Abstract
Memory effects refer to the impacts of antecedent climate conditions on current vegetation productivity. This temporal linkage has been found to be strong in arid and semi-arid regions. However, the dominant climatic factors that determine such patterns are still unclear. Here, we defined’water-memory effects’ as the persistent effects of antecedent precipitation on the vegetation productivity for a given memory length (from 1 to up to 12 months). Based on satellite observations and climate data, we quantified the length of water-memory effects and evaluated the contributions of antecedent precipitation on current vegetation. Our results showed that vegetation productivity was highly dependent on antecedent precipitation in arid and semi-arid regions. The average length of water memory was approximately 5.6 months. Globally, water-memory effects could explain the geographical pattern and strength of memory effects, indicating that precipitation might be the dominant climatic factor determining memory effects because of its impact on water availability. Moreover, our results showed vegetation in regions with low mean annual precipitation or a longer water memory has lower engineering resilience (i.e. slower recovery rate) to disturbances. These findings will enable better assessment of memory effects and improve our understanding of the vulnerability of vegetation to climate change.
Introduction
Memory effects can be defined as the dependence of vegetation productivity on both contemporary disturbances and the residual effects of past climate conditions1–4. The occurrence of such effects highlights the importance of considering time in ecological studies and provides an explanation for the observed relationship between antecedent climate conditions and current vegetation growth2. Indeed, there is clear evidence that past climate conditions, including precipitation, temperature, and other abiotic factors can significantly influence phenology5,6, vegetation productivity7–11 and terrestrial ecosystem carbon cycles12,13. However, the relationship between past climate conditions and current vegetation productivity is still poorly understood2. Hence, a better understanding of vegetation memory effects is a critical requirement for projecting future vegetation dynamics.
Recent studies have indicated that memory effects play a more significant role in influencing the vegetation productivity of arid and semi-arid regions at a global scale1,4. However, the first-order autoregressive [AR (1)] model adopted in previous studies1,4 have not identified the relative contributions of each climatic factor to the observed effects. Thus, the underlying dominant climatic driver that explains this pattern remains unknown, despite the knowledge that vegetation in arid and semi-arid regions is predominantly limited by water availability14. Additionally, although the effects of antecedent precipitation on vegetation growth in dry regions have been established in previous studies7,9,11,15–18, there has been a lack of analysis of the contributions of antecedent water availability to memory effects globally. The elucidation of such contributions should provide valuable insight into the mechanism of global vegetation memory effects and contribute to a more comprehensive understanding of water-related vegetation responses. Here, we defined vegetation ‘water-memory effects’ as the persistent effects of antecedent precipitation on the vegetation productivity for a given memory length (from 1 to up to 12 months). Since the time lag of the responses of vegetation to antecedent precipitation differ significantly19,20, an important approach for evaluating water memory effects is to determine the period during which past precipitation significantly influenced the current state of vegetation productivity, which as can be referred to as ‘water-memory length’2.
In addition, memory effects are considered to be a useful indicator for quantifying the recovery rates of natural ecosystems to their equilibrium state after perturbations from fluctuations in climatic or other factors, which is an important component of ecosystem engineering resilience4,21. Specifically, engineering resilience estimates the recovery rates of a system to equilibrium state after the disturbance22, whereas ecological resilience quantifies the magnitude of disturbances that could be absorbed by a system changes to another state23. Studies indicate that systems with lower ecological resilience may also have longer ecological memory and therefore may also indicate slower recovery rates (i.e. lower engineering resilience)24. This slowing of ecosystem recovery can be detected through an increase in temporal autocorrelation4,24,25. For instance, Verbesselt et al.25, adopted this method using satellite observations and found that tropical forests in drier regions exhibit slower recovery rates and therefore inferred that these areas had lower ecological resilience. This finding suggested that precipitation could be an important mechanism underlying tropical forest resilience. Therefore, precipitation and the memory length may be critical for understanding vegetation engineering resilience and could be used to help recognize ecosystems that are vulnerable to collapse.
In this study, climate-vegetation relationships were determined using multiple linear regression (MLR) models and one AR (1) model, employing use of 31 years of satellite-derived Normalized Difference Vegetation Index (NDVI) data26 (a proxy of vegetation productivity) and the Standardized Precipitation Index (SPI) together with global precipitation, temperature and solar radiation data (See Methods). Here, we aim to (1) determine the period during which past precipitation significantly influenced the current state of vegetation productivity, i.e., water memory length; (2) evaluate the contributions of within-memory precipitation (i.e., accumulated precipitation within the water memory length) to memory effects and investigate the reason why stronger memory effects are observed in global arid and semi-arid regions; and (3) investigate the relationship between precipitation/water memory length and ecosystem engineering resilience at the global scale to improve our understanding of vegetation resilience.
