Plant phenology, the annually recurring sequence of plant developmental stages, is important for plant functioning and ecosystem services and their biophysical and biogeochemical feedbacks to the ...climate system. Plant phenology depends on temperature, and the current rapid climate change has revived interest in understanding and modeling the responses of plant phenology to the warming trend and the consequences thereof for ecosystems. Here, we review recent progresses in plant phenology and its interactions with climate change. Focusing on the start (leaf unfolding) and end (leaf coloring) of plant growing seasons, we show that the recent rapid expansion in ground‐ and remote sensing‐ based phenology data acquisition has been highly beneficial and has supported major advances in plant phenology research. Studies using multiple data sources and methods generally agree on the trends of advanced leaf unfolding and delayed leaf coloring due to climate change, yet these trends appear to have decelerated or even reversed in recent years. Our understanding of the mechanisms underlying the plant phenology responses to climate warming is still limited. The interactions between multiple drivers complicate the modeling and prediction of plant phenology changes. Furthermore, changes in plant phenology have important implications for ecosystem carbon cycles and ecosystem feedbacks to climate, yet the quantification of such impacts remains challenging. We suggest that future studies should primarily focus on using new observation tools to improve the understanding of tropical plant phenology, on improving process‐based phenology modeling, and on the scaling of phenology from species to landscape‐level.
This review examines the recent progresses in plant phenology and its interactions with climate change. Over its long history, phenology has grown from an empirical subject of observing and recording the timing of annual natural events for specific species to a comprehensive field that involves expanded observations, experiments, modeling, as well as the ecological consequences and climatic feedbacks of phenological changes. This review also emphasizes the need for future studies on the understanding of tropical plant phenology with new tools, on improving process‐based modeling, and on the scaling of phenology from species level to landscape level.
While climate warming reduces the occurrence of frost events, the warming-induced lengthening of the growing season of plants in the Northern Hemisphere may actually induce more frequent frost days ...during the growing season (GSFDs, days with minimum temperature < 0 °C). Direct evidence of this hypothesis, however, is limited. Here we investigate the change in the number of GSFDs at latitudes greater than 30° N using remotely-sensed and in situ phenological records and three minimum temperature (T
) data sets from 1982 to 2012. While decreased GSFDs are found in northern Siberia, the Tibetan Plateau, and northwestern North America (mainly in autumn), ~43% of the hemisphere, especially in Europe, experienced a significant increase in GSFDs between 1982 and 2012 (mainly during spring). Overall, regions with larger increases in growing season length exhibit larger increases in GSFDs. Climate warming thus reduces the total number of frost days per year, but GSFDs nonetheless increase in many areas.
Earlier spring leaf unfolding is a frequently observed response of plants to climate warming. Many deciduous tree species require chilling for dormancy release, and warming-related reductions in ...chilling may counteract the advance of leaf unfolding in response to warming. Empirical evidence for this, however, is limited to saplings or twigs in climate-controlled chambers. Using long-term in situ observations of leaf unfolding for seven dominant European tree species at 1,245 sites, here we show that the apparent response of leaf unfolding to climate warming (ST, expressed in days advance of leaf unfolding per °C warming) has significantly decreased from 1980 to 2013 in all monitored tree species. Averaged across all species and sites, ST decreased by 40% from 4.0 ± 1.8 days °C(-1) during 1980-1994 to 2.3 ± 1.6 days °C(-1) during 1999-2013. The declining ST was also simulated by chilling-based phenology models, albeit with a weaker decline (24-30%) than observed in situ. The reduction in ST is likely to be partly attributable to reduced chilling. Nonetheless, other mechanisms may also have a role, such as 'photoperiod limitation' mechanisms that may become ultimately limiting when leaf unfolding dates occur too early in the season. Our results provide empirical evidence for a declining ST, but also suggest that the predicted strong winter warming in the future may further reduce ST and therefore result in a slowdown in the advance of tree spring phenology.
