Seasonal and elevational changes of plant-pollinator interaction networks in East African mountains.

Across an elevation gradient, several biotic and abiotic factors influence community assemblages of interacting species leading to a shift in species distribution, functioning, and ultimately topologies of species interaction networks. However, empirical studies of climate-driven seasonal and elevational changes in plant-pollinator networks are rare, particularly in tropical ecosystems. Eastern Afromontane Biodiversity Hotspots in Kenya, East Africa. We recorded plant-bee interactions at 50 study sites between 515 and 2600 m asl for a full year, following all four major seasons in this region. We analysed elevational and seasonal network patterns using generalised additive models (GAMs) and quantified the influence of climate, floral resource availability, and bee diversity on network structures using a multimodel inference framework. We recorded 16,741 interactions among 186 bee and 314 plant species of which a majority involved interactions with honeybees. We found that nestedness and bee species specialisation of plant-bee interaction networks increased with elevation and that the relationships were consistent in the cold-dry and warm-wet seasons respectively. Link rewiring increased in the warm-wet season with elevation but remained indifferent in the cold-dry seasons. Conversely, network modularity and plant species were more specialised at lower elevations during both the cold-dry and warm-wet seasons, with higher values observed during the warm-wet seasons. We found flower and bee species diversity and abundance rather than direct effects of climate variables to best predict modularity, specialisation, and link rewiring in plant-bee-interaction networks. This study highlights changes in network architectures with elevation suggesting a potential sensitivity of plant-bee interactions with climate warming and changes in rainfall patterns along the elevation gradients of the Eastern Afromontane Biodiversity Hotspot.

Enhancing the structural diversity between forest patches-A concept and real-world experiment to study biodiversity, multifunctionality and forest resilience across spatial scales.

Intensification of land use by humans has led to a homogenization of landscapes and decreasing resilience of ecosystems globally due to a loss of biodiversity, including the majority of forests. Biodiversity-ecosystem functioning (BEF) research has provided compelling evidence for a positive effect of biodiversity on ecosystem functions and services at the local (α-diversity) scale, but we largely lack empirical evidence on how the loss of between-patch ß-diversity affects biodiversity and multifunctionality at the landscape scale (γ-diversity). Here, we present a novel concept and experimental framework for elucidating BEF patterns at α-, ß-, and γ-scales in real landscapes at a forest management-relevant scale. We examine this framework using 22 temperate broadleaf production forests, dominated by Fagus sylvatica. In 11 of these forests, we manipulated the structure between forest patches by increasing variation in canopy cover and deadwood. We hypothesized that an increase in landscape heterogeneity would enhance the ß-diversity of different trophic levels, as well as the ß-functionality of various ecosystem functions. We will develop a new statistical framework for BEF studies extending across scales and incorporating biodiversity measures from taxonomic to functional to phylogenetic diversity using Hill numbers. We will further expand the Hill number concept to multifunctionality allowing the decomposition of γ-multifunctionality into α- and ß-components. Combining this analytic framework with our experimental data will allow us to test how an increase in between patch heterogeneity affects biodiversity and multifunctionality across spatial scales and trophic levels to help inform and improve forest resilience under climate change. Such an integrative concept for biodiversity and functionality, including spatial scales and multiple aspects of diversity and multifunctionality as well as physical and environmental structure in forests, will go far beyond the current widely applied approach in forestry to increase resilience of future forests through the manipulation of tree species composition.

Alpine butterflies want to fly high: Species and communities shift upwards faster than their host plants.

Despite sometimes strong codependencies of insect herbivores and plants, the responses of individual taxa to accelerating climate change are typically studied in isolation. For this reason, biotic interactions that potentially limit species in tracking their preferred climatic niches are ignored. Here, we chose butterflies as a prominent representative of herbivorous insects to investigate the impacts of temperature changes and their larval host plant distributions along a 1.4-km elevational gradient in the German Alps. Following a sampling protocol of 2009, we revisited 33 grassland plots in 2019 over an entire growing season. We quantified changes in butterfly abundance and richness by repeated transect walks on each plot and disentangled the direct and indirect effects of locally assessed temperature, site management, and larval and adult food resource availability on these patterns. Additionally, we determined elevational range shifts of butterflies and host plants at both the community and species level. Comparing the two sampled years (2009 and 2019), we found a severe decline in butterfly abundance and a clear upward shift of butterflies along the elevational gradient. We detected shifts in the peak of species richness, community composition, and at the species level, whereby mountainous species shifted particularly strongly. In contrast, host plants showed barely any change, neither in connection with species richness nor individual species shifts. Further, temperature and host plant richness were the main drivers of butterfly richness, with change in temperature best explaining the change in richness over time. We concluded that host plants were not yet hindering butterfly species and communities from shifting upwards. However, the mismatch between butterfly and host plant shifts might become a problem for this very close plant-herbivore relationship, especially toward higher elevations, if butterflies fail to adapt to new host plants. Further, our results support the value of conserving traditional extensive pasture use as a promoter of host plant and, hence, butterfly richness.

