levels.

Global gene flow releases invasive plants from environmental constraints on genetic diversity.

When plants establish outside their native range, their ability to adapt to the new environment is influenced by both demography and dispersal. However, the relative importance of these two factors is poorly understood. To quantify the influence of demography and dispersal on patterns of genetic diversity underlying adaptation, we used data from a globally distributed demographic research network comprising 35 native and 18 nonnative populations of Plantago lanceolata Species-specific simulation experiments showed that dispersal would dilute demographic influences on genetic diversity at local scales. Populations in the native European range had strong spatial genetic structure associated with geographic distance and precipitation seasonality. In contrast, nonnative populations had weaker spatial genetic structure that was not associated with environmental gradients but with higher within-population genetic diversity. Our findings show that dispersal caused by repeated, long-distance, human-mediated introductions has allowed invasive plant populations to overcome environmental constraints on genetic diversity, even without strong demographic changes. The impact of invasive plants may, therefore, increase with repeated introductions, highlighting the need to constrain future introductions of species even if they already exist in an area.

The relationship between pathogen life-history traits and metapopulation dynamics.

Plant pathogen traits, such as transmission mode and overwintering strategy, may have important effects on dispersal and persistence, and drive disease dynamics. Still, we lack insights into how life-history traits influence spatiotemporal disease dynamics. We adopted a multifaceted approach, combining experimental assays, theory and field surveys, to investigate whether information about two pathogen life-history traits - infectivity and overwintering strategy - can predict pathogen metapopulation dynamics in natural systems. For this, we focused on four fungal pathogens (two rust fungi, one chytrid fungus and one smut fungus) on the forest herb Anemone nemorosa. Pathogens infecting new plants mostly via spores (the chytrid and smut fungi) had higher patch occupancies and colonization rates than pathogens causing mainly systemic infections and overwintering in the rhizomes (the two rust fungi). Although the rust fungi more often occupied well-connected plant patches, the chytrid and smut fungi were equally or more common in isolated patches. Host patch size was positively related to patch occupancy and colonization rates for all pathogens. Predicting disease dynamics is crucial for understanding the ecological and evolutionary dynamics of host-pathogen interactions, and to prevent disease outbreaks. Our study shows that combining experiments, theory and field observations is a useful way to predict disease dynamics.

Evidence for host-microbiome co-evolution in apple.

Plants evolved in association with a diverse community of microorganisms. The effect of plant phylogeny and domestication on host-microbiome co-evolutionary dynamics are poorly understood. Here we examined the effect of domestication and plant lineage on the composition of the endophytic microbiome of 11 Malus species, representing three major groups: domesticated apple (M. domestica), wild apple progenitors, and wild Malus species. The endophytic community of M. domestica and its wild progenitors showed higher microbial diversity and abundance than wild Malus species. Heirloom and modern cultivars harbored a distinct community composition, though the difference was not significant. A community-wide Bayesian model revealed that the endophytic microbiome of domesticated apple is an admixture of its wild progenitors, with clear evidence for microbiome introgression, especially for the bacterial community. We observed a significant correlation between the evolutionary distance of Malus species and their microbiome. This study supports co-evolution between Malus species and their microbiome during domestication. This finding has major implications for future breeding programs and our understanding of the evolution of plants and their microbiomes.

Elevation and plant species identity jointly shape a diverse arbuscular mycorrhizal fungal community in the High Arctic.

Knowledge about the distribution and local diversity patterns of arbuscular mycorrhizal (AM) fungi are limited for extreme environments such as the Arctic, where most studies have focused on spore morphology or root colonization. We here studied the joint effects of plant species identity and elevation on AM fungal distribution and diversity. We sampled roots of 19 plant species in 18 locations in Northeast Greenland, using next generation sequencing to identify AM fungi. We studied the joint effect of plant species, elevation and selected abiotic conditions on AM fungal presence, richness and composition. We identified 29 AM fungal virtual taxa (VT), of which six represent putatively new VT. Arbuscular mycorrhizal fungal presence increased with elevation, and as vegetation cover and the active soil layer decreased. Arbuscular mycorrhizal fungal composition was shaped jointly by elevation and plant species identity. We demonstrate that the Arctic harbours a relatively species-rich and nonrandomly distributed diversity of AM fungi. Given the high diversity and general lack of knowledge exposed herein, we encourage further research into the diversity, drivers and functional role of AM fungi in the Arctic. Such insight is urgently needed for an area with some of the globally highest rates of climate change.

