Phenological Shifts Research Articles

Generating ecological insights from historical data

Generating ecological insights from historical data

Urban environments provide new perspectives for forecasting vegetation phenology responses under climate warming.

Given that already-observed temperature increase within cities far exceeds the projected global temperature rise by the end of the century, urban environments often offer a unique opportunity for studying ecosystem response to future warming. However, the validity of thermal gradients in space serving as a substitute for those in time is rarely tested. Here, we investigated vegetation phenology dynamics in China's 343 cities and empirically test whether phenological responses to spatial temperature rise in urban settings can substitute for those to temporal temperature rise in their natural counterparts based on satellite-derived vegetation phenology and land surface temperature from 2003 to 2018. We found prevalent advancing spring phenology with "high confidence" and delaying autumn phenology with "medium confidence" under the context of widespread urban warming. Furthermore, we showed that space cannot substitute for time in predicting phenological shifts under climate warming at the national scale and for most cities. The thresholds of ~11°C mean annual temperature and ~600 mm annual precipitation differentiated the magnitude of phenological sensitivity to temperature across space and through time. Below those thresholds, there existed stronger advanced spring phenology and delayed autumn phenology across the spatial urbanization gradients than through time, and vice versa. Despite the complex and diverse relationships between phenological sensitivities across space and through time, we found that the directions of the temperature changes across spatial gradients were converged (i.e., mostly increased), but divergent through temporal gradients (i.e., increased or decreased without a predominant direction). Similarly, vegetation phenology changes more uniformly over space than through time. These results suggested that the urban environments provide a real-world condition to understand vegetation phenology response under future warming.

Climate change is altering the physiology and phenology of an arctic hibernator.

Climate warming is rapid in the Arctic, yet impacts to biological systems are unclear because few long-term studies linking biophysiological processes with environmental conditions exist for this data-poor region. In our study spanning 25 years in the Alaskan Arctic, we demonstrate that climate change is affecting the timing of freeze-thaw cycles in the active layer of permafrost soils and altering the physiology of arctic ground squirrels (Urocitellus parryii). Soil freeze has been delayed and, in response, arctic ground squirrels have delayed when they up-regulate heat production during torpor to prevent freezing. Further, the termination of hibernation in spring has advanced 4 days per decade in females but not males. Continued warming and phenological shifts will alter hibernation energetics, change the seasonal availability of this important prey species, and potentially disrupt intraspecific interactions.

Spring phenology rather than climate dominates the trends in peak of growing season in the Northern Hemisphere.

Shifts in plant phenology regulate ecosystem structure and function, which feeds back to the climate system. However, drivers for the peak of growing season (POS) in seasonal dynamics of terrestrial ecosystems remain unclear. Here, spatial-temporal patterns of POS dynamics were analyzed by solar-induced chlorophyll fluorescence (SIF) and vegetation index in the Northern Hemisphere over the past two decades from 2001 to 2020. Overall, a slow advanced POS was observed in the Northern Hemisphere, while a delayed POS distributed mainly in northeastern North America. Trends of POS were driven by the start of growing season (SOS) rather than pre-POS climate both at hemisphere and biome scale. The effect of SOS on the trends in POS was the strongest in shrublands while the weakest in evergreen broad-leaved forest. These findings highlight the crucial role of biological rhythms rather than climatic factors in exploring seasonal carbon dynamics and global carbon balance.

Why sex matters in phenological research

Males and females often desynchronise their mating activity during the breeding season (intersexual phenological asynchrony). This suggests that the two sexes differentially use environmental cues to initiate seasonal reproduction, and climate change may cause phenological shifts in a sex‐specific manner, subsequently altering frequency distribution of mating attempts over time and influencing the emergence timing and recruitment success of juveniles. In this article, we tested these hypotheses through literature reviews and theoretical modelling. We found that the sex specificity of environmental cues and phenological shifts remain poorly understood in most sexually reproducing animal taxa because of sex‐specific publication bias and data limitations. Meanwhile, our theoretical model predicted that the ecological consequences of phenological shifts are sexually asymmetric, with earlier mating onset of males having generally greater negative effects on population growth than that of females. We therefore suggest that further research is necessary to collect and incorporate sex‐specific information on seasonal reproduction into the theory of phenological mismatch, for which previous work has mostly focused on interspecific trophic asynchrony. We also outline a future research agenda to better understand the consequences of sex‐specific phenological shifts on seasonal population dynamics and long‐term persistence of species.

