Long-term, climate-driven phenological shift in a tropical large carnivore.

Understanding the degree to which animals are shifting their phenology to track optimal conditions as the climate changes is essential to predicting ecological responses to global change. Species at low latitudes or high trophic levels are theoretically expected to exhibit weaker phenological responses than other species, but limited research on tropical systems or on top predators impedes insight into the contexts in which these predictions are upheld. Moreover, a lack of phenological studies on top predators limits understanding of how climate change impacts propagate through entire ecosystems. Using a 30-y dataset on endangered African wild dogs (Lycaon pictus), we examined changes in reproductive phenology and temperatures during birthing and denning over time, as well as potential fitness consequences of these changes. We hypothesized that their phenology would shift to track a stable thermal range over time. Data from 60 packs and 141 unique pack-years revealed that wild dogs have delayed parturition by 7 days per decade on average in response to long-term warming. This shift has led to temperatures on birthing dates remaining relatively stable but, contrary to expectation, has led to increased temperatures during denning periods. Increased denning temperatures were associated with reduced reproductive success, suggesting that a continued phenological shift in the species may become maladaptive. Such results indicate that climate-driven shifts could be more widespread in upper trophic levels than previously appreciated, and they extend theoretical understanding of the species traits and environmental contexts in which large phenological shifts can be expected to occur as the climate changes.

Climate change increases flowering duration, driving phenological reassembly and elevated co-flowering richness.

Changes to flowering phenology are a key response of plants to climate change. However, we know little about how these changes alter temporal patterns of reproductive overlap (i.e. phenological reassembly). We combined long-term field (1937-2012) and herbarium records (1850-2017) of 68 species in a flowering plant community in central North America and used a novel application of Bayesian quantile regression to estimate changes to flowering season length, altered richness and composition of co-flowering assemblages, and whether phenological shifts exhibit seasonal trends. Across the past century, phenological shifts increased species' flowering durations by 11.5 d on average, which resulted in 94% of species experiencing greater flowering overlap at the community level. Increases to co-flowering were particularly pronounced in autumn, driven by a greater tendency of late season species to shift the ending of flowering later and to increase flowering duration. Our results demonstrate that species-level phenological shifts can result in considerable phenological reassembly and highlight changes to flowering duration as a prominent, yet underappreciated, effect of climate change. The emergence of an autumn co-flowering mode emphasizes that these effects may be season-dependent.

Beyond the usual climate? Factors determining flowering and fruiting phenology across a genus over 117 years.

PREMISE: Although changes in plant phenology are largely attributed to changes in climate, the roles of other factors such as genetic constraints, competition, and self-compatibility are underexplored. METHODS: We compiled >900 herbarium records spanning 117 years for all eight nominal species of the winter-annual genus Leavenworthia (Brassicaceae). We used linear regression to determine the rate of phenological change across years and phenological sensitivity to climate. Using a variance partitioning analysis, we assessed the relative influence of climatic and nonclimatic factors (self-compatibility, range overlap, latitude, and year) on Leavenworthia reproductive phenology. RESULTS: Flowering advanced by ~2.0 days and fruiting by ~1.3 days per decade. For every 1°C increase in spring temperature, flowering advanced ~2.3 days and fruiting ~3.3 days. For every 100 mm decrease in spring precipitation, each advanced ~6-7 days. The best models explained 35.4% of flowering variance and 33.9% of fruiting. Spring precipitation accounted for 51.3% of explained variance in flowering date and 44.6% in fruiting. Mean spring temperature accounted for 10.6% and 19.3%, respectively. Year accounted for 16.6% of flowering variance and 5.4% of fruiting, and latitude for 2.3% and 15.1%, respectively. Nonclimatic variables combined accounted for <11% of the variance across phenophases. CONCLUSIONS: Spring precipitation and other climate-related factors were dominant predictors of phenological variance. Our results emphasize the strong effect of precipitation on phenology, especially in the moisture-limited habitats preferred by Leavenworthia. Among the many factors that determine phenology, climate is the dominant influence, indicating that the effects of climate change on phenology are expected to increase.

Climate change is associated with increased allocation to potential outcrossing in a common mixed mating species.

PREMISE: Although the balance between cross- and self-fertilization is driven by the environment, no long-term study has documented whether anthropogenic climate change is affecting reproductive strategy allocation in species with mixed mating systems. Here, we test whether the common blue violet (Viola sororia; Violaceae) has altered relative allocation to the production of potentially outcrossing flowers as the climate has changed throughout the 20th century. METHODS: Using herbarium records spanning from 1875 to 2015 from the central United States, we quantified production of obligately selfing cleistogamous (CL) flowers and potentially outcrossing chasmogamous (CH) flowers by V. sororia, coupled these records with historic temperature and precipitation data, and tested whether changes to the proportion of CL flowers correlate with temporal climate trends. RESULTS: We find that V. sororia progressively produced lower proportions of CL flowers across the past century and in environments with lower mean annual temperature and higher total annual precipitation. We also find that both CL and CH flower phenology has advanced across this time period. CONCLUSIONS: Our results suggest that V. sororia has responded to lower temperatures and greater water availability by shifting reproductive strategy allocation away from selfing and toward potential outcrossing. This provides the first long-term study of how climate change may affect relative allocation to potential outcrossing in species with mixed mating systems. By revealing that CL flowering is associated with low water availability and high temperature, our results suggest the production of obligately selfing flowers is favored in water limited environments.