Results
Length of water memory effects
On a global scale, we first determined the water memory length as the period for which the correlation coefficient between NDVI and within-memory precipitation (SPI) was highest (See Methods). Note that we removed all areas where the percentage of missing values in the Climate Research Unit (CRU) climate datasets was greater than 5% based on the station files (Fig. S1). We found that NDVI in 72.8% of the vegetated land areas was significantly correlated with SPI (P < 0.05) (Fig. S2), especially in arid and semi-arid regions of vegetated areas, as identified by the aridity index (Fig. S3a). Water memory length during the growing season exhibited high spatial heterogeneity but mainly ranged from 1 to 3 months (Fig. 1). We also found that longer memory was prominent in several arid and semi-arid regions, including central-western America, southern Argentina, western Australia, and central Asia.
In addition, based on a global unchanged land cover map that was derived from moderate-resolution imaging spectroradiometer (MODIS) data (Fig. S4), we found that southern open shrubland and grassland exhibited the greatest water memory length (6.9 and 6.5 months, respectively). Additionally, forest and savanna ecosystems presented shorter water memory lengths than other vegetation types. The mean lengths of the water memory effects for deciduous broadleaf, evergreen broadleaf, deciduous needleleaf, and evergreen needleleaf forests were 5.2, 5.0, 5.2, and 4.5 months, respectively (Table S1). Furthermore, we analyzed the time scales at which the correlation coefficients between vegetation productivity and within-memory precipitation were highest at a monthly resolution and found that only a few areas exhibited significant relationships during each month of the main growing season, such as Australia (Fig. S5).
Contribution of precipitation to memory effects
The water memory length is the length of time over which past precipitation significantly impacts the current vegetation productivity. Therefore, to quantify the effects of variation in within-memory precipitation on NDVI during the growing season from 1982 to 2012, we used a MLR model in which NDVI was the dependent variable and the independent variables were as follows: SPI at the timescale of water memory length, temperature, and solar radiation (cloud cover as the proxy). Accordingly, the linear regression slope of SPI to NDVI (i.e., the SPI coefficient) was defined as the effects of within-memory precipitation on NDVI, and the influence of contemporary temperature and solar radiation were quantified in the same manner. For a comparison, we also constructed a MLR model without considering antecedent precipitation, in which SPI was replaced by the contemporary precipitation. The variables were all detrended and standardized. In addition, we constructed an AR (1) model to characterize the strength of the general vegetation memory effects (i.e., the coefficient of NDVIt−1) when antecedent water availability is not considered1,4(Equation 3, see Methods).
First, we compared the average explanatory power of the three climatic factors for vegetation growth with or without considering water memory effects. We found that the MLR model with water memory effects provided a better explanation for the variation in vegetation productivity globally (Fig. S6). Furthermore, vegetation in arid and semi-arid regions showed much higher sensitivity (higher SPI coefficient values) to water availability when antecedent precipitation was considered than when it was not (Fig. 2a and b). More importantly, this result is consistent with areas of strong memory effects (high NDVIt−1 coefficient values) (Fig. 2a and c). To determine the strength of the linkage between water-memory effects and the general memory effects from the AR (1) model, we analyzed the correlation between the SPI and NDVIt−1 coefficients and found a particularly strong correlation (R2 = 0.99, p < 0.001) (Fig. 3), which indicated that water memory effects could dominate the strength of memory effects, especially in arid and semi-arid regions. Additionally, weak water memory effects were also observed at middle-to-high latitudes in the Northern Hemisphere and tropical forests, where the climate is more humid (Fig. 2a). To test the dependency of the strength of water memory effects on the gradient of precipitation, the pixel values of SPI coefficient were averaged by MAP bin (each interval size of 50 mm yr−1). As illustrated in Fig. S7, the coefficients of SPI decreased with increasing MAP (R2 = 0.89, P < 0.001). Furthermore, similar results were also observed when we used other precipitation datasets from Global Precipitation Climatology Centre27 and University of Delaware28, a temperature dataset from University of Delaware and a CRU-NCEP shortwave radiation dataset (Figs S8–12).
In addition, weak memory effects (low NDVIt−1 coefficient values) were mainly observed at middle-to-high latitudes in the Northern Hemisphere and tropical forests (Fig. 2c), where temperature and shortwave radiation are the predominant limiting climatic factors1,14. Positive coefficients of temperature were also observed in these regions (Figs S13a–15a). Furthermore, we also observed negative coefficients of temperature in Australia and Africa, which indicated that the NDVI anomalies in these regions respond in an opposite manner, which may might suggest a co-effect of water limitation29,30. Additionally, the coefficient of solar radiation was smaller than those of the other two climatic factors, which implied that NDVI was less sensitive to variation in solar radiation than to either precipitation or temperature. However, the sensitivity of vegetation productivity to variation in solar radiation was higher at high latitudes in the Northern Hemisphere, as well as in central Europe, southern China, and northwest Australia (Figs S13b–15b). Nevertheless, no general pattern was found in the responses of vegetation to the effects of radiation variability.
