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.

Recent evolution of flowering time across multiple European plant species correlates with changes in aridity.

Ongoing global warming and increasing drought frequencies impact plant populations and potentially drive rapid evolutionary adaptations. Historical comparisons, where plants grown from seeds collected in the past are compared to plants grown from freshly collected seeds from populations of the same sites, are a powerful method to investigate recent evolutionary changes across many taxa. We used 21-38 years old seeds of 13 European plant species, stored in seed banks and originating from Mediterranean and temperate regions, together with recently collected seeds from the same sites for a greenhouse experiment to investigate shifts in flowering phenology as a potential result of adaptive evolution to changes in drought intensities over the last decades. We further used single nucleotide polymorphism (SNP) markers to quantify relatedness and levels of genetic variation. We found that, across species, current populations grew faster and advanced their flowering. These shifts were correlated with changes in aridity at the population origins, suggesting that increased drought induced evolution of earlier flowering, whereas decreased drought lead to weak or inverse shifts in flowering phenology. In five out of the 13 species, however, the SNP markers detected strong differences in genetic variation and relatedness between the past and current populations collected, indicating that other evolutionary processes may have contributed to changes in phenotypes. Our results suggest that changes in aridity may have influenced the evolutionary trajectories of many plant species in different regions of Europe, and that flowering phenology may be one of the key traits that is rapidly evolving.

Evolution of plant drought strategies and herbivore tolerance after two decades of climate change.

Ongoing global warming, coupled with increased drought frequencies, together with other biotic drivers may have resulted in complex evolutionary adaptation. The resurrection approach, comparing ancestors raised from stored seeds with their contemporary descendants under common conditions, is a powerful method to test for recent evolution in plant populations. We used 21-26-yr-old seeds of four European plant species - Matthiola tricuspidata, Plantago crassifolia, Clinopodium vulgare and Leontodon hispidus - stored in seed banks together with re-collected seeds from their wild populations. To test for evolutionary changes, we conducted a glasshouse experiment that quantified heritable changes in plant responses to drought and simulated insect herbivory. In three out of the four studied species, we found evidence that descendants had evolved shorter life cycles through faster growth and flowering. Shifts in the osmotic potential and leaf dry matter content indicated that descendants also evolved increased drought tolerance. A comparison of quantitative genetic differentiation (QST ) vs neutral molecular differentiation (FST ) values, using double digest restriction-site associated DNA (ddRAD) genotyping data, suggested that directional selection, and therefore adaptive evolution, was underlying some of the observed phenotypic changes. In summary, our study revealed evolutionary changes in plant populations over the last decades that are consistent with adaptation of drought escape and tolerance as well as herbivory avoidance.

Continuous inbreeding affects genetic variation, phenology, and reproductive strategy in ex situ cultivated Digitalis lutea.

PREMISE: Ex situ cultivation is important for plant conservation, but cultivation in small populations may result in genetic changes by drift, inbreeding, or unconscious selection. Repeated inbreeding potentially influences not only plant fitness, but also floral traits and interactions with pollinators, which has not yet been studied in an ex situ context. METHODS: We studied the molecular genetic variation of Digitalis lutea from a botanic garden population cultivated for 30 years, a frozen seed bank conserving the original genetic structure, and two current wild populations including the source population. In a common garden, we studied the effects of experimental inbreeding and between-population crosses on performance, reproductive traits, and flower visitation of plants from the garden and a wild population. RESULTS: Significant genetic differentiation was found between the garden population and the wild population from which the seeds had originally been gathered. After experimental selfing, inbreeding depression was only found for germination and leaf size of plants from the wild population, indicating a history of inbreeding in the smaller garden population. Moreover, garden plants flowered earlier and had floral traits related to selfing, whereas wild plants had traits related to attracting pollinators. Bumblebees visited more flowers of outbred than inbred plants and of wild than garden plants. CONCLUSIONS: Our case study suggests that high levels of inbreeding during ex situ cultivation can influence reproductive traits and thus interactions with pollinators. Together with the effects of genetic erosion and unconscious selection, these changes may affect the success of reintroductions into natural habitats.

Phylogenetic classification of the world's tropical forests.

Knowledge about the biogeographic affinities of the world's tropical forests helps to better understand regional differences in forest structure, diversity, composition, and dynamics. Such understanding will enable anticipation of region-specific responses to global environmental change. Modern phylogenies, in combination with broad coverage of species inventory data, now allow for global biogeographic analyses that take species evolutionary distance into account. Here we present a classification of the world's tropical forests based on their phylogenetic similarity. We identify five principal floristic regions and their floristic relationships: (i) Indo-Pacific, (ii) Subtropical, (iii) African, (iv) American, and (v) Dry forests. Our results do not support the traditional neo- versus paleotropical forest division but instead separate the combined American and African forests from their Indo-Pacific counterparts. We also find indications for the existence of a global dry forest region, with representatives in America, Africa, Madagascar, and India. Additionally, a northern-hemisphere Subtropical forest region was identified with representatives in Asia and America, providing support for a link between Asian and American northern-hemisphere forests.

Variation in life-history traits and their plasticities to elevational transplantation among seed families suggests potential for adaptative evolution of 15 tropical plant species to climate change.