Temperature and livestock grazing trigger transcriptome responses in bumblebees along an elevational gradient.

Climate and land-use changes cause increasing stress to pollinators but the molecular pathways underlying stress responses are poorly understood. Here, we analyzed the transcriptomic response of Bombus lucorum workers to temperature and livestock grazing. Bumblebees sampled along an elevational gradient, and from differently managed grassland sites (livestock grazing vs unmanaged) in the German Alps did not differ in the expression of genes known for thermal stress responses. Instead, metabolic energy production pathways were upregulated in bumblebees sampled in mid- or high elevations or during cool temperatures. Extensive grazing pressure led to an upregulation of genetic pathways involved in immunoregulation and DNA-repair. We conclude that widespread bumblebees are tolerant toward temperature fluctuations in temperate mountain environments. Moderate temperature increases may even release bumblebees from metabolic stress. However, transcriptome responses to even moderate management regimes highlight the completely underestimated complexity of human influence on natural pollinators.

Contrasting patterns of richness, abundance, and turnover in mountain bumble bees and their floral hosts.

Environmental gradients generate and maintain biodiversity on Earth. Mountain slopes are among the most pronounced terrestrial environmental gradients, and the elevational structure of species and their interactions can provide unique insight into the processes that govern community assembly and function in mountain ecosystems. We recorded bumble bee-flower interactions over 3 years along a 1400-m elevational gradient in the German Alps. Using nonlinear modeling techniques, we analyzed elevational patterns at the levels of abundance, species richness, species ß-diversity, and interaction ß-diversity. Though floral richness exhibited a midelevation peak, bumble bee richness increased with elevation before leveling off at the highest sites, demonstrating the exceptional adaptation of these bees to cold temperatures and short growing seasons. In terms of abundance, though, bumble bees exhibited divergent species-level responses to elevation, with a clear separation between species preferring low versus high elevations. Overall interaction ß-diversity was mainly caused by strong turnover in the floral community, which exhibited a well-defined threshold of ß-diversity rate at the tree line ecotone. Interaction ß-diversity increased sharply at the upper extreme of the elevation gradient (1800-2000 m), an interval over which we also saw steep decline in floral richness and abundance. Turnover of bumble bees along the elevation gradient was modest, with the highest rate of ß-diversity occurring over the interval from low- to mid-elevation sites. The contrast between the relative robustness bumble bee communities and sensitivity of plant communities to the elevational gradient in our study suggests that the strongest effects of climate change on mountain bumble bees may be indirect effects mediated by the responses of their floral hosts, though bumble bee species that specialize in high-elevation habitats may also experience significant direct effects of warming.

Species richness is more important for ecosystem functioning than species turnover along an elevational gradient.

Many experiments have shown that biodiversity enhances ecosystem functioning. However, we have little understanding of how environmental heterogeneity shapes the effect of diversity on ecosystem functioning and to what extent this diversity effect is mediated by variation in species richness or species turnover. This knowledge is crucial to scaling up the results of experiments from local to regional scales. Here we quantify the diversity effect and its components-that is, the contributions of variation in species richness and species turnover-for 22 ecosystem functions of microorganisms, plants and animals across 13 major ecosystem types on Mt Kilimanjaro, Tanzania. Environmental heterogeneity across ecosystem types on average increased the diversity effect from explaining 49% to 72% of the variation in ecosystem functions. In contrast to our expectation, the diversity effect was more strongly mediated by variation in species richness than by species turnover. Our findings reveal that environmental heterogeneity strengthens the relationship between biodiversity and ecosystem functioning and that species richness is a stronger driver of ecosystem functioning than species turnover. Based on a broad range of taxa and ecosystem functions in a non-experimental system, these results are in line with predictions from biodiversity experiments and emphasize that conserving biodiversity is essential for maintaining ecosystem functioning.