Relationship between precipitation/water memory length and vegetation engineering resilience
According to a previous study4, the AR(1) model (equation 3) used to denote general memory effects globally may be used as a proxy for vegetation engineering resilience. Specifically, high absolute values of the coefficient of NDVIt−1 (γ) may indicate a slow recovery rate to equilibrium, i.e., low engineering resilience4. Therefore, it may be interesting to assess the relationship between precipitation/water memory length and vegetation engineering resilience here.
Based on the analysis of the AR (1) models (Fig. 2c), we found that the coefficients of NDVIt−1 increased markedly when the MAP fell globally (Fig. 4a). Among different vegetation types, the highest coefficient of NDVIt−1 was observed in southern open shrubland (0.59) where the lowest MAP was observed (318 mm). In contrast, forests appeared to exhibit low coefficients of NDVIt−1. For example, evergreen broadleaf forest presented the lowest coefficient of NDVIt−1 (0.25), with the highest MAP (2352 mm) (Table S2). However, this relation is not strictly true among all vegetation types, such as savanna. In addition, as within-memory precipitation has been suggested to play a dominant role in determining memory effects (Figs 2a,c and 3), vegetation with a long water memory would likely to be out of equilibrium with contemporary climate perturbations. It might also be expected to exhibit slower recovery rates and lower ecological resilience. Indeed, on a global scale, we found a significant positive correlation between the coefficients of NDVIt−1 and the length of water memory (R2 = 0.94, p < 0.001) (Fig. 4b). For example, southern open shrubland displayed a long water memory length (6.9 months) and high coefficient of NDVIt−1 (low engineering resilience). Evergreen broadleaf forest have short water memory length (5.0 months) and low coefficient of NDVIt−1 (high engineering resilience). Spatially, several patterns were evident. For example, lower and higher engineering resilience levels were observed in southern and northern Argentina, respectively. A similar pattern was also observed for the MAP and the length of water memory; i.e., lower MAP and longer water memory were observed in southern Argentina, and higher MAP and shorter water memory were observed in northern Argentina (Fig. 1, Fig. 2c and Fig. S3b). Similar patterns were also apparent in eastern and western America. However, the patterns in several regions were less evident, such as South Africa.
Discussion
In this study, we quantified the length of water memory effects and the contributions of within-memory precipitation to current vegetation productivity globally and implications of MAP and water memory length for vegetation engineering resilience.
Importance of water memory effects
Our results concerning the vegetation water memory length suggested that arid and semi-arid regions showed the longest time scales, of approximately 5–7 months. The obtained time scales were comparable to a previous study that reported vegetation in arid and semi-arid regions were most sensitive to water anomalies for about 4–6 months16. Twelve-month-persistent responses of vegetation’s to antecedent precipitation were also identified in arid regions, such as central-western America and central Asia. This is supported by recent studies indicating that above-ground net primary production in arid ecosystems is highly dependent on previous-year precipitation9,11. This finding can be explained by (1) the adaptations of vegetation to frequent water shortages due to relevant physiological mechanisms;20,31 (2) the lagged vegetation response to soil moisture anomalies in arid or semi-arid regions;3,32,33 and (3) the hierarchical of responses of vegetation’s responses to resource availability34. Hence, it has been suggested that a hierarchical response framework should be be involved in future research to understand the complex mechanisms11,35.
Furthermore, we found that the strength of vegetation water memory effects was greatest in arid and semi-arid regions at the global scale and decreased with increasing MAP. This observation is consistent with previous studies, which have reported arid or semi-arid ecosystems showed largest legacy or time-lag effects of precipitation15–17,19. For instance, a recent investigation of the responses of forests to pervasive water deficits indicated that the legacy effects of water deficits on forest trees are highly dependent on MAP, with this effect being most pronounced in dry ecosystems36. Moreover, recent studies1,4 have shown that strong memory effects are found in arid and semi-arid regions globally. However, the AR (1) model adopted in previous studies1,4 cannot differentiate the dominant climatic factors determining memory effects globally. Our results showed that within-memory water availability can explain the geographical pattern and strength of memory effects globally. This suggests that antecedent precipitation may be the dominant climate factor that determine the memory effects, especially in arid and semi-arid regions.