The ongoing changes in vegetation spring phenology in temperate/cold regions are widely attributed to temperature. However, in arid/semiarid ecosystems, the correlation between spring temperature and ...phenology is much less clear. We test the hypothesis that precipitation plays an important role in the temperature dependency of phenology in arid/semiarid regions. We therefore investigated the influence of preseason precipitation on satellite‐derived estimates of starting date of vegetation growing season (SOS) across the Tibetan Plateau (TP). We observed two clear patterns linking precipitation to SOS. First, SOS is more sensitive to interannual variations in preseason precipitation in more arid than in wetter areas. Spatially, an increase in long‐term averaged preseason precipitation of 10 mm corresponds to a decrease in the precipitation sensitivity of SOS by about 0.01 day mm⁻¹. Second, SOS is more sensitive to variations in preseason temperature in wetter than in dryer areas of the plateau. A spatial increase in precipitation of 10 mm corresponds to an increase in temperature sensitivity of SOS of 0.25 day °C⁻¹ (0.25 day SOS advance per 1 °C temperature increase). Those two patterns indicate both direct and indirect impacts of precipitation on SOS on TP. This study suggests a balance between maximizing benefit from the limiting climatic resource and minimizing the risk imposed by other factors. In wetter areas, the lower risk of drought allows greater temperature sensitivity of SOS to maximize the thermal benefit, which is further supported by the weaker interannual partial correlation between growing degree days and preseason precipitation. In more arid areas, maximizing the benefit of water requires greater sensitivity of SOS to precipitation, with reduced sensitivity to temperature. This study highlights the impacts of precipitation on SOS in a large cold and arid/semiarid region and suggests that influences of water should be included in SOS module of terrestrial ecosystem models for drylands.
The reported progressive change of vegetation activity along elevational gradients has important aesthetic and conservation values. With climate change, cooler locations are suggested to warm faster ...than warmer ones, raising concerns of a more homogenized landscape along the elevation. Here, we use global satellite data to investigate the spatio-temporal dynamics of the elevational gradient (EG) in vegetation greenness (NDVI
), spring (SOS) and autumn phenology (EOS) during 1982-2015. Although we find clear geographical patterns of the EG in NDVI
and SOS, there are no prevalent trends of vegetation homogenization or phenology synchronization along elevational gradients. Possible mechanisms, including spatially heterogeneous temperature lapse rate changes, different vegetation sensitivities to climate change, and human disturbances, may play diverse roles across different regions. Our finding of mixed EG trends and no general rules controlling EG dynamics poses challenges for mitigating possible adverse impacts of climate change on mountainous biological diversity and ecosystem services.
Temperature data over the past five decades show faster warming of the global land surface during the night than during the day. This asymmetric warming is expected to affect carbon assimilation and ...consumption in plants, because photosynthesis in most plants occurs during daytime and is more sensitive to the maximum daily temperature, Tmax, whereas plant respiration occurs throughout the day and is therefore influenced by both Tmax and the minimum daily temperature, Tmin. Most studies of the response of terrestrial ecosystems to climate warming, however, ignore this asymmetric forcing effect on vegetation growth and carbon dioxide (CO2) fluxes. Here we analyse the interannual covariations of the satellite-derived normalized difference vegetation index (NDVI, an indicator of vegetation greenness) with Tmax and Tmin over the Northern Hemisphere. After removing the correlation between Tmax and Tmin, we find that the partial correlation between Tmax and NDVI is positive in most wet and cool ecosystems over boreal regions, but negative in dry temperate regions. In contrast, the partial correlation between Tmin and NDVI is negative in boreal regions, and exhibits a more complex behaviour in dry temperate regions. We detect similar patterns in terrestrial net CO2 exchange maps obtained from a global atmospheric inversion model. Additional analysis of the long-term atmospheric CO2 concentration record of the station Point Barrow in Alaska suggests that the peak-to-peak amplitude of CO2 increased by 23 ± 11% for a +1 °C anomaly in Tmax from May to September over lands north of 51° N, but decreased by 28 ± 14% for a +1 °C anomaly in Tmin. These lines of evidence suggest that asymmetric diurnal warming, a process that is currently not taken into account in many global carbon cycle models, leads to a divergent response of Northern Hemisphere vegetation growth and carbon sequestration to rising temperatures.