Estimating phenology and phenological shifts with hierarchical modeling.

Climate-driven changes to phenology are some of the most prevalent climate change impacts, yet there is no commonly accepted approach to modeling phenological shifts. Here, we present a hierarchical modeling framework for estimating intra-annual patterns in phenology (e.g., peak phenological expression) and analyzing interannual rates of change in peak phenology. Our approach allows for the estimation of multiple sources of uncertainty, including observation error (e.g., imperfect observations of intra-annual patterns in phenology like peak flowering date) and variation in phenological processes (e.g., uncertainty in the rate of change in annual peak phenological expression). Covariates may be included as predictors of annual peaks or interannual variability in phenological responses. We demonstrate the use of our hierarchical modeling framework in two migratory species-juvenile chum salmon and Swainson's thrush. We acknowledge that the complexity of hierarchical models can be difficult to implement from scratch and present an R package that can be used to model peak dates and range (number of days between 25th- and 75th-quartile dates), as well as a rate of change in peak phenology. Increasing precision, calculating uncertainty, and allowing for imperfect data sets when estimating phenological shifts should help ecologists understand how organisms respond to climate change.

Delineation of Orchard, Vineyard, and Olive Trees Based on Phenology Metrics Derived from Time Series of Sentinel-2

This study aimed to propose an accurate and cost-effective analytical approach for the delineation of fruit trees in orchards, vineyards, and olive groves in Southern France, considering two locations. A classification based on phenology metrics (PM) derived from the Sentinel-2 time series was developed to perform the classification. The PM were computed by fitting a double logistic model on temporal profiles of vegetation indices to delineate orchard and vineyard classes. The generated PM were introduced into a random forest (RF) algorithm for classification. The method was tested on different vegetation indices, with the best results obtained with the leaf area index. To delineate the olive class, the temporal features of the green chlorophyll vegetation index were found to be the most appropriate. Obtained overall accuracies ranged from 89–96% and a Kappa of 0.86–0.95 (2016–2021), respectively. These accuracies are much better than applying the RF algorithm to the LAI time series, which led to a Kappa ranging between 0.3 and 0.52 and demonstrates the interest in using phenological traits rather than the raw time series of the remote sensing data. The method can be well reproduced from one year to another. This is an interesting feature to reduce the burden of collecting ground-truth information. If the method is generic, it needs to be calibrated in given areas as soon as a phenology shift is expected.

Phenological shifts and mismatch with marine productivity vary among Pacific salmon species and populations.

Global climate change is shifting the timing of life-cycle events, sometimes resulting in phenological mismatches between predators and prey. Phenological shifts and subsequent mismatches may be consistent across populations, or they could vary unpredictably across populations within the same species. For anadromous Pacific salmon (Oncorhynchus spp.), juveniles from thousands of locally adapted populations migrate from diverse freshwater habitats to the Pacific Ocean every year. Both the timing of freshwater migration and ocean arrival, relative to nearshore prey (phenological match/mismatch), can control marine survival and population dynamics. Here we examined phenological change of 66 populations across six anadromous Pacific salmon species throughout their range in western North America with the longest time series spanning 1951-2019. We show that different salmon species have different rates of phenological change but that there was substantial within-species variation that was not correlated with changing environmental conditions or geographic patterns. Moreover, outmigration phenologies have not tracked shifts in the timing of marine primary productivity, potentially increasing the frequency of future phenological mismatches. Understanding population responses to mismatches with prey are an important part of characterizing overall population-specific climate vulnerability.

Parasite-mediated selection on host phenology.