In addition, many studies may underestimate the real sensitivity of vegetation to precipitation variability due to considering only the effects of short-term concurrent precipitation perturbations on vegetation growth19,37. This potential issue is supported by our finding that current vegetation productivity is more strongly affected by antecedent precipitation than contemporary precipitation in arid and semi-arid regions; i.e., vegetation shows the higher sensitivity of vegetation to within-memory precipitation than to contemporary precipitation. For example, Sala et al.11, found antecedent precipitation largely controlled current-year Aboveground Net Primary Production (ANPP) mainly in North America and central Asia based on 16 long-term in situ series of ANPP. This observation is consistent with our finding that vegetation in North America and central Asia shows higher sensitivity to within-memory precipitation than to contemporary precipitation. Hence, it is important to recognize that water-limited regions might also exhibit high sensitivity to climate variability and may therefore also be vulnerable to climate change38. In addition to the important role of antecedent precipitation in determining current vegetation dynamics, other factors, such as changes in antecedent temperature and solar radiation, could modify vegetation responses, as well6,8. Thus, there is also a compelling need to understand the temporal linkages between other abiotic factors, including temperature and shortwave radiation, and the ecological dynamics of current vegetation2.
Implications for vegetation resilience
Another finding of this study was a linear relationship between the MAP and recovery rates, as may be inferred by the general AR (1) coefficient in equation 3. Due to the lack of very long time series of data that can describe a period of gradual change in the vegetation state39, we didn’t detect the changes in recovery rates across time nor assess the spatial patterns of it. This result of the declining recovery rates across the decreasing gradient of MAP is consistent with a previous study4 showing that vegetation in dry regions exhibits low engineering resilience at the global scale. A recent study also indicated that tropical forests in drier regions present slower recovery rates and therefore might be less resilient25. The declining recovery rates observed across the decreasing MAP gradient could be caused by the intrinsic differences in vegetation structures, such as tree cover and canopy height, or other mechanisms influenced by the variations in MAP25. For instance, Hirota et al.40, also found tropical forest show low resilience where there is low tree cover (low MAP)40, which may partly explained our estimates of low engineering resilience for savanna and higher engineering resilience for evergreen broadleaf forest. Moreover, as within-memory precipitation was suggested to play a dominant role in memory effects, vegetation with a greater water memory length is likely to recover to an equilibrium state more slowly, which is consistent with current theory24. However, vegetation resilience is complex and challenging to assess because it can be regulated by a number of mechanisms, including ecosystem biodiversity41,42, ecosystem structure4,40, and plant trait diversity43. It should be also noted that a high t−1 coefficient in the AR (1) model might be caused by some mechanisms other than low engineering resilience. For example, we identified that some regions with low engineering resilience actually responded to a lagged extrinsic water variable, which might be related to “extrinsic ecological memory”2. The next challenge is to understand the complex biological and hydrological processes underlying these patterns and relationships. Hence, in the future, long-term field experiments along the gradient of precipitation may help validate and clarify the mechanisms of vegetation engineering resilience based on remotely observations.
Conclusions
In summary, based on the simultaneous analysis of satellite observations and climatic data, we found that the vegetation water memory length was prominent in arid and semi-arid regions, with a globally averaged water memory length of 5.6 months. Our results also concluded that water memory effects could explain the geographical pattern and strength of memory effects, suggesting that precipitation might be the dominant climatic factors determining memory effects because of its impact on water availability. This finding contributes to a more comprehensive understanding of water-related vegetation responses. In terms of the relationship between MAP/water memory length and vegetation engineering resilience, strong linear correlations were observed at a global scale. This finding may imply that vegetation in regions with low MAP or a longer water memory is likely to have low engineering resilience (i.e. slower recovery rate) to disturbances. Future field experiments are needed to confirm and interpret the satellite-derived vegetation engineering resilience results. Since future increases in the occurrences or intensity of extreme events are likely to generate unknown effects on terrestrial ecosystems and ecosystem services44, the assessment of vegetation water memory effects and engineering resilience can improve our understanding of the vulnerability of vegetation to climate change.
Methods
Climate data
We first used monthly precipitation, temperature and cloud cover datasets from the Climate Research Unit, version TS 4.01. These datasets had been interpolated from meteorological stations, based on spatial autocorrelation functions, and included data from 1901 to 201645,46. The cloud cover has been widely used a proxy of solar radiation in previous studies1,47. Since the CRU dataset included fewer observations in the early part of its record (before the 1950s)48, we used only CRU precipitation dataset for 1960–2013 and the temperature and cloud cover datasets for 1982–2012. In addition, we used two precipitation datasets (Global Precipitation Climatology Centre (GPCC) version 727 and (University of Delaware) UDel precipitation version 428) and the new temperature dataset UDel version 4 as well as a new shortwave radiation dataset. The new shortwave radiation data for the same period were obtained from the CRU-NCEP dataset, version V5.2, which combined the CRU climate dataset from 1901 to 2012 and the NCEP reanalysis from 1948 to 2012. These climate datasets have a spatial resolution of 0.5° and temporal resolution of one month. These climate datasets were used separately to test the robustness of our results. A global aridity index dataset with a spatial resolution of 0.0083° from Consultative Group for International Agricultural Research Consortium for Spatial Information (CGIAR-CSI) was used to identify arid and semi-arid regions (Fig. S3a)49,50. All the climate datasets cover our study period of 1982 to 2012, and their use in global climate and vegetation studies is well established20,47,51.
