Bente J. Graae

Microclimate moderates plant responses to macroclimate warming

Significance Around the globe, climate warming is increasing the dominance of warm-adapted species—a process described as “thermophilization.” However, thermophilization often lags behind warming of the climate itself, with some recent studies showing no response at all. Using a unique database of more than 1,400 resurveyed vegetation plots in forests across Europe and North America, we document significant thermophilization of understory vegetation. However, the response to macroclimate warming was attenuated in forests whose canopies have become denser. This microclimatic effect likely reflects cooler forest-floor temperatures via increased shading during the growing season in denser forests. Because standing stocks of trees have increased in many temperate forests in recent decades, microclimate may commonly buffer understory plant responses to macroclimate warming. Recent global warming is acting across marine, freshwater, and terrestrial ecosystems to favor species adapted to warmer conditions and/or reduce the abundance of cold-adapted organisms (i.e., “thermophilization” of communities). Lack of community responses to increased temperature, however, has also been reported for several taxa and regions, suggesting that “climatic lags” may be frequent. Here we show that microclimatic effects brought about by forest canopy closure can buffer biotic responses to macroclimate warming, thus explaining an apparent climatic lag. Using data from 1,409 vegetation plots in European and North American temperate forests, each surveyed at least twice over an interval of 12–67 y, we document significant thermophilization of ground-layer plant communities. These changes reflect concurrent declines in species adapted to cooler conditions and increases in species adapted to warmer conditions. However, thermophilization, particularly the increase of warm-adapted species, is attenuated in forests whose canopies have become denser, probably reflecting cooler growing-season ground temperatures via increased shading. As standing stocks of trees have increased in many temperate forests in recent decades, local microclimatic effects may commonly be moderating the impacts of macroclimate warming on forest understories. Conversely, increases in harvesting woody biomass—e.g., for bioenergy—may open forest canopies and accelerate thermophilization of temperate forest biodiversity.

Latitudinal gradients as natural laboratories to infer species' responses to temperature

Macroclimatic variation along latitudinal gradients provides an excellent natural laboratory to investigate the role of temperature and the potential impacts of climate warming on terrestrial organisms. Here, we review the use of latitudinal gradients for ecological climate change research, in comparison with altitudinal gradients and experimental warming, and illustrate their use and caveats with a meta-analysis of latitudinal intraspecific variation in important life-history traits of vascular plants. We first provide an overview of latitudinal patterns in temperature and other abiotic and biotic environmental variables in terrestrial ecosystems. We then assess the latitudinal intraspecific variation present in five key life-history traits [plant height, specific leaf area (SLA), foliar nitrogen:phosphorus (N:P) stoichiometry, seed mass and root:shoot (R:S) ratio] in natural populations or common garden experiments across a total of 98 plant species. Intraspecific leaf N:P ratio and seed mass significantly decreased with latitude in natural populations. Conversely, the plant height decreased and SLA increased significantly with latitude of population origin in common garden experiments. However, less than a third of the investigated latitudinal transect studies also formally disentangled the effects of temperature from other environmental drivers which potentially hampers the translation from latitudinal effects into a temperature signal. Synthesis. Latitudinal gradients provide a methodological set-up to overcome the drawbacks of other observational and experimental warming methods. Our synthesis indicates that many life-history traits of plants vary with latitude but the translation of latitudinal clines into responses to temperature is a crucial step. Therefore, especially adaptive differentiation of populations and confounding environmental factors other than temperature need to be considered. More generally, integrated approaches of observational studies along temperature gradients, experimental methods and common garden experiments increasingly emerge as the way forward to further our understanding of species and community responses to climate warming.

Local temperatures inferred from plant communities suggest strong spatial buffering of climate warming across Northern Europe

Recent studies from mountainous areas of small spatial extent (<2500 km(2) ) suggest that fine-grained thermal variability over tens or hundreds of metres exceeds much of the climate warming expected for the coming decades. Such variability in temperature provides buffering to mitigate climate-change impacts. Is this local spatial buffering restricted to topographically complex terrains? To answer this, we here study fine-grained thermal variability across a 2500-km wide latitudinal gradient in Northern Europe encompassing a large array of topographic complexities. We first combined plant community data, Ellenberg temperature indicator values, locally measured temperatures (LmT) and globally interpolated temperatures (GiT) in a modelling framework to infer biologically relevant temperature conditions from plant assemblages within <1000-m(2) units (community-inferred temperatures: CiT). We then assessed: (1) CiT range (thermal variability) within 1-km(2) units; (2) the relationship between CiT range and topographically and geographically derived predictors at 1-km resolution; and (3) whether spatial turnover in CiT is greater than spatial turnover in GiT within 100-km(2) units. Ellenberg temperature indicator values in combination with plant assemblages explained 46-72% of variation in LmT and 92-96% of variation in GiT during the growing season (June, July, August). Growing-season CiT range within 1-km(2) units peaked at 60-65°N and increased with terrain roughness, averaging 1.97 °C (SD = 0.84 °C) and 2.68 °C (SD = 1.26 °C) within the flattest and roughest units respectively. Complex interactions between topography-related variables and latitude explained 35% of variation in growing-season CiT range when accounting for sampling effort and residual spatial autocorrelation. Spatial turnover in growing-season CiT within 100-km(2) units was, on average, 1.8 times greater (0.32 °C km(-1) ) than spatial turnover in growing-season GiT (0.18 °C km(-1) ). We conclude that thermal variability within 1-km(2) units strongly increases local spatial buffering of future climate warming across Northern Europe, even in the flattest terrains.