Specialization of plant-pollinator interactions increases with temperature at Mt. Kilimanjaro.

AIM: Species differ in their degree of specialization when interacting with other species, with significant consequences for the function and robustness of ecosystems. In order to better estimate such consequences, we need to improve our understanding of the spatial patterns and drivers of specialization in interaction networks. METHODS: Here, we used the extensive environmental gradient of Mt. Kilimanjaro (Tanzania, East Africa) to study patterns and drivers of specialization, and robustness of plant-pollinator interactions against simulated species extinction with standardized sampling methods. We studied specialization, network robustness and other network indices of 67 quantitative plant-pollinator networks consisting of 268 observational hours and 4,380 plant-pollinator interactions along a 3.4 km elevational gradient. Using path analysis, we tested whether resource availability, pollinator richness, visitation rates, temperature, and/or area explain average specialization in pollinator communities. We further linked pollinator specialization to different pollinator taxa, and species traits, that is, proboscis length, body size, and species elevational ranges. RESULTS: We found that specialization decreased with increasing elevation at different levels of biological organization. Among all variables, mean annual temperature was the best predictor of average specialization in pollinator communities. Specialization differed between pollinator taxa, but was not related to pollinator traits. Network robustness against simulated species extinctions of both plants and pollinators was lowest in the most specialized interaction networks, that is, in the lowlands. CONCLUSIONS: Our study uncovers patterns in plant-pollinator specialization along elevational gradients. Mean annual temperature was closely linked to pollinator specialization. Energetic constraints, caused by short activity timeframes in cold highlands, may force ectothermic species to broaden their dietary spectrum. Alternatively or in addition, accelerated evolutionary rates might facilitate the establishment of specialization under warm climates. Despite the mechanisms behind the patterns have yet to be fully resolved, our data suggest that temperature shifts in the course of climate change may destabilize pollination networks by affecting network architecture.

Increasing the phylogenetic coverage for understanding broad-scale diversity gradients.

Despite decades of scientific effort, there is still no consensus on the determinants of broad-scale gradients of animal diversity. We argue that general drivers of diversity are unlikely to be found among the narrowly defined taxa which are typically analyzed in studies of broad-scale diversity gradients because ecological niches evolve largely conservatively. This causes constraints in the use of available niche space leading to systematic differences in diversity gradients among taxa. We instead advocate studies of phylogenetically diverse animal communities along broad environmental gradients. Such multi-taxa communities are less constrained in resource use and diversification and may be better targets for testing major classical hypotheses on diversity gradients. Besides increasing the spatial scale in analyses, expanding the phylogenetic coverage may be a second way to achieve higher levels of generality in studies of broad-scale diversity gradients.

A global synthesis reveals biodiversity-mediated benefits for crop production.

Human land use threatens global biodiversity and compromises multiple ecosystem functions critical to food production. Whether crop yield-related ecosystem services can be maintained by a few dominant species or rely on high richness remains unclear. Using a global database from 89 studies (with 1475 locations), we partition the relative importance of species richness, abundance, and dominance for pollination; biological pest control; and final yields in the context of ongoing land-use change. Pollinator and enemy richness directly supported ecosystem services in addition to and independent of abundance and dominance. Up to 50% of the negative effects of landscape simplification on ecosystem services was due to richness losses of service-providing organisms, with negative consequences for crop yields. Maintaining the biodiversity of ecosystem service providers is therefore vital to sustain the flow of key agroecosystem benefits to society.

Climate-land-use interactions shape tropical mountain biodiversity and ecosystem functions.

Agriculture and the exploitation of natural resources have transformed tropical mountain ecosystems across the world, and the consequences of these transformations for biodiversity and ecosystem functioning are largely unknown1-3. Conclusions that are derived from studies in non-mountainous areas are not suitable for predicting the effects of land-use changes on tropical mountains because the climatic environment rapidly changes with elevation, which may mitigate or amplify the effects of land use4,5. It is of key importance to understand how the interplay of climate and land use constrains biodiversity and ecosystem functions to determine the consequences of global change for mountain ecosystems. Here we show that the interacting effects of climate and land use reshape elevational trends in biodiversity and ecosystem functions on Africa's largest mountain, Mount Kilimanjaro (Tanzania). We find that increasing land-use intensity causes larger losses of plant and animal species richness in the arid lowlands than in humid submontane and montane zones. Increases in land-use intensity are associated with significant changes in the composition of plant, animal and microorganism communities; stronger modifications of plant and animal communities occur in arid and humid ecosystems, respectively. Temperature, precipitation and land use jointly modulate soil properties, nutrient turnover, greenhouse gas emissions, plant biomass and productivity, as well as animal interactions. Our data suggest that the response of ecosystem functions to land-use intensity depends strongly on climate; more-severe changes in ecosystem functioning occur in the arid lowlands and the cold montane zone. Interactions between climate and land use explained-on average-54% of the variation in species richness, species composition and ecosystem functions, whereas only 30% of variation was related to single drivers. Our study reveals that climate can modulate the effects of land use on biodiversity and ecosystem functioning, and points to a lowered resistance of ecosystems in climatically challenging environments to ongoing land-use changes in tropical mountainous regions.