SPI data
Following a previous study16, we used the standard precipitation index (SPI) to quantify accumulated monthly precipitation anomalies. SPI is a traditionally multi-scale drought index that is useful as an indicator of cumulative precipitation anomalies. Negative SPI values indicate dry conditions, whereas positive values indicate wet conditions. Using the CRU, GPCC and UDel monthly precipitation data for 1960 to 2013, we calculated SPI from 1982 to 2012 at time scales from 1 to 12 months, following McKee et al.52.
Satellite NDVI data
The third-generation Normalized Difference Vegetation Index (NDVI3g) data used in the present study were obtained from the Global Inventory Monitoring and Modelling Studies (GIMMS) group and were derived from the NOAA/AVHRR land dataset, at a 0.083° spatial resolution and 15-day interval, for the period of January 1982 to December 2012. The GIMMS3g NDVI dataset, which provides the longest time series, has been widely used for vegetation monitoring18,47,53. The biweekly GIMSS-NDVI series were composited monthly, according to the maximum monthly value, to further eliminate disturbance from clouds, atmospheric conditions, and changes in solar altitude angle26. In order to match the NDVI data with the climate datasets (0.5° spatial resolution), we averaged the monthly NDVI data that corresponded to each climate dataset pixel.
Land cover data
We used the 5.1 MODIS land cover type climate modelling grid product (MCD12C1), which had a spatial resolution of 0.05° and provided dominant land cover types from 2001 to 201254,55. We used a land cover classification that was derived from a supervised decision-tree classification method and that was defined by the International Geography Biosphere Programme (IGBP). The classification system included 11 natural vegetation classes, three developed and mosaicked land classes, and three non-vegetated land classes. To match the data with the CRU climate datasets, we used the majority scheme to resample the land cover data to a 0.5° spatial resolution, for the period from 2001 to 2012, as described by Jong et al.47. Then, to minimize the impacts of land cover changes on vegetation, only pixels that exhibited constant vegetation types from 2001 to 2012 were kept, which yielded an unchanged vegetation type map for 2001 to 2012, at a spatial resolution of 0.5° (Fig. S4). Moreover, due to the apparent differences in climate conditions observed for shrubland at high and low latitudes, shrublands distributed north and south of 45°N were divided into two categories (Table S1).
Analysis
Because little is known about the general temporal pattern of vegetation water memory length on a monthly scale and global scales16, we assumed that the length of water memory would range from 1 to 12 months. All of the time series of the GIMMS NDVI and climate variables were detrended and standardized10. We defined the growing season as any month with a mean NDVI larger than 0.1 and a mean monthly temperature of larger than 0 °C. Additionally, pixels with annual mean NDVI values of less than 0.1 during the 31 years were excluded from the analysis. Moreover, to eliminate the negative effects from the missing values, we removed all areas where the percentage of missing values in the CRU precipitation, temperature and cloud cover datasets was greater than 5% based on the station files (Fig. S1). Thus, for each pixel, we obtained N (growing season length) series of NDVI values (one per month for each month of the growing season) from 1982 to 2012, as well as the 1- to 12-month SPI series. Then, to differentiate the responses of vegetation to SPI during different time scales within growing seasons, each of the NDVI time series was correlated with the corresponding 1- to 12-month SPI series for the period from 1982 to 2012. Finally, we obtained N*12 correlation values for each pixel (12 for each month of the growing season), and the time scale at which the maximum correlation coefficient between SPI and NDVI was highest was defined as the length of water memory.
Considering water memory effects, we took past precipitation information into account and constructed a multiple linear regression (MLR) model to quantify the sensitivity of vegetation productivity to climate variability and to identify regions with strong water memory effects, using the following equation:
1 |
where NDVIt is the standardized NDVI anomaly series at moment t; SPIt is the standardized SPI index at moment t at the time scale of water memory length; Tt is the standardized temperature anomaly series at moment t; Rt is the standardized radiation anomaly series at moment t; and ε is the residual error. Since the time series of data were detrended and standardized, the model coefficients were comparable. In particular, SPI quantifies the variation of within-memory precipitation; α describes the sensitivity of NDVI to changes in SPI; and β and δ refer to the sensitivity of NDVI to changes in temperature and shortwave radiation. Positive (negative) values of α, β and δ indicate an increase (decrease) in the NDVI response to the climate under wetter, warmer and higher solar-radiation conditions, respectively. In addition, we also constructed a model without considering antecedent precipitation, in which SPI was replaced by the contemporary precipitation, using the following equation:
2 |
where P is the standardized precipitation anomaly series at moment t, and other variables are similar to equation (1).