COMMUNITY ASSEMBLY IN EXPERIMENTAL GRASSLANDS: SUITABLE ENVIRONMENT OR TIMELY ARRIVAL?

It is hard to defend the view that biotic communities represent a simple and predictable response to the abiotic environment. Biota and the abiotic environment interact, and the environment of an individual certainly includes its neighbors and visitors in the community. The complexity of community assembly calls forth a quest for general principles, yet current results and theories on assembly rules differ widely. Using a grassland microcosm as a model system, we manipulated fertility, disturbance by defoliation, soil/microclimate, and arrival order of species belonging to two groups differing in functional attributes. We analyzed the outcome of community assembly dynamics in terms of species richness, invasibility, and species composition. The analyses revealed strong environmental control over species richness and invasibility. Species composition was mainly determined by the arrival order of species, indicating that historical contingency may change the outcome of community assembly. The probability for multiple equilibria appeared to increase with productivity and environmental stability. The importance of arrival order offers an explanation of the difficulties in predicting local occurrences of species in the field. In our experiment, variation in fertility and disturbance was controlling colonization with predictable effects on emergent community properties such as species richness. The key mechanism is suggested to be asymmetric competition, and our results show that this mechanism is relatively insensitive to the species through which it works. While our analyses indicate a positive and significant correlation between richness and invasibility, the significance disappears after accounting for the effect of the environment. The importance of arrival order (historical contingency) and environmental control supports the assumption of the unified neutral theory that different species within a trophic level can be considered functionally equivalent when it comes to community assembly. However, our results indicate that variation in asymmetric competition is the key factor determining the richness of the resulting communities, and this is far from neutral.

Putting plant resistance traits on the map: a test of the idea that plants are better defended at lower latitudes

• It has long been believed that plant species from the tropics have higher levels of traits associated with resistance to herbivores than do species from higher latitudes. A meta-analysis recently showed that the published literature does not support this theory. However, the idea has never been tested using data gathered with consistent methods from a wide range of latitudes. • We quantified the relationship between latitude and a broad range of chemical and physical traits across 301 species from 75 sites world-wide. • Six putative resistance traits, including tannins, the concentration of lipids (an indicator of oils, waxes and resins), and leaf toughness were greater in high-latitude species. Six traits, including cyanide production and the presence of spines, were unrelated to latitude. Only ash content (an indicator of inorganic substances such as calcium oxalates and phytoliths) and the properties of species with delayed greening were higher in the tropics. • Our results do not support the hypothesis that tropical plants have higher levels of resistance traits than do plants from higher latitudes. If anything, plants have higher resistance toward the poles. The greater resistance traits of high-latitude species might be explained by the greater cost of losing a given amount of leaf tissue in low-productivity environments.

Effects of a warmer climate on seed germination in the subarctic

BACKGROUND AND AIMS In a future warmer subarctic climate, the soil temperatures experienced by dispersed seeds are likely to increase during summer but may decrease during winter due to expected changes in snow depth, duration and quality. Because little is known about the dormancy-breaking and germination requirements of subarctic species, how warming may influence the timing and level of germination in these species was examined. METHODS Under controlled conditions, how colder winter and warmer summer soil temperatures influenced germination was tested in 23 subarctic species. The cold stratification and warm incubation temperatures were derived from real soil temperature measurements in subarctic tundra and the temperatures were gradually changed over time to simulate different months of the year. KEY RESULTS Moderate summer warming (+2.5 degrees C) substantially accelerated germination in all but four species but did not affect germination percentages. Optimum germination temperatures (20/10 degrees C) further decreased germination time and increased germination percentages in three species. Colder winter soil temperatures delayed the germination in ten species and decreased the germination percentage in four species, whereas the opposite was found in Silene acaulis. In most species, the combined effect of a reduced snow cover and summer warming resulted in earlier germination and thus a longer first growing season, which improves the chance of seedling survival. In particular the recruitment of (dwarf) shrubs (Vaccinium myrtillus, V. vitis-idaea, Betula nana), trees (Alnus incana, Betula pubescens) and grasses (Calamagrostis lapponica, C. purpurea) is likely to benefit from a warmer subarctic climate. CONCLUSIONS Seedling establishment is expected to improve in a future warmer subarctic climate, mainly by considerably earlier germination. The magnitudes of the responses are species-specific, which should be taken into account when modelling population growth and migration of subarctic species.