The timing of seasonal activity, or phenology, is an adaptive trait that maximizes individual fitness by timing key life events to coincide with favorable abiotic factors and biotic interactions. Studies on the biotic interactions that determine optimal phenology have focused on temporal overlaps among positively-interacting species such as mutualisms. Less well understood is the extent that negative interactions such as parasitism impact the evolution of host phenology. Here, we present a mathematical model demonstrating the evolution of host phenological patterns in response to sterilizing parasites. Environments with parasites favor hosts with shortened activity periods or greater distributions in emergence timing, both of which reduce the temporal overlap between hosts and parasites and thus reduce infection risk. Although host populations with these altered phenological patterns are less likely to mature and reproduce, the fitness advantage of parasite avoidance can be greater than the cost of reduced reproduction. These results illustrate the impact of parasitism on the evolution of host phenology and suggest that shifts in host phenology could serve as a strategy to mitigate the risk of infection.

Shifted Global Vegetation Phenology in Response to Climate Changes and Its Feedback on Vegetation Carbon Uptake

Green vegetation plays a vital role in energy flows and matter cycles in terrestrial ecosystems, and vegetation phenology may not only be influenced by, but also impose active feedback on, climate changes. The phenological events of vegetation such as the start of season (SOS), end of season (EOS), and length of season (LOS) can respond to climate changes and affect gross primary productivity (GPP). Here, we coupled satellite remote sensing imagery with FLUXNET observations to systematically map the shift of SOS, EOS, and LOS in global vegetated area, and explored their response to climate fluctuations and feedback on GPP during the last two decades. The results indicated that 11.5% of the global vegetated area showed a significantly advanced trend in SOS, and that only 5.2% of the area presented significantly delayed EOS during the past two decades, resulting in significantly prolonged LOS in 12.6% of the vegetated area. The climate factors, including seasonal temperature and precipitation, attributed to the shifts in vegetation phenology, but with high spatial and temporal difference. LOS was positively and significantly correlated with GPP in 20.2% of the total area, highlighting that longer LOS is likely to promote vegetation productivity. The feedback on GPP from the shifted vegetation phenology may serve as an adaptation mechanism for terrestrial ecosystems to mitigate global warming through improved carbon uptake from the atmosphere.

Phenology advances uniformly in spring but diverges in autumn among three temperate tree species in response to warming

Predicting the length of growing season to further warming relies on both spring and autumn phenological responses of different species, but with little experimental evidence under different levels of warming. Here, the timing of spring phenology including budburst and leaf unfolding, and autumn phenology including leaf coloration and leaf fall, were examined in 2-year-old seedlings of three temperate tree species (Fraxinus mandschurica, Quercus mongolica, and Juglans mandshurica) that were grown in the field under warming conditions (W0, ambient; W2, +2°C; W4, +4°C). Our study showed that warming advanced budburst and leaf unfolding by 9 and 8 days in the W2 treatments and by 13 and 15 days in the W4 treatments, respectively, with the magnitude varied greatly among species. However, we found a delayed autumn leaf senescence only for Q. mongolica, for which leaf coloration and leaf fall delayed by 19 and 6 days and by 17 and 12 days in the W2 and W4 treatments, respectively. The temperature sensitivity of budburst declined with increasing temperature in Q. mongolica. The growing season was extended by 7–18 and 10–25 days in W2 and W4, primarily through the advancement of spring phenology. Warming increased budburst synchrony, such that J. mandshurica, which typically has the earliest leaf emergence, lost its growth and competitive advantages over the more phenologically plastic species, F. mandschurica and Q. mongolica. Our results provide new insights into the effects of elevated temperatures on phenological shifts and their potential influences on tree species recruitment and forest structure and composition.

Phytoplankton life strategies, phenological shifts and climate change in the North Atlantic Ocean from 1850-2100.

Significant phenological shifts induced by climate change are projected within the phytoplankton community. However, projections from current Earth System Models (ESMs) understandably rely on simplified community responses that do not consider evolutionary strategies manifested as various phenotypes and trait groups. Here, we use a species-based modelling approach, combined with large-scale plankton observations, to investigate past, contemporary and future phenological shifts in diatoms (grouped by their morphological traits) and dinoflagellates in three key areas of the North Atlantic Ocean (North Sea, North-East Atlantic and Labrador Sea) from 1850 to 2100. Our study reveals that the three phytoplanktonic groups exhibit coherent and different shifts in phenology and abundance throughout the North Atlantic Ocean. The seasonal duration of large flattened (i.e., oblate) diatoms is predicted to shrink and their abundance to decline, whereas the phenology of slow-sinking elongated (i.e., prolate) diatoms and of dinoflagellates is expected to expand and their abundance to rise, which may alter carbon export in this important sink region. The increase in prolates and dinoflagellates, two groups currently not considered in ESMs, may alleviate the negative influence of global climate change on oblates, which are responsible of massive peaks of biomass and carbon export in spring. We suggest that including prolates and dinoflagellates in models may improve our understanding of the influence of global climate change on the biological carbon cycle in the oceans.

