Pieter De Frenne

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.

Global meta-analysis reveals no net change in local-scale plant biodiversity over time

Significance A major advance of the last 20 y at the interface of biological, environmental, and conservation sciences has been the demonstration that plant biodiversity positively influences ecosystem function. Linking these results to applied conservation efforts hinges on the assumption that biodiversity is actually declining at the local scale at which diversity–function relationships are strongest. Our compilation and analysis of a global database of >16,000 repeat survey vegetation plots from habitats across the globe directly contradict this assumption. We find no general tendency for local-scale plant species diversity to decline over the last century, calling into question the widespread use of ecosystem function experiments to argue for the importance of biodiversity conservation in nature. Global biodiversity is in decline. This is of concern for aesthetic and ethical reasons, but possibly also for practical reasons, as suggested by experimental studies, mostly with plants, showing that biodiversity reductions in small study plots can lead to compromised ecosystem function. However, inferring that ecosystem functions will decline due to biodiversity loss in the real world rests on the untested assumption that such loss is actually occurring at these small scales in nature. Using a global database of 168 published studies and >16,000 nonexperimental, local-scale vegetation plots, we show that mean temporal change in species diversity over periods of 5–261 y is not different from zero, with increases at least as likely as declines over time. Sites influenced primarily by plant species’ invasions showed a tendency for declines in species richness, whereas sites undergoing postdisturbance succession showed increases in richness over time. Other distinctions among studies had little influence on temporal richness trends. Although maximizing diversity is likely important for maintaining ecosystem function in intensely managed systems such as restored grasslands or tree plantations, the clear lack of any general tendency for plant biodiversity to decline at small scales in nature directly contradicts the key assumption linking experimental results to ecosystem function as a motivation for biodiversity conservation in nature. How often real world changes in the diversity and composition of plant communities at the local scale cause ecosystem function to deteriorate, or actually to improve, remains unknown and is in critical need of further study.

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.

Global environmental change effects on ecosystems: the importance of land-use legacies.

One of the major challenges in ecology is to predict how multiple global environmental changes will affect future ecosystem patterns (e.g. plant community composition) and processes (e.g. nutrient cycling). Here, we highlight arguments for the necessary inclusion of land-use legacies in this endeavour. Alterations in resources and conditions engendered by previous land use, together with influences on plant community processes such as dispersal, selection, drift and speciation, have steered communities and ecosystem functions onto trajectories of change. These trajectories may be modulated by contemporary environmental changes such as climate warming and nitrogen deposition. We performed a literature review which suggests that these potential interactions have rarely been investigated. This crucial oversight is potentially due to an assumption that knowledge of the contemporary state allows accurate projection into the future. Lessons from other complex dynamic systems, and the recent recognition of the importance of previous conditions in explaining contemporary and future ecosystem properties, demand the testing of this assumption. Vegetation resurvey databases across gradients of land use and environmental change, complemented by rigorous experiments, offer a means to test for interactions between land-use legacies and multiple environmental changes. Implementing these tests in the context of a trait-based framework will allow biologists to synthesize compositional and functional ecosystem responses. This will further our understanding of the importance of land-use legacies in determining future ecosystem properties, and soundly inform conservation and restoration management actions.

Plasticity in response to phosphorus and light availability in four forest herbs.

The differential ability of forest herbs to colonize secondary forests on former agricultural land is generally attributed to different rates of dispersal. After propagule arrival, however, establishing individuals still have to cope with abiotic soil legacies from former agricultural land use. We focused on the plastic responses of forest herbs to increased phosphorus availability, as phosphorus is commonly found to be persistently bioavailable in post-agricultural forest soils. In a pot experiment performed under field conditions, we applied three P levels to four forest herbs with contrasting colonization capacities: Anemone nemorosa, Primula elatior, Circaea lutetiana and Geum urbanum. To test interactions with light availability, half of the replicas were covered with shade cloths. After two growing seasons, we measured aboveground P uptake as well as vegetative and regenerative performance. We hypothesized that fast-colonizing species respond the most opportunistically to increased P availability, and that a low light availability can mask the effects of P on performance. All species showed a significant increase in P uptake in the aboveground biomass. The addition of P had a positive effect on the vegetative performances of two of the species, although this was unrelated to their colonization capacities. The regenerative performance was affected by light availability (not by P addition) and was related to the species’ phenology. Forest herbs can obviously benefit from the increased availability of P in post-agricultural forests, but not all species respond in the same way. Such differential patterns of plasticity may be important in community dynamics, as they affect the interactions among species.

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.