To investigate the relationship between water memory effects and vegetation memory effects or engineering resilience, we calculated the memory effects or engineering resilience of global vegetation using the following equation:
3 |
As described by Keersmaecker et al.4, NDVIt−1 is the standardized NDVI anomaly series at moment t−1, and γ indicates the magnitude of memory effects and the relative ecosystem recovery rates to an equilibrium state. In general, high absolute values of γ indicated strong memory effects and low recovery rate to equilibrium (i.e., a low engineering resilience). Other variables are similar to equation (1).
Data availability statement
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Electronic supplementary material
Acknowledgements
This study was supported by the National Basic Research Program of China (Grant No. 2015CB452702). We thank the Climate Research Unit, Global Precipitation Climatology Centre, and NOAA/OAR/ESRL PSD for providing climate datasets. We thank the two reviewers for their insightful comments that significantly improved the paper.
Author Contributions
S. Li. and L. Liu. designed the research; L. Liu. performed the analysis; L. Liu., Y. Zhang., and S. Li. drafted the paper. All authors contributed in the discussion of the results and in writing the paper.
Competing Interests
The authors declare no competing interests.
Footnotes
Electronic supplementary material
Supplementary information accompanies this paper at 10.1038/s41598-018-21339-4.
Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
- 1.Seddon AW, Macias-Fauria M, Long PR, Benz D, Willis KJ. Sensitivity of global terrestrial ecosystems to climate variability. Nature. 2016;531:229–232. doi: 10.1038/nature16986. [DOI] [PubMed] [Google Scholar]
- 2.Ogle K, et al. Quantifying ecological memory in plant and ecosystem processes. Ecol Lett. 2015;18:221–35. doi: 10.1111/ele.12399. [DOI] [PubMed] [Google Scholar]
- 3.Richard, Y. et al. Interannual memory effects for spring NDVI in semi-arid South Africa. Geophysical Research Letters35 (2008).
- 4.De Keersmaecker W, et al. A model quantifying global vegetation resistance and resilience to short-term climate anomalies and their relationship with vegetation cover. Global Ecology and Biogeography. 2015;24:539–548. doi: 10.1111/geb.12279. [DOI] [Google Scholar]
- 5.Shilong P, Fang J, Zhou L, Philippe C, Zhu B. Variations in satellite-derived phenology in China’s temperate vegetation. Global Change Biology. 2006;12:672–685. doi: 10.1111/j.1365-2486.2006.01123.x. [DOI] [Google Scholar]
- 6.Fu YH, et al. Declining global warming effects on the phenology of spring leaf unfolding. Nature. 2015;526:104–7. doi: 10.1038/nature15402. [DOI] [PubMed] [Google Scholar]
- 7.Malo AR, Nicholson SE. A study of rainfall and vegetation dynamics in the African Sahel using normalized difference vegetation index. Journal of Arid Environments. 1990;19:1–24. [Google Scholar]
- 8.Wang, X. et al. Spring temperature change and its implication in the change of vegetation growth in North America from 1982 to 2006. Proceedings of the National Academy of Sciences of the United States of America108, 1240 (2011). [DOI] [PMC free article] [PubMed]
- 9.Reichmann LG, Sala OE, Peters DPC. Precipitation legacies in desert grassland primary production occur through previous‐year tiller density. Ecology. 2013;94:435–443. doi: 10.1890/12-1237.1. [DOI] [PubMed] [Google Scholar]
- 10.Zeng F-W, Collatz G, Pinzon J, Ivanoff A. Evaluating and Quantifying the Climate-Driven Interannual Variability in Global Inventory Modeling and MappingStudies (GIMMS) Normalized Difference Vegetation Index (NDVI3g) at Global Scales. Remote Sensing. 2013;5:3918–3950. doi: 10.3390/rs5083918. [DOI] [Google Scholar]
- 11.Sala OE, Gherardi LA, Reichmann L, Jobbagy E, Peters D. Legacies of precipitation fluctuations on primary production: theory and data synthesis. Philos Trans R Soc Lond B Biol Sci. 2012;367:3135–44. doi: 10.1098/rstb.2011.0347. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Vargas R, et al. On the multi-temporal correlation between photosynthesis and soil CO2 efflux: reconciling lags and observations. New Phytologist. 2011;191:1006. doi: 10.1111/j.1469-8137.2011.03771.x. [DOI] [PubMed] [Google Scholar]
- 13.Ahlström A, et al. Carbon cycle. The dominant role of semi-arid ecosystems in the trend and variability of the land CO2 sink. Science. 2015;348:895–899. doi: 10.1126/science.aaa1668. [DOI] [PubMed] [Google Scholar]
- 14.Nemani RR, et al. Climate-Driven Increases in Global Terrestrial Net Primary Production from 1982 to 1999. Science. 2003;300:1560. doi: 10.1126/science.1082750. [DOI] [PubMed] [Google Scholar]
- 15.Wang J, Rich PM, Price KP. Temporal responses of NDVI to precipitation and temperature in the central Great Plains, USA. International Journal of Remote Sensing. 2003;24:2345–2364. doi: 10.1080/01431160210154812. [DOI] [Google Scholar]
- 16.Lotsch, A., Friedl, M. A., Anderson, B. T. & Tucker, C. J. Coupled vegetation-precipitation variability observed from satellite and climate records. Geophysical Research Letters30 (2003).