The co-existence of multiple oak leaf flushes contributes to the large within-tree variation in chemistry, insect attack and pathogen infection.

Many plant species produce multiple leaf flushes during the growing season, which might have major consequences for within-plant variation in chemistry and species interactions. Yet, we lack a theoretical or empirical framework for how differences among leaf flushes might shape variation in damage by insects and diseases. We assessed the impact of leaf flush identity on leaf chemistry, insect attack and pathogen infection on the pedunculate oak Quercus robur by sampling leaves from each leaf flush in 20 populations across seven European countries during an entire growing season. The first leaf flush had higher levels of primary compounds, and lower levels of secondary compounds, than the second flush, whereas plant chemistry was highly variable in the third flush. Insect attack decreased from the first to the third flush, whereas infection by oak powdery mildew was lowest on leaves from the first flush. The relationship between plant chemistry, insect attack and pathogen infection varied strongly among leaf flushes and seasons. Our findings demonstrate the importance of considering differences among leaf flushes for our understanding of within-tree variation in chemistry, insect attack and disease levels, something particularly relevant given the expected increase in the number of leaf flushes with climate change.

Climate variability and aridity modulate the role of leaf shelters for arthropods: A global experiment.

Current climate change is disrupting biotic interactions and eroding biodiversity worldwide. However, species sensitive to aridity, high temperatures, and climate variability might find shelter in microclimatic refuges, such as leaf rolls built by arthropods. To explore how the importance of leaf shelters for terrestrial arthropods changes with latitude, elevation, and climate, we conducted a distributed experiment comparing arthropods in leaf rolls versus control leaves across 52 sites along an 11,790 km latitudinal gradient. We then probed the impact of short- versus long-term climatic impacts on roll use, by comparing the relative impact of conditions during the experiment versus average, baseline conditions at the site. Leaf shelters supported larger organisms and higher arthropod biomass and species diversity than non-rolled control leaves. However, the magnitude of the leaf rolls' effect differed between long- and short-term climate conditions, metrics (species richness, biomass, and body size), and trophic groups (predators vs. herbivores). The effect of leaf rolls on predator richness was influenced only by baseline climate, increasing in magnitude in regions experiencing increased long-term aridity, regardless of latitude, elevation, and weather during the experiment. This suggests that shelter use by predators may be innate, and thus, driven by natural selection. In contrast, the effect of leaf rolls on predator biomass and predator body size decreased with increasing temperature, and increased with increasing precipitation, respectively, during the experiment. The magnitude of shelter usage by herbivores increased with the abundance of predators and decreased with increasing temperature during the experiment. Taken together, these results highlight that leaf roll use may have both proximal and ultimate causes. Projected increases in climate variability and aridity are, therefore, likely to increase the importance of biotic refugia in mitigating the effects of climate change on species persistence.

Spring phenology and pathogen infection affect multigenerational plant attackers throughout the growing season.

Climate change has been shown to advance spring phenology, increase the number of insect generations per year (multivoltinism) and increase pathogen infection levels. However, we lack insights into the effects of plant spring phenology and the biotic environment on the preference and performance of multivoltine herbivores and whether such effects extend into the later part of the growing season. To this aim, we used a multifactorial growth chamber experiment to examine the influence of spring phenology on plant pathogen infection, and how the independent and interactive effects of spring phenology and plant pathogen infection affect the preference and performance of multigenerational attackers (the leaf miner Tischeria ekebladella and the aphid Tuberculatus annulatus) on the pedunculate oak in the early, mid and late parts of the plant growing season. Pathogen infection was highest on late phenology plants, irrespective of whether inoculations were conducted in the early, mid or late season. The leaf miner consistently preferred to oviposit on middle and late phenology plants, as well as healthy plants, during all parts of the growing season, whereas we detected an interactive effect between spring phenology and pathogen infection on the performance of the leaf miner. Aphids preferred healthy, late phenology plants during the early season, healthy plants during the mid season, and middle phenology plants during the late season, whereas aphid performance was consistently higher on healthy plants during all parts of the growing season. Our findings highlight that the impact of spring phenology on pathogen infection and the preference and performance of insect herbivores is not restricted to the early season, but that its imprint is still present - and sometimes equally strong - during the peak and end of the growing season. Plant pathogens generally negatively affected herbivore preference and performance, and modulated the effects of spring phenology. We conclude that spring phenology and pathogen infection are two important factors shaping the preference and performance of multigenerational plant attackers, which is particularly relevant given the current advance in spring phenology, pathogen outbreaks and increase in voltinism with climate change.