The effects of sampling method and vegetation type on the estimated abundance of Ixodes ricinus ticks in forests

Estimating the spatial and temporal variation in tick abundance is of great economical and ecological importance. Entire-blanket dragging is the most widely used method to sample free-living ixodid ticks. However, this technique is not equally efficient in different vegetation types. The height and structure of the vegetation under study will not only determine the likelihood of a tick-blanket contact, but will also determine the rate of dislodgement. The purpose of this study was therefore to determine whether the alternative strip-blanket is more effectively in picking up ticks than the standard entire-blanket. Sampling was carried out in four forest understory vegetation types that differed in height and structure on five collection dates between April and September 2008. A total of 8,068 Ixodes ricinus ticks was collected (778 adults, 1,920 nymphs, and 5,370 larvae). The highest numbers of ticks were collected along the forest trails, where the dominant vegetation consisted of short grasses. The lowest numbers of ticks were collected in bracken-fern-dominated sites, where the vegetation seriously hampered tick sampling. Surprisingly, in each vegetation type, significantly more nymphs and adults were collected using the entire-blanket. However, the strip-blanket was more effectively in collecting larvae, especially in dense and tall vegetation.

The response of forest plant regeneration to temperature variation along a latitudinal gradient

BACKGROUND AND AIMS The response of forest herb regeneration from seed to temperature variations across latitudes was experimentally assessed in order to forecast the likely response of understorey community dynamics to climate warming. METHODS Seeds of two characteristic forest plants (Anemone nemorosa and Milium effusum) were collected in natural populations along a latitudinal gradient from northern France to northern Sweden and exposed to three temperature regimes in growth chambers (first experiment). To test the importance of local adaptation, reciprocal transplants were also made of adult individuals that originated from the same populations in three common gardens located in southern, central and northern sites along the same gradient, and the resulting seeds were germinated (second experiment). Seedling establishment was quantified by measuring the timing and percentage of seedling emergence, and seedling biomass in both experiments. KEY RESULTS Spring warming increased emergence rates and seedling growth in the early-flowering forb A. nemorosa. Seedlings of the summer-flowering grass M. effusum originating from northern populations responded more strongly in terms of biomass growth to temperature than southern populations. The above-ground biomass of the seedlings of both species decreased with increasing latitude of origin, irrespective of whether seeds were collected from natural populations or from the common gardens. The emergence percentage decreased with increasing home-away distance in seeds from the transplant experiment, suggesting that the maternal plants were locally adapted. CONCLUSIONS Decreasing seedling emergence and growth were found from the centre to the northern edge of the distribution range for both species. Stronger responses to temperature variation in seedling growth of the grass M. effusum in the north may offer a way to cope with environmental change. The results further suggest that climate warming might differentially affect seedling establishment of understorey plants across their distribution range and thus alter future understorey plant dynamics.

Estimates of local biodiversity change over time stand up to scrutiny

We present new data and analyses revealing fundamental flaws in a critique of two recent meta-analyses of local-scale temporal biodiversity change. First, the conclusion that short-term time series lead to biased estimates of long-term change was based on two errors in the simulations used to support it. Second, the conclusion of negative relationships between temporal biodiversity change and study duration was entirely dependent on unrealistic model assumptions, the use of a subset of data, and inclusion of one outlier data point in one study. Third, the finding of a decline in local biodiversity, after eliminating post-disturbance studies, is not robust to alternative analyses on the original data set, and is absent in a larger, updated data set. Finally, the undebatable point, noted in both original papers, that studies in the ecological literature are geographically biased, was used to cast doubt on the conclusion that, outside of areas converted to croplands or asphalt, the distribution of biodiversity trends is centered approximately on zero. Future studies may modify conclusions, but at present, alternative conclusions based on the geographic-bias argument rely on speculation. In sum, the critique raises points of uncertainty typical of all ecological studies, but does not provide an evidence-based alternative interpretation.

Combining Biodiversity Resurveys across Regions to Advance Global Change Research

More and more ecologists have started to resurvey communities sampled in earlier decades to determine long-term shifts in community composition and infer the likely drivers of the ecological changes observed. However, to assess the relative importance of and interactions among multiple drivers, joint analyses of resurvey data from many regions spanning large environmental gradients are needed. In this article, we illustrate how combining resurvey data from multiple regions can increase the likelihood of driver orthogonality within the design and show that repeatedly surveying across multiple regions provides higher representativeness and comprehensiveness, allowing us to answer more completely a broader range of questions. We provide general guidelines to aid the implementation of multiregion resurvey databases. In so doing, we aim to encourage resurvey database development across other community types and biomes to advance global environmental change research.