- 17.Yves R, et al. Interannual memory for spring NDVI in semi-arid South Africa. Geophysical Research Letters. 2008;35:195–209. [Google Scholar]
- 18.Wu D, et al. Time-lag effects of global vegetation responses to climate change. Glob Chang Biol. 2015;21:3520–31. doi: 10.1111/gcb.12945. [DOI] [PubMed] [Google Scholar]
- 19.Ji L, Peters AJ. Assessing vegetation response to drought in the northern Great Plains using vegetation and drought indices. Remote Sensing of Environment. 2003;87:85–98. doi: 10.1016/S0034-4257(03)00174-3. [DOI] [Google Scholar]
- 20.Vicente-Serrano SM, et al. Response of vegetation to drought time-scales across global land biomes. Proc Natl Acad Sci USA. 2013;110:52–7. doi: 10.1073/pnas.1207068110. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Pimm SL. The complexity and stability of ecosystems. Nature. 1984;307:321–326. doi: 10.1038/307321a0. [DOI] [Google Scholar]
- 22.Tilman D. Biodiversity: population versus ecosystem stability. Ecology. 1996;77:350–363. doi: 10.2307/2265614. [DOI] [Google Scholar]
- 23.Holling CS. Engineering resilience versus ecological resilience. Engineering within ecological constraints. 1996;31:32. [Google Scholar]
- 24.Scheffer M, et al. Early-warning signals for critical transitions. Nature. 2009;461:53–9. doi: 10.1038/nature08227. [DOI] [PubMed] [Google Scholar]
- 25.Verbesselt J, et al. Remotely sensed resilience of tropical forests. Nature Climate Change. 2016;6:1028–1031. doi: 10.1038/nclimate3108. [DOI] [Google Scholar]
- 26.Tucker CJ, et al. An extended AVHRR 8‐km NDVI dataset compatible with MODIS and SPOT vegetation NDVI data. International Journal of Remote Sensing. 2005;26:4485–4498. doi: 10.1080/01431160500168686. [DOI] [Google Scholar]
- 27.Schneider U, et al. GPCC’s new land surface precipitation climatology based on quality-controlled in situ data and its role in quantifying the global water cycle. Theoretical and Applied Climatology. 2014;115:15–40. doi: 10.1007/s00704-013-0860-x. [DOI] [Google Scholar]
- 28.Willmott, C. J., Matsuura, K. & Legates, D. Terrestrial air temperature and precipitation: monthly and annual time series (1950–1999). Center for climate research version1 (2001).
- 29.Piao S, et al. Evidence for a weakening relationship between interannual temperature variability and northern vegetation activity. Nature Communications. 2014;5:5018. doi: 10.1038/ncomms6018. [DOI] [PubMed] [Google Scholar]
- 30.Beer C, et al. Terrestrial gross carbon dioxide uptake: global distribution and covariation with climate. Science. 2010;329:834–8. doi: 10.1126/science.1184984. [DOI] [PubMed] [Google Scholar]
- 31.Chaves MM, Maroco JP, Pereira JS. Understanding plant responses to drought — from genes to the whole plant. Functional Plant Biology. 2003;30:239–264. doi: 10.1071/FP02076. [DOI] [PubMed] [Google Scholar]
- 32.Nicholson SE, Davenport ML, Malo AR. A comparison of the vegetation response to rainfall in the Sahel and East Africa, using normalized difference vegetation index from NOAA AVHRR. Climatic Change. 1990;17:209–241. doi: 10.1007/BF00138369. [DOI] [Google Scholar]
- 33.Chen T, de Jeu RAM, Liu YY, van der Werf GR, Dolman AJ. Using satellite based soil moisture to quantify the water driven variability in NDVI: A case study over mainland Australia. Remote Sensing of Environment. 2014;140:330–338. doi: 10.1016/j.rse.2013.08.022. [DOI] [Google Scholar]
- 34.Schwinning S, Sala OE. Hierarchy of responses to resource pulses in arid and semi-arid ecosystems. Oecologia. 2004;141:211–20. doi: 10.1007/s00442-004-1520-8. [DOI] [PubMed] [Google Scholar]
- 35.Smith MD, Knapp AK, Collins SL. A framework for assessing ecosystem dynamics in response to chronic resource alterations induced by global change. Ecology. 2009;90:3279–89. doi: 10.1890/08-1815.1. [DOI] [PubMed] [Google Scholar]
- 36.Anderegg WR, et al. Pervasive drought legacies in forest ecosystems and their implications for carbon cycle models. Science. 2015;349:528–532. doi: 10.1126/science.aab1833. [DOI] [PubMed] [Google Scholar]