Increasing temperature regulates the advance of peak photosynthesis timing in the boreal ecosystem

The shift in vegetation phenology is an essential indicator of global climate change. Numerous researches based on reflectance-based vegetation index data have explored the changes in the start (SOS) and end (EOS) of vegetation life events at long time scales, while a huge discrepancy existed between the phenological metrics of vegetation structure and function. The peak photosynthesis timing (PPT), which is crucial in regulating terrestrial ecosystem carbon balance, has not received much attention. Using two global reconstructed solar-induced chlorophyll fluorescence data (CSIF and GOSIF) directly associated with vegetation photosynthesis, the spatio-temporal dynamics in PPT as well as the key environmental controls across the boreal ecosystem during 2001–2019 were systematically explored. Multi-year mean pattern showed that PPT mainly appeared in the first half of July. Compared to the northern Eurasia, later PPT appeared in the northern North America continent for about 4–5 days. Meanwhile, spatial trend in PPT exhibited an advanced trend during the last two decades. Especially, shrubland and grassland were obvious among all biomes. Spatial partial correlation analysis revealed that preseason temperature was the dominant environmental driver of PPT trends, occupying 81.32% and 78.04% of the total pixels of PPTCSIF and PPTGOSIF, respectively. Attribution analysis by ridge regression again emphasized the largest contribution of temperature to PPT dynamics in the boreal ecosystem by 52.22% (PPTCSIF) and 46.59% (PPTGOSIF), followed by radiation (PPTCSIF: 24.44%; PPTGOSIF: 28.66%) and precipitation (PPTCSIF: 23.34%; PPTGOSIF: 24.75%). These results have significant implications for deepening our understanding between vegetation photosynthetic phenology and carbon cycling with respect to future climate change in the boreal ecosystem.

Rubber leaf fall phenomenon linked to increased temperature

Understanding phenological responses of vegetation to temperature have become increasingly important as the global climate changes. We examined how changes in temperature may be associated with the occurrence of rubber leaf fall, a new phenomenon affecting many rubber (Hevea brasiliensis) plantations. Spatial and temporal characteristics of the start and end of the rubber season for six study areas from four major rubber-producing countries were investigated using satellite imagery and 10 years of surface temperature data from 2010 to 2019. These study areas were Palembang (1154 ha) in South Sumatra, Indonesia; Medan (2667 ha) in North Sumatra, Indonesia; Ratnapura (581 ha) in Sri Lanka; Johor (195 ha) in Malaysia; Kedah (803 ha) in Malaysia; and Tboung Khmum (2421 ha) in Cambodia. Our results showed that there was a significant upward trend in average mean temperature for Palembang, Medan, Ratnapura and Johor, and that these trends were associated with a statistically significant difference in rubber defoliation and refoliation events. This shift also coincides with the reported occurrence of Rubber Leaf Fall disease from these study areas. In contrast, no change in temperature trends or phenological shift was identified for the two other study areas, and the disease was not reported in these areas. Overall, warming resulted in delayed phenological timing in most locations. While additional research is required to exclude alternative explanations, there is a strong possibility that climate change is responsible for the emergence of the new Rubber Leaf Fall disease.

Experimental warming causes mismatches in alpine plant-microbe-fauna phenology

Long-term observations have shown that many plants and aboveground animals have changed their phenology patterns due to warmer temperatures over the past decades. However, empirical evidence for phenological shifts in alpine organisms, particularly belowground organisms, is scarce. Here, we investigate how the activities and phenology of plants, soil microbes, and soil fauna will respond to warming in an alpine meadow on the Tibetan Plateau, and whether their potential phenological changes will be synchronized. We experimentally simulate an increase in soil temperature by 2–4 °C according to future projections for this region. We find that warming promotes plant growth, soil microbial respiration, and soil fauna feeding by 8%, 57%, and 20%, respectively, but causes dissimilar changes in their phenology during the growing season. Specifically, warming advances soil faunal feeding activity in spring and delays it in autumn, while their peak activity does not change; whereas warming increases the peak activity of plant growth and soil microbial respiration but with only minor shifts in their phenology. Such phenological asynchrony in alpine organisms may alter ecosystem functioning and stability.