Phenotypic plasticity masks range-wide genetic differentiation for vegetative but not reproductive traits in a short-lived plant.

Genetic differentiation and phenotypic plasticity jointly shape intraspecific trait variation, but their roles differ among traits. In short-lived plants, reproductive traits may be more genetically determined due to their impact on fitness, whereas vegetative traits may show higher plasticity to buffer short-term perturbations. Combining a multi-treatment greenhouse experiment with observational field data throughout the range of a widespread short-lived herb, Plantago lanceolata, we (1) disentangled genetic and plastic responses of functional traits to a set of environmental drivers and (2) assessed how genetic differentiation and plasticity shape observational trait-environment relationships. Reproductive traits showed distinct genetic differentiation that largely determined observational patterns, but only when correcting traits for differences in biomass. Vegetative traits showed higher plasticity and opposite genetic and plastic responses, masking the genetic component underlying field-observed trait variation. Our study suggests that genetic differentiation may be inferred from observational data only for the traits most closely related to fitness.

Experimental evidence of microbial inheritance in plants and transmission routes from seed to phyllosphere and root.

While the environment is considered the primary origin of the plant microbiome, the potential role of seeds as a source of transmitting microorganisms has not received much attention. Here we tested the hypothesis that the plant microbiome is partially inherited through vertical transmission. An experimental culturing device was constructed to grow oak seedlings in a microbe-free environment while keeping belowground and aboveground tissues separated. The microbial communities associated with the acorn's embryo and pericarp and the developing seeding's phyllosphere and root systems were analysed using amplicon sequencing of fungal ITS and bacterial 16S rDNA. Results showed that the seed microbiome is diverse and non-randomly distributed within an acorn. The microbial composition of the phyllosphere was diverse and strongly resembled the composition found in the embryo, whereas the roots and pericarp each had a less diverse and distinct microbial community. Our findings demonstrate a high level of microbial diversity and spatial partitioning of the fungal and bacterial community within both seed and seedling, indicating inheritance, niche differentiation and divergent transmission routes for the establishment of root and phyllosphere communities.

Climate warming dominates over plant genotype in shaping the seasonal trajectory of foliar fungal communities on oak.

Leaves interact with a wealth of microorganisms. Among these, fungi are highly diverse and are known to contribute to plant health, leaf senescence and early decomposition. However, patterns and drivers of the seasonal dynamics of foliar fungal communities are poorly understood. We used a multifactorial experiment to investigate the influence of warming and tree genotype on the foliar fungal community on the pedunculate oak Quercus robur across one growing season. Fungal species richness increased, evenness tended to decrease, and community composition strongly shifted during the growing season. Yeasts increased in relative abundance as the season progressed, while putative fungal pathogens decreased. Warming decreased species richness, reduced evenness and changed community composition, especially at the end of the growing season. Warming also negatively affected putative fungal pathogens. We only detected a minor imprint of tree genotype and warming × genotype interactions on species richness and community composition. Overall, our findings demonstrate that warming plays a larger role than plant genotype in shaping the seasonal dynamics of the foliar fungal community on oak. These warming-induced shifts in the foliar fungal community may have a pronounced impact on plant health, plant-fungal interactions and ecosystem functions.

Effects of latitude and conspecific plant density on insect leaf herbivory in oak saplings and seedlings.

PREMISE: Abiotic factors and plant species traits have been shown to drive latitudinal gradients in herbivory, and yet, population-level factors have been largely overlooked within this context. One such factor is plant density, which may influence the strength of herbivory and may vary with latitude. METHODS: We measured insect herbivory and conspecific plant density (CPD) of oak (Quercus robur) seedlings and saplings along a 17° latitudinal gradient (2700 km) to test whether herbivory exhibited a latitudinal gradient, whether herbivory was associated with CPD, and whether such an association changed with latitude. RESULTS: We found a positive but saturating association between latitude and leaf herbivory. Furthermore, we found no significant relationship between CPD and herbivory, and such lack of density effects remained consistent throughout the sampled latitudinal gradient. CONCLUSIONS: Despite the apparently negligible influence of plant density on herbivory for Q. robur, further research with other plant taxa and in different types of plant communities are needed to investigate density-dependent processes shaping geographical variation in plant-herbivore interactions.