Plant and animal functional diversity drive mutualistic network assembly across an elevational gradient.

Species' functional traits set the blueprint for pair-wise interactions in ecological networks. Yet, it is unknown to what extent the functional diversity of plant and animal communities controls network assembly along environmental gradients in real-world ecosystems. Here we address this question with a unique dataset of mutualistic bird-fruit, bird-flower and insect-flower interaction networks and associated functional traits of 200 plant and 282 animal species sampled along broad climate and land-use gradients on Mt. Kilimanjaro. We show that plant functional diversity is mainly limited by precipitation, while animal functional diversity is primarily limited by temperature. Furthermore, shifts in plant and animal functional diversity along the elevational gradient control the niche breadth and partitioning of the respective other trophic level. These findings reveal that climatic constraints on the functional diversity of either plants or animals determine the relative importance of bottom-up and top-down control in plant-animal interaction networks.

Qualitative and quantitative analysis of chemicals emitted from the pheromone gland of individual Heliothis subflexa females.

The chemicals emitted from the sex pheromone gland of individual Heliothis subflexa females were sampled using a short section of thick-film megabore fused silica capillary column, and the pheromone glands of the same females were extracted after the effluvia collection. Both samples were treated with a silylation reagent, and then subjected to gas chromatography-chemical ionization-mass spectrometry for quantitative and qualitative analysis of all components. The total amount of all 11 components emitted from the glands of calling females was 153 ng/female/hr, which was substantially higher than previously reported. The ratios of the pheromone components in the volatile emissions and pheromone gland extracts were generally similar to previous studies, but with notable differences. The collections of volatiles and gland extractions contained, respectively: Z9-14:Ald (1.57%, 1.35%), 14:Ald (3.78%, 1.51%), Z7 + Z9-16:Ald (9.60%, 3.59%), Z11-16:Ald (76.14%, 18.94%), 16:Ald (2.95%, 2.17%), Z9-16:OH (0.07%, 7.21%), Z11-16:OH (1.11%, 49.04%), Z7-16:OAc (0.48%, 1.73%), Z9-16:OAc (1.32%, 4.02%), and Z11-16:OAc (2.98%, 10.43%). The thick-film megabore column is an efficient approach for sampling the headspace for semiochemicals.

Alcohol Contributes to Attraction of Heliothis (= Chloridea) virescens Males to Females.

Female-emitted volatile sex pheromones in most moths are composed of biosynthetically related blends of fatty acid derivatives, such as aldehydes, acetate esters and alcohols. In many moths, as in the noctuid Heliothis (Chloridea) virescens, the pheromone gland contains alcohols (e.g., (Z)-11-hexadecen-1-ol, hereafter Z11-16:OH) that may serve dual functions as pheromone components as well as precursors of other pheromone components. The relative importance of Z11-16:OH to male attraction in H. virescens has been controversial. It occurs in the pheromone gland in relatively large amounts, but several studies could neither detect Z11-16:OH in gland emissions nor attribute any conspecific behavioral function to it in flight- tunnel assays. Trapping assays in the field, however, have more consistently documented that the addition of Z11-16:OH increased trap catch. Using a short section of thick film megabore column, in combination with derivatization and GC-CI-SIM-MS, we determined that Z11-16:OH is emitted from the sex pheromone gland during calling. Field trapping studies demonstrated that trap catch increased when Z11-16:OH was added to a 2-component minimal blend and to a 6-component blend. Behavioral observations in the field confirmed that more males responded to a pheromone blend that contained a low blend ratio of Z11-16:OH, but ≥5% Z11-16:OH depressed both male behavior and trap catch. We conclude that Z11-16:OH should be considered a component of the sex pheromone of H. virescens females.