Climate change is leading to rapid shifts in seasonality in the himalaya.

Climate change has significantly impacted vegetation phenology across the globe with vegetation experiencing an advance in the spring green-up phases and a delay in fall senescence. However, some studies from high latitudes and high elevations have instead shown delayed spring phenology, owing to a lack of chilling fulfillment and altered snow cover and photoperiods. Here we use the MODIS satellite-derived view-angle corrected surface reflectance data (MCD43A4) to document the four phenological phases in the high elevations of the Sikkim Himalaya and compared the phenological trends between below-treeline zones and above-treeline zones. This analysis of remotely sensed data for the study period (2001-2017) reveals considerable shifts in the phenology of the Sikkim Himalaya. Advances in the spring start of the season phase (SOS) were more pronounced than delays in the dates for maturity (MAT), senescence (EOS), and advanced dormancy (DOR). The SOS significantly advanced by 21.3 days while the MAT and EOS were delayed by 15.7 days and 6.5 days respectively over the 17-year study period. The DOR showed an advance of 8.2 days over the study period. The region below the treeline showed more pronounced shifts in phenology with respect to an advanced SOS and a delayed EOS and DOR that above treeline. The MAT, however, showed a greater delay in the zone above the treeline than below. Lastly, unlike other studies from high elevations, there is no indication that winter chilling requirements are driving the spring phenology in this region. We discuss four possible explanations for why vegetation phenology in the high elevations of the Eastern Himalaya may exhibit trends independent of chilling requirements and soil moisture due to mediation by snow cover.

TRANCO: Thermo radiometric normalization of crop observations

Crop type maps are essential for a wide range of applications such as crop monitoring, and yield estimation. In addition, Earth Observation (EO) systems allow robust and timely mapping of the earth’s surface, usually based on time-series. Yet, existing crop type maps are either global at coarse spatial resolution, or have a local or regional scope. The reasons for this gap can be linked to the scarcity of global crop type datasets at field level to train the models, their bias towards the Northern Hemisphere, as well as the limited transferability of existing crop type models across different regions. One of the main limitations on the transferability is driven by the phenological shift of the crops’ radiometric time series detected by Earth Observation (EO) systems, which is mainly induced by the different climates across regions. In this study, we explore the normalization of EO-based wheat time series with the accumulation of Growing Degree Days (GDD): the Thermo-RAdiometric Normalization of Crop Observations (TRANCO) system. The TRANCO system is based on the assumption that crop phenology evolution is mainly driven by temperature accumulation, represented by the accumulated GDD from Start of Season (SOS) to End of Season (EOS) dates, derived from a crop calendar. We tested the proposed method to normalize wheat on a database of globally distributed samples, whose results show a great improvement of the GDD F1 score (0.90) compared to a simpler normalization approach based on Time windows defined from SOS calendars (0.87) and a baseline without normalization (0.83).

Multiple factors induce temporal shifts in herbaceous plant leaf senescence dates on the Qinghai–Tibetan Plateau