Pathogen infection influences the relationship between spring and autumn phenology at the seedling and leaf level.

Seasonal life history events are often interdependent, but we know relatively little about how the relationship between different events is influenced by the abiotic and biotic environment. Such knowledge is important for predicting the immediate and evolutionary phenological response of populations to changing conditions. We manipulated germination timing and shade in a multi-factorial experiment to investigate the relationship between spring and autumn phenology in seedlings of the pedunculate oak, Quercus robur, and whether this relationship was mediated by natural colonization of leaves by specialist fungal pathogens (i.e., the oak powdery mildew complex). Each week delay in germination corresponded to about 2 days delay in autumn leaf senescence, and heavily shaded seedlings senesced 5-8 days later than seedlings in light shade or full sun. Within seedlings, leaves on primary-growth shoots senesced later than those on secondary-growth shoots in some treatments. Path analyses demonstrated that germination timing and shade affected autumn phenology both directly and indirectly via pathogen load, though the specific pattern differed among and within seedlings. Pathogen load increased with later germination and greater shade. Greater pathogen load was in turn associated with later senescence for seedlings, but with earlier senescence for individual leaves. Our findings show that relationships between seasonal events can be partly mediated by the biotic environment and suggest that these relationships may differ between the plant and leaf level. The influence of biotic interactions on phenological correlations across scales has implications for understanding phenotypic variation in phenology and for predicting how populations will respond to climatic perturbation.

The timing and asymmetry of plant-pathogen-insect interactions.

Insects and pathogens frequently exploit the same host plant and can potentially impact each other's performance. However, studies on plant-pathogen-insect interactions have mainly focused on a fixed temporal setting or on a single interaction partner. In this study, we assessed the impact of time of attacker arrival on the outcome and symmetry of interactions between aphids (Tuberculatus annulatus), powdery mildew (Erysiphe alphitoides), and caterpillars (Phalera bucephala) feeding on pedunculate oak, Quercus robur, and explored how single versus multiple attackers affect oak performance. We used a multifactorial greenhouse experiment in which oak seedlings were infected with either zero, one, two, or three attackers, with the order of attacker arrival differing among treatments. The performances of all involved organisms were monitored throughout the experiment. Overall, attackers had a weak and inconsistent impact on plant performance. Interactions between attackers, when present, were asymmetric. For example, aphids performed worse, but powdery mildew performed better, when co-occurring. Order of arrival strongly affected the outcome of interactions, and early attackers modified the strength and direction of interactions between later-arriving attackers. Our study shows that interactions between plant attackers can be asymmetric, time-dependent, and species specific. This is likely to shape the ecology and evolution of plant-pathogen-insect interactions.

Accounting for environmental variation in co-occurrence modelling reveals the importance of positive interactions in root-associated fungal communities.

Understanding the role of interspecific interactions in shaping ecological communities is one of the central goals in community ecology. In fungal communities, measuring interspecific interactions directly is challenging because these communities are composed of large numbers of species, many of which are unculturable. An indirect way of assessing the role of interspecific interactions in determining community structure is to identify the species co-occurrences that are not constrained by environmental conditions. In this study, we investigated co-occurrences among root-associated fungi, asking whether fungi co-occur more or less strongly than expected based on the environmental conditions and the host plant species examined. We generated molecular data on root-associated fungi of five plant species evenly sampled along an elevational gradient at a high arctic site. We analysed the data using a joint species distribution modelling approach that allowed us to identify those co-occurrences that could be explained by the environmental conditions and the host plant species, as well as those co-occurrences that remained unexplained and thus more probably reflect interactive associations. Our results indicate that not only negative but also positive interactions play an important role in shaping microbial communities in arctic plant roots. In particular, we found that mycorrhizal fungi are especially prone to positively co-occur with other fungal species. Our results bring new understanding to the structure of arctic interaction networks by suggesting that interactions among root-associated fungi are predominantly positive.