The availability of carbon (C) from high levels of atmospheric carbon dioxide (CO2) and anthropogenic release of nitrogen (N) is increasing, but these increases are not paralleled by increases in ...levels of phosphorus (P). The current unstoppable changes in the stoichiometries of C and N relative to P have no historical precedent. We describe changes in P and N fluxes over the last five decades that have led to asymmetrical increases in P and N inputs to the biosphere. We identified widespread and rapid changes in N:P ratios in air, soil, water, and organisms and important consequences to the structure, function, and biodiversity of ecosystems. A mass‐balance approach found that the combined limited availability of P and N was likely to reduce C storage by natural ecosystems during the remainder of the 21st Century, and projected crop yields of the Millennium Ecosystem Assessment indicated an increase in nutrient deficiency in developing regions if access to P fertilizer is limited. Imbalances of the N:P ratio would likely negatively affect human health, food security, and global economic and geopolitical stability, with feedbacks and synergistic effects on drivers of global environmental change, such as increasing levels of CO2, climatic warming, and increasing pollution. We summarize potential solutions for avoiding the negative impacts of global imbalances of N:P ratios on the environment, biodiversity, climate change, food security, and human health.
The anthropogenic release of nitrogen (N) is increasing, with no parallel increase in levels of phosphorus (P). We identify widespread and rapid changes in N:P ratios in air, soil, water, and organisms and important consequences to the structure, function, and biodiversity of ecosystems, food security, human health, and global economic and geopolitical stability. We finally summarize potential solutions for avoiding the negative impacts of global imbalances of N:P ratios for the environment and humans.
Recent warming significantly advanced leaf onset in the northern hemisphere. This signal cannot be accurately reproduced by current models parameterized by daily mean temperature (T(mean)). Here ...using in situ observations of leaf unfolding dates (LUDs) in Europe and the United States, we show that the interannual anomalies of LUD during 1982-2011 are triggered by daytime (Tmax) more than by nighttime temperature (T(min)). Furthermore, an increase of 1 °C in Tmax would advance LUD by 4.7 days in Europe and 4.3 days in the United States, more than the conventional temperature sensitivity estimated from T(mean). The triggering role of Tmax, rather than the T(min) or T(mean) variable, is also supported by analysis of the large-scale patterns of satellite-derived vegetation green-up in spring in the northern hemisphere (>30 °N). Our results suggest a new conceptual framework of leaf onset using daytime temperature to improve the performance of phenology modules in current Earth system models.
Significantly more carbon is stored in the world's soils-including peatlands, wetlands and permafrost-than is present in the atmosphere. Disagreement exists, however, regarding the effects of climate ...change on global soil carbon stocks. If carbon stored belowground is transferred to the atmosphere by a warming-induced acceleration of its decomposition, a positive feedback to climate change would occur. Conversely, if increases of plant-derived carbon inputs to soils exceed increases in decomposition, the feedback would be negative. Despite much research, a consensus has not yet emerged on the temperature sensitivity of soil carbon decomposition. Unravelling the feedback effect is particularly difficult, because the diverse soil organic compounds exhibit a wide range of kinetic properties, which determine the intrinsic temperature sensitivity of their decomposition. Moreover, several environmental constraints obscure the intrinsic temperature sensitivity of substrate decomposition, causing lower observed 'apparent' temperature sensitivity, and these constraints may, themselves, be sensitive to climate.
Despite decades of research, how climate warming alters the global flux of soil respiration is still poorly characterized. Here, we use meta‐analysis to synthesize 202 soil respiration datasets from ...50 ecosystem warming experiments across multiple terrestrial ecosystems. We found that, on average, warming by 2 °C increased soil respiration by 12% during the early warming years, but warming‐induced drought partially offset this effect. More significantly, the two components of soil respiration, heterotrophic respiration and autotrophic respiration showed distinct responses. The warming effect on autotrophic respiration was not statistically detectable during the early warming years, but nonetheless decreased with treatment duration. In contrast, warming by 2 °C increased heterotrophic respiration by an average of 21%, and this stimulation remained stable over the warming duration. This result challenged the assumption that microbial activity would acclimate to the rising temperature. Together, our findings demonstrate that distinguishing heterotrophic respiration and autotrophic respiration would allow us better understand and predict the long‐term response of soil respiration to warming. The dependence of soil respiration on soil moisture condition also underscores the importance of incorporating warming‐induced soil hydrological changes when modeling soil respiration under climate change.
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