UNLABELLED: • PREMISE OF THE STUDY: Because not all plant species will be able to move in response to global warming, adaptive evolution matters largely for plant persistence. As prerequisites for adaptive evolution, genetic variation in and selection on phenotypic traits are needed, but these aspects have not been studied in tropical species. We studied how plants respond to transplantation to different elevations on Mt. Kilimanjaro, Tanzania, and whether there is quantitative genetic (among-seed family) variation in and selection on life-history traits and their phenotypic plasticity to the different environments.• METHODS: We reciprocally transplanted seed families of 15 common tropical, herbaceous species of the montane and savanna vegetation zone at Mt. Kilimanjaro to a watered experimental garden in the montane (1450 m) and in the savanna (880 m) zone at the mountain's slope and measured performance, reproductive, and phenological traits.• RESULTS: Plants generally performed worse in the savanna garden, indicating that the savanna climate was more stressful and thus that plants may suffer from future climate warming. We found significant quantitative genetic variation in all measured performance and reproductive traits in both gardens and for several measures of phenotypic plasticity in response to elevational transplantation. Moreover, we found positive selection on traits at low and intermediate trait values levelling to neutral or negative selection at high values.• CONCLUSIONS: We conclude that common plants at Mt. Kilimanjaro express quantitative genetic variation in fitness-relevant traits and in their plasticities, suggesting potential to adapt evolutionarily to future climate warming and increased temperature variability.

Are rare plant species less resistant than common ones to herbivores? A multi-plant species study using above- and below-ground generalist herbivores.

Rare plant species are suggested to be less resistant to herbivores than common species. Their lower apparency and the fact that they often live in isolated populations, resulting in fewer herbivore encounters, might have led to the evolution of reduced defences. Moreover, their frequent lower levels of genetic diversity compared with common species could negatively affect their resistance against enemies. However, the hypothesis that plant resistance depends on plant regional and local rarity, independently of habitat and competitive and growth strategy, lacks evidence. To test this hypothesis, we assessed the performance and preference of one belowground and three aboveground generalist invertebrate herbivores from different taxonomic groups as indicators of plant resistance. Herbivores were fed a total of 62 regionally and locally rare and common plant species from Switzerland. We accounted for differences in a plant's growth and competitive strategy and habitat resource availability. We found that regionally and locally rare and common plant species did not generally differ in their resistance to most generalist herbivores. However, one herbivore species even performed better and preferred locally and regionally common plant species over rarer ones, indicating that common species are not more resistant, but tend to be less resistant. We also found that all herbivore species consistently performed better on competitive and large plant species, although different herbivore species generally preferred and performed better on different plant species. The latter indicates that the use of generalist herbivores as indicators of plant-resistance levels can be misleading. Synthesis: Our results show that rare plant species are not inherently less resistant than common ones to herbivores. Instead, our results suggest that the ability of plants to allocate resources away from defence towards enhancing their competitive ability might have allowed plants to tolerate herbivory, and to become locally and regionally common.

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.

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.

Vertical and Horizontal Vegetation Structure across Natural and Modified Habitat Types at Mount Kilimanjaro.

In most habitats, vegetation provides the main structure of the environment. This complexity can facilitate biodiversity and ecosystem services. Therefore, measures of vegetation structure can serve as indicators in ecosystem management. However, many structural measures are laborious and require expert knowledge. Here, we used consistent and convenient measures to assess vegetation structure over an exceptionally broad elevation gradient of 866-4550 m above sea level at Mount Kilimanjaro, Tanzania. Additionally, we compared (human)-modified habitats, including maize fields, traditionally managed home gardens, grasslands, commercial coffee farms and logged and burned forests with natural habitats along this elevation gradient. We distinguished vertical and horizontal vegetation structure to account for habitat complexity and heterogeneity. Vertical vegetation structure (assessed as number, width and density of vegetation layers, maximum canopy height, leaf area index and vegetation cover) displayed a unimodal elevation pattern, peaking at intermediate elevations in montane forests, whereas horizontal structure (assessed as coefficient of variation of number, width and density of vegetation layers, maximum canopy height, leaf area index and vegetation cover) was lowest at intermediate altitudes. Overall, vertical structure was consistently lower in modified than in natural habitat types, whereas horizontal structure was inconsistently different in modified than in natural habitat types, depending on the specific structural measure and habitat type. Our study shows how vertical and horizontal vegetation structure can be assessed efficiently in various habitat types in tropical mountain regions, and we suggest to apply this as a tool for informing future biodiversity and ecosystem service studies.

Simulating carbon stocks and fluxes of an African tropical montane forest with an individual-based forest model.

Tropical forests are carbon-dense and highly productive ecosystems. Consequently, they play an important role in the global carbon cycle. In the present study we used an individual-based forest model (FORMIND) to analyze the carbon balances of a tropical forest. The main processes of this model are tree growth, mortality, regeneration, and competition. Model parameters were calibrated using forest inventory data from a tropical forest at Mt. Kilimanjaro. The simulation results showed that the model successfully reproduces important characteristics of tropical forests (aboveground biomass, stem size distribution and leaf area index). The estimated aboveground biomass (385 t/ha) is comparable to biomass values in the Amazon and other tropical forests in Africa. The simulated forest reveals a gross primary production of 24 tcha(-1) yr(-1). Modeling above- and belowground carbon stocks, we analyzed the carbon balance of the investigated tropical forest. The simulated carbon balance of this old-growth forest is zero on average. This study provides an example of how forest models can be used in combination with forest inventory data to investigate forest structure and local carbon balances.