Relationships between abiotic environment, plant functional traits, and animal body size at Mount Kilimanjaro, Tanzania.

The effect-response framework states that plant functional traits link the abiotic environment to ecosystem functioning. One ecosystem property is the body size of the animals living in the system, which is assumed to depend on temperature or resource availability, among others. For primary consumers, resource availability may directly be related to plant traits, while for secondary consumers the relationship is indirect. We used plant traits to describe resource availability along an elevational gradient on Mount Kilimanjaro, Tanzania. Using structural equation models, we determined the response of plant traits to changes in precipitation, temperature and disturbance with and assessed whether abiotic conditions or community-weighted means of plant traits are stronger predictors of the mean size of bees, moths, frugivorous birds, and insectivorous birds. Traits indicating tissue density and nutrient content strongly responded to variations in precipitation, temperature and disturbance. They had direct effects on pollination and fruit traits. However, the average body sizes of the animal groups considered could only be explained by temperature and habitat structure, not by plant traits. Our results demonstrate a strong link between traits and the abiotic environment, but suggest that temperature is the most relevant predictor of mean animal body size. Community-weighted means of plant traits and body sizes appear unsuitable to capture the complexity of plant-animal interactions.

Predictors of elevational biodiversity gradients change from single taxa to the multi-taxa community level.

The factors determining gradients of biodiversity are a fundamental yet unresolved topic in ecology. While diversity gradients have been analysed for numerous single taxa, progress towards general explanatory models has been hampered by limitations in the phylogenetic coverage of past studies. By parallel sampling of 25 major plant and animal taxa along a 3.7 km elevational gradient on Mt. Kilimanjaro, we quantify cross-taxon consensus in diversity gradients and evaluate predictors of diversity from single taxa to a multi-taxa community level. While single taxa show complex distribution patterns and respond to different environmental factors, scaling up diversity to the community level leads to an unambiguous support for temperature as the main predictor of species richness in both plants and animals. Our findings illuminate the influence of taxonomic coverage for models of diversity gradients and point to the importance of temperature for diversification and species coexistence in plant and animal communities.

Within-population variability in a moth sex pheromone blend: genetic basis and behavioural consequences.

Evolutionary diversification of sexual communication systems in moths is perplexing because signal and response are under stabilizing selection in many species, and this is expected to constrain evolutionary change. In the moth Heliothis virescens, we consistently found high phenotypic variability in the female sex pheromone blend within each of four geographically distant populations. Here, we assess the heritability, genetic basis and behavioural consequences of this variation. Artificial selection with field-collected moths dramatically increased the relative amount of the saturated compound 16:Ald and decreased its unsaturated counterpart Z11-16:Ald, the major sex pheromone component (high line). In a cross between the high- and low-selected lines, one quantitative trait locus (QTL) explained 11-21% of the phenotypic variance in the 16:Ald/Z11-16:Ald ratio. Because changes in activity of desaturase enzymes could affect this ratio, we measured their expression levels in pheromone glands and mapped desaturase genes onto our linkage map. A delta-11-desaturase had lower expression in females producing less Z11-16:Ald; however, this gene mapped to a different chromosome than the QTL. A model in which the QTL is a trans-acting repressor of delta-11 desaturase expression explains many features of the data. Selection favouring heterozygotes which produce more unsaturated components could maintain a polymorphism at this locus.

Complementary ecosystem services provided by pest predators and pollinators increase quantity and quality of coffee yields.

Wild animals substantially support crop production by providing ecosystem services, such as pollination and natural pest control. However, the strengths of synergies between ecosystem services and their dependencies on land-use management are largely unknown. Here, we took an experimental approach to test the impact of land-use intensification on both individual and combined pollination and pest control services in coffee production systems at Mount Kilimanjaro. We established a full-factorial pollinator and vertebrate exclosure experiment along a land-use gradient from traditional homegardens (agroforestry systems), shaded coffee plantations to sun coffee plantations (total sample size = 180 coffee bushes). The exclusion of vertebrates led to a reduction in fruit set of ca 9%. Pollinators did not affect fruit set, but significantly increased fruit weight of coffee by an average of 7.4%. We found no significant decline of these ecosystem services along the land-use gradient. Pest control and pollination service were thus complementary, contributing to coffee production by affecting the quantity and quality of a major tropical cash crop across different coffee production systems at Mount Kilimanjaro.