A hierarchical framework for integrating invasibility experiments incorporating different factors and spatial scales

Results from experiments studying different factors determining invasibility (e.g. land use, disturbance, biotic interactions) at different spatial scales are mainly used in isolation, probably because a methodology for integration is lacking. Recent studies show that factors affecting invasibility most likely do so in a hierarchical manner, with different factors acting more strongly at different spatial scales. Climate can be considered the dominant factor at the continental scale, while at regional and landscape scale topography, land cover and land use become increasingly important. At smaller spatial scales, soil type, disturbance, biotic interactions, resources, and microclimate may become significant. In the current paper, we propose a hierarchical framework for combining results from different types of studies. In this hierarchical system, factors operating at a smaller scale are subordinate to factors operating at a larger scale, but if conditions at higher levels are satisfied, the small-scale factors may become indispensable for making accurate predictions. Depending on the aim of the study, the accuracy of prediction can be selected by the researcher, which in its turn determines which data are required. We discuss several applications of the framework and indicate some options for future research. Although the complexity of natural systems presents fundamental limits to predictions, we think this framework can provide a useful tool for the identification of areas of risk for biological invasions, for improving our understanding of invasibility, and for identifying gaps in our current knowledge.

Strong microsite control of seedling recruitment in tundra.

The inclusion of environmental variation in studies of recruitment is a prerequisite for realistic predictions of the responses of vegetation to a changing environment. We investigated how seedling recruitment is affected by seed availability and microsite quality along a steep environmental gradient in dry tundra. A survey of natural seed rain and seedling density in vegetation was combined with observations of the establishment of 14 species after sowing into intact or disturbed vegetation. Although seed rain density was closely correlated with natural seedling establishment, the experimental seed addition showed that the microsite environment was even more important. For all species, seedling emergence peaked at the productive end of the gradient, irrespective of the adult niches realized. Disturbance promoted recruitment at all positions along the environmental gradient, not just at high productivity. Early seedling emergence constituted the main temporal bottleneck in recruitment for all species. Surprisingly, winter mortality was highest at what appeared to be the most benign end of the gradient. The results highlight that seedling recruitment patterns are largely determined by the earliest stages in seedling emergence, which again are closely linked to microsite quality. A fuller understanding of microsite effects on recruitment with implications for plant community assembly and vegetation change is provided.

Plant community type and small‐scale disturbances, but not altitude, influence the invasibility in subarctic ecosystems

Little of our knowledge about invasibility comes from arctic and alpine ecosystems, despite increasing plant migration and invasion in those regions. Here, we examine how community type, altitude, and small-scale disturbances affect invasibility in a subarctic ecosystem. Over a period of 4 yr, we studied seedling emergence and establishment in 17 species sown in gaps or undisturbed vegetation in four subarctic community types (Salix scrub, meadow, rich heath, poor heath) along an elevation gradient. Invasibility was lowest in rich heath and highest in Salix scrub. Small disturbances significantly increased the invasibility in most communities, thereby showing the importance of biotic resistance to invasion in subarctic regions. Unexpectedly, invasibility did not decrease with increasing elevation, and it was also not related to summer temperature. Our data suggest that biotic resistance might be more important than abiotic stress for invasibility in subarctic tundra and that low temperatures do not necessarily limit seedling establishment at high altitudes. High elevations are therefore potentially more vulnerable to invasion than was originally thought. Changes in community composition as a result of species migration or invasion are most likely to occur in Salix scrub and meadow, whereas Empetrum-dominated rich heath will largely remain unchanged.

The use of open-top chambers in forests for evaluating warming effects on herbaceous understorey plants

Open-top chambers (OTCs) are widely used experimental warming devices in open-field ecosystems such as tundra and alpine heath. However, knowledge of their performance in temperate deciduous forest ecosystems is largely lacking. The application of OTCs in forests might become important in the future since the effects of climate warming on growth, reproduction, and future distribution of understorey forest herbs have rarely been investigated. Therefore, polycarbonate OTCs covered with (OTCs+GF) and without permeable polypropylene GardenFleece (OTCs−GF) were installed in a temperate deciduous forest to create an experimental warming gradient. Short-term responses in phenology, growth, and reproduction of a model understorey forest herb (Anemone nemorosa L.) to OTC installation were determined. In a second growing season, an in-depth study of multiple abiotic conditions inside OTCs−GF was performed. Both OTCs+GF and OTCs−GF raised air and soil temperature in a realistic manner (ca. +0.4°C to +1.15°C), but OTCs−GF only in the leafless period (up to +1.5°C monthly average soil temperature). The early flowering forest herb A. nemorosa also showed a clear phenotypic response to OTC installation. Based on these facts and the large ecological drawbacks associated with OTCs+GF (mostly in connection with a higher relative air humidity and a lower light quantity) and very modest abiotic changes in OTCs−GF, we encourage the use of OTCs−GF in deciduous forest ecosystems for evaluating climate-warming effects on early flowering understorey forest herbs. There is also a potential to use this warming method on later flowering species, but this needs further research.