- 37.Huete A. Ecology: Vegetation’s responses to climate variability. Nature. 2016;531:181. doi: 10.1038/nature17301. [DOI] [PubMed] [Google Scholar]
- 38.Rammig A, Mahecha MD. Ecology: Ecosystem responses to climate extremes. Nature. 2015;527:315. doi: 10.1038/527315b. [DOI] [PubMed] [Google Scholar]
- 39.Dakos V, Carpenter SR, van Nes EH, Scheffer M. Resilience indicators: prospects and limitations for early warnings of regime shifts. Philosophical Transactions of the Royal Society B Biological Sciences. 2015;370:20130263–20130263. doi: 10.1098/rstb.2013.0263. [DOI] [Google Scholar]
- 40.Hirota M, Holmgren M, Van Nes EH, Scheffer M. Global resilience of tropical forest and savanna to critical transitions. Science. 2011;334:232–235. doi: 10.1126/science.1210657. [DOI] [PubMed] [Google Scholar]
- 41.Isbell F, et al. Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature. 2015;526:574. doi: 10.1038/nature15374. [DOI] [PubMed] [Google Scholar]
- 42.Mori AS. Resilience in the Studies of Biodiversity-Ecosystem Functioning. Trends Ecol Evol. 2016;31:87–9. doi: 10.1016/j.tree.2015.12.010. [DOI] [PubMed] [Google Scholar]
- 43.Sakschewski B, et al. Resilience of Amazon forests emerges from plant trait diversity. Nature Climate Change. 2016;6:1032–1036. doi: 10.1038/nclimate3109. [DOI] [Google Scholar]
- 44.Stocker, T. F. et al. Climate change 2013: The physical science basis. Intergovernmental Panel on Climate Change, Working Group I Contribution to the IPCC Fifth Assessment Report (AR5)(CambridgeUniv Press, New York) (2013).
- 45.New M, Hulme M, Jones P. Representing twentieth-century space–time climate variability. Part II: development of 1901–96 monthly grids of terrestrial surface climate. Journal of climate. 2000;13:2217–2238. doi: 10.1175/1520-0442(2000)013<2217:RTCSTC>2.0.CO;2. [DOI] [Google Scholar]
- 46.Mitchell TD, Jones PD. An improved method of constructing a database of monthly climate observations and associated high–resolution grids. International journal of climatology. 2005;25:693–712. doi: 10.1002/joc.1181. [DOI] [Google Scholar]
- 47.Jong R, Schaepman ME, Furrer R, Bruin S, Verburg PH. Spatial relationship between climatologies and changes in global vegetation activity. Global change biology. 2013;19:1953–1964. doi: 10.1111/gcb.12193. [DOI] [PubMed] [Google Scholar]
- 48.Macias-Fauria M, Seddon AW, Benz D, Long PR, Willis K. Spatiotemporal patterns of warming. Nature Climate Change. 2014;4:845. doi: 10.1038/nclimate2372. [DOI] [Google Scholar]
- 49.Zorner RJ, Trabucco A, Bossio DA, Verchot LV. Climate change mitigation: A spatial analysis of global land suitability for clean development mechanism afforestation and reforestation. Agriculture Ecosystems & Environment. 2008;126:67–80. doi: 10.1016/j.agee.2008.01.014. [DOI] [Google Scholar]
- 50.Middleton, N. J. & Thomas, D. S. World atlas of desertification. (1992).
- 51.Peng S, et al. Asymmetric effects of daytime and night-time warming on Northern Hemisphere vegetation. Nature. 2013;501:88. doi: 10.1038/nature12434. [DOI] [PubMed] [Google Scholar]
- 52.McKee, T. B., Doesken, N. J. & Kleist, J. The relationship of drought frequency and duration to time scales. Proceedings of the 8th Conference on Applied Climatology 179–183 (American Meteorological Society, Boston, MA, 1993).
- 53.Zhou L, et al. Variations in northern vegetation activity inferred from satellite data of vegetation index during 1981 to 1999. Journal of Geophysical Research: Atmospheres. 2001;106:20069–20083. doi: 10.1029/2000JD000115. [DOI] [Google Scholar]
- 54.McIver D, Friedl M. Using prior probabilities in decision-tree classification of remotely sensed data. Remote sensing of Environment. 2002;81:253–261. doi: 10.1016/S0034-4257(02)00003-2. [DOI] [Google Scholar]
- 55.Friedl MA, et al. MODIS Collection 5 global land cover: Algorithm refinements and characterization of new datasets. Remote sensing of Environment. 2010;114:168–182. doi: 10.1016/j.rse.2009.08.016. [DOI] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.