Latitudinal variation in seed predation correlates with latitudinal variation in seed defensive and nutritional traits in a widespread oak species.

BACKGROUND AND AIMS: Classic theory on geographical gradients in plant-herbivore interactions assumes that herbivore pressure and plant defences increase towards warmer and more stable climates found at lower latitudes. However, the generality of these expectations has been recently called into question by conflicting empirical evidence. One possible explanation for this ambiguity is that most studies have reported on patterns of either herbivory or plant defences whereas few have measured both, thus preventing a full understanding of the implications of observed patterns for plant-herbivore interactions. In addition, studies have typically not measured climatic factors affecting plant-herbivore interactions, despite their expected influence on plant and herbivore traits. METHODS: Here we tested for latitudinal variation in insect seed predation and seed traits putatively associated with insect attack across 36 Quercus robur populations distributed along a 20° latitudinal gradient. We then further investigated the associations between climatic factors, seed traits and seed predation to test for climate-based mechanisms of latitudinal variation in seed predation. KEY RESULTS: We found strong but contrasting latitudinal clines in seed predation and seed traits, whereby seed predation increased whereas seed phenolics and phosphorus decreased towards lower latitudes. We also found a strong direct association between temperature and seed predation, with the latter increasing towards warmer climates. In addition, temperature was negatively associated with seed traits, with populations at warmer sites having lower levels of total phenolics and phosphorus. In turn, these negative associations between temperature and seed traits led to a positive indirect association between temperature and seed predation. CONCLUSIONS: These results help unravel how plant-herbivore interactions play out along latitudinal gradients and expose the role of climate in driving these outcomes through its dual effects on plant defences and herbivores. Accordingly, this emphasizes the need to account for abiotic variation while testing concurrently for latitudinal variation in plant traits and herbivore pressure.

Host plant phenology, insect outbreaks and herbivore communities - The importance of timing.

Climate change may alter the dynamics of outbreak species by changing the phenological synchrony between herbivores and their host plants. As host plant phenology has a genotypic component that may interact with climate, infestation levels among genotypes might change accordingly. When the outbreaking herbivore is active early in the season, its infestation levels may also leave a detectable imprint on herbivores colonizing the plant later in the season. In this study, we first investigated how the spring phenology and genotype of Quercus robur influenced the density of the spring-active, outbreaking leaf miner Acrocercops brongniardellus. We then assessed how intraspecific density affected the performance of A. brongniardellus and how oak genotype and density of A. brongniardellus affected the insect herbivore community. We found that Q. robur individuals of late spring phenology were more strongly infested by A. brongniardellus. Conspecific pupae on heavily infested oaks tended to be lighter, and fewer heterospecific insect herbivores colonized the oak later in the season. Beyond its effects through phenology, plant genotype left an imprint on herbivore species richness and on two insect herbivores. Our results suggest a chain of knock-on effects from plant phenology, through the outbreaking species to the insect herbivore community. Given the finding of how phenological synchrony between the outbreak species and its host plant influences infestation levels, a shift in synchrony may then change outbreak dynamics and cause cascading effects on the insect community.

Multiscale patterns and drivers of arbuscular mycorrhizal fungal communities in the roots and root-associated soil of a wild perennial herb.

Arbuscular mycorrhizal (AM) fungi form diverse communities and are known to influence above-ground community dynamics and biodiversity. However, the multiscale patterns and drivers of AM fungal composition and diversity are still poorly understood. We sequenced DNA markers from roots and root-associated soil from Plantago lanceolata plants collected across multiple spatial scales to allow comparison of AM fungal communities among neighbouring plants, plant subpopulations, nearby plant populations, and regions. We also measured soil nutrients, temperature, humidity, and community composition of neighbouring plants and nonAM root-associated fungi. AM fungal communities were already highly dissimilar among neighbouring plants (c. 30 cm apart), albeit with a high variation in the degree of similarity at this small spatial scale. AM fungal communities were increasingly, and more consistently, dissimilar at larger spatial scales. Spatial structure and environmental drivers explained a similar percentage of the variation, from 7% to 25%. A large fraction of the variation remained unexplained, which may be a result of unmeasured environmental variables, species interactions and stochastic processes. We conclude that AM fungal communities are highly variable among nearby plants. AM fungi may therefore play a major role in maintaining small-scale variation in community dynamics and biodiversity.