Plant autumn phenology affects ecosystem carbon and water cycles. However, autumn phenological shifts of herbaceous plants and their primary regulators on the Qinghai–Tibetan Plateau (QTP) remain uncertain because previous studies were mainly based on remote sensing data. Studies using ground autumn phenological data observed at many stations are very few. This study explored the primary drivers of temporal shifts in leaf senescence date (LSD) and assessed the relative importance of climatic factors and spring phenophases to LSD shifts using correlation analysis, general linear regression, and partial least squares regression based on 1685 phenological records at 27 stations on the QTP. Results showed that, preseason total precipitation (PRE) and minimum air temperature (Tmin) had higher correlation coefficients with LSD and displayed more extensive importance in predicting LSD than other factors. Despite larger influences, contributions of PRE and Tmin to LSD inter-annual variations were only 14.9% and 14.2%, respectively. In total, PRE and air temperatures (TEMs) just explained 38.0% of LSD temporal shifts. These results indicate that although PRE and TEMs are the major regulators of LSD, temporal shifts in LSD are controlled by multiple factors. Overall, climatic factors and spring phenology contributed 53.7% and 15.6% to LSD variations, respectively, which means that climate change obviously outweighed spring phenology in driving LSD shifts. Our study revealed a critical role of PRE in regulating LSD shifts directly or indirectly by enhancing the sensitivity of LSD to TEMs. Moreover, we found that the impacts of precipitation change were more prominent on LSD of sedges than those of grasses and forbs. Therefore, we suggest that accurate autumn phenological models for plants on the QTP should include multiple factors and incorporate the influences of precipitation. This study can also provide insight into QTP grassland management from the perspective of phenological responses to climate change.

Emergence phenology of the giant salmonfly and responses by birds in Idaho river networks

Emergence of adult aquatic insects from rivers is strongly influenced by water temperature, and emergence timing helps to determine the availability of this ephemeral food resource for birds and other terrestrial insectivores. It is poorly understood how spatial heterogeneity in riverine habitat mediates the timing of emergence. Such spatiotemporal variation may have consequences for terrestrial insectivores that rely on aquatic-derived prey resources. We investigated emergence phenology of the giant salmonfly, Pteronarcys californica, at three spatial scales in two Idaho river networks. We examined the influence of tributary confluences on salmonfly emergence timing and associated insectivorous bird responses. Salmonfly emergence timing was highly variable at the basin-scale during the period we sampled (May–June). Within sub-drainage pathways not punctuated by major tributaries, emergence followed a downstream-to-upstream pattern. At the scale of reaches, abrupt changes in thermal regimes created by 10 major tributary confluences created asynchrony in emergence of 1–6 days among the 20 reaches bracketing the confluences. We observed 10 bird species capturing emerged salmonflies, including 5 species typically associated with upland habitats (e.g., American robin, red-tailed hawk, American kestrel) but that likely aggregated along rivers to take advantage of emerging salmonflies. Some birds (e.g., Lewis’s woodpecker, western tanager, American dipper) captured large numbers of salmonflies, and some of these fed salmonflies to nestlings. Emergence asynchrony created by tributaries was associated with shifts in bird abundance and richness which both nearly doubled, on average, during salmonfly emergence. Thermal heterogeneity in river networks created asynchrony in aquatic insect phenology which prolonged the availability of this pulsed prey resource for insectivorous birds during key breeding times. Such interactions between spatial and temporal heterogeneity and organism phenology may be critical to understanding the consequences of fluxes of resources that link water and land. Shifts in phenology or curtailment of life history diversity in organisms like salmonflies may have implications for these organisms, but could also contribute to mismatches or constrain availability of pulsed resources to dependent consumers. These could be unforeseen consequences, for both aquatic and terrestrial organisms, of human-driven alteration and homogenization of riverscapes.

Tracking phenological distributions and interaction potential across life stages

Climate change is shifting the phenological timing, duration, and temporal overlap of interacting species in natural communities, reshaping temporal interaction networks worldwide. Despite much recent progress in documenting these phenological shifts, little is known about how the phenologies of species interactions are tracked across different life history stages. Here we analyze four key phenological traits and the pairwise interaction potential of nine amphibian species for the adult (calling/breeding) and subsequent larval (tadpole) stage at eight different sites over six years. We found few strong correlations among phenological traits within species, but the strength of these correlations varied across species. As a consequence, phenological trait combinations of both stages varied substantially across species without clear signs of multidimensional clustering, indicating a distinct and diverse range of species‐specific phenological strategies. Despite this considerable variation in the phenologies across species, the temporal overlap between species was largely preserved through the two life history stages. Further, we also detected significant correlations among the duration and temporal overlap of interactions with other species across stages in five species, demonstrating that temporal patterns of species interactions are mirrored across life history stages. For these species, these results indicate a strong tracking of phenologies and species interactions across life history stages even in species with complex life cycles where stages occupy completely different environments. This suggests that phenological shifts in one stage can impact the temporal dynamics and structure of interaction networks across developmental stages.