Global warming leads to more uniform spring phenology across elevations.

One hundred years ago, Andrew D. Hopkins estimated the progressive delay in tree leaf-out with increasing latitude, longitude, and elevation, referred to as "Hopkins' bioclimatic law." What if global warming is altering this well-known law? Here, based on ∼20,000 observations of the leaf-out date of four common temperate tree species located in 128 sites at various elevations in the European Alps, we found that the elevation-induced phenological shift (EPS) has significantly declined from 34 d⋅1,000 m-1 conforming to Hopkins' bioclimatic law in 1960, to 22 d⋅1,000 m-1 in 2016, i.e., -35%. The stronger phenological advance at higher elevations, responsible for the reduction in EPS, is most likely to be connected to stronger warming during late spring as well as to warmer winter temperatures. Indeed, under similar spring temperatures, we found that the EPS was substantially reduced in years when the previous winter was warmer. Our results provide empirical evidence for a declining EPS over the last six decades. Future climate warming may further reduce the EPS with consequences for the structure and function of mountain forest ecosystems, in particular through changes in plant-animal interactions, but the actual impact of such ongoing change is today largely unknown.

Climate warming increases spring phenological differences among temperate trees.

Climate warming has substantially advanced spring leaf flushing, but winter chilling and photoperiod co-determine the leaf flushing process in ways that vary among species. As a result, the interspecific differences in spring phenology (IDSP) are expected to change with climate warming, which may, in turn, induce negative or positive ecological consequences. However, the temporal change of IDSP at large spatiotemporal scales remains unclear. In this study, we analyzed long-term in-situ observations (1951-2016) of six, coexisting temperate tree species from 305 sites across Central Europe and found that phenological ranking did not change when comparing the rapidly warming period 1984-2016 to the marginally warming period 1951-1983. However, the advance of leaf flushing was significantly larger in early-flushing species EFS (6.7 ± 0.3 days) than in late-flushing species LFS (5.9 ± 0.2 days) between the two periods, indicating extended IDSP. This IDSP extension could not be explained by differences in temperature sensitivity between EFS and LFS; however, climatic warming-induced heat accumulation effects on leaf flushing, which were linked to a greater heat requirement and higher photoperiod sensitivity in LFS, drove the shifts in IDSP. Continued climate warming is expected to further extend IDSP across temperate trees, with associated implications for ecosystem function.

Experimental shifts in phenology affect fitness, foraging, and parasitism in a native solitary bee.

Phenological shifts have been observed in a wide range of taxa, but the fitness consequences of these shifts are largely unknown, and we often lack experimental studies to assess their population-level and evolutionary consequences. Here, we describe an experimental study to determine the fitness consequences of phenological shifts in blue orchard bee (Osmia lignaria) emergence, compare the measured seasonal fitness landscape with observed phenology in the unmanipulated population, and assess seasonal variation in key factors related to reproduction, foraging, and brood parasitism that were expected to affect the shape of the fitness landscape. By tracking individually marked females, we were able to estimate the lifetime fitness impacts of phenological advances and delays. We also measured parasitism risk, floral resource use, and nesting behavior to understand how each varies seasonally, and their combined effects on realized fitness. Survival to nesting decreased non-monotonically throughout the season, with a 20.4% decline in survival rates between the first and second cohorts. The total reproductive output per maternal bee was 14.9% higher in the second cohort compared to the first, and 161% higher in the second cohort compared to the third. Combining seasonal patterns in survival and reproductive output, experimentally advanced females showed 30.6% higher fitness than bees released at the historic peak. In contrast, the nesting phenology of unmanipulated bees showed nearly equal numbers of nesting attempts in the first two cohorts. Both increased resource availability and reduced parasitism risk favored earlier emergence. These results are consistent with a population experiencing directional selection for earlier emergence, adaptive bet-hedging, or developmental constraints. Our study offers insight into the fitness consequences of phenological shifts, the mechanisms affecting the fitness consequences of phenological shifts in a community context, and the potential for adaptive responses to climate change.

Desynchronizations in bee-plant interactions cause severe fitness losses in solitary bees.

Global warming can disrupt mutualistic interactions between solitary bees and plants when increasing temperature differentially changes the timing of interacting partners. One possible scenario is for insect phenology to advance more rapidly than plant phenology. However, empirical evidence for fitness consequences due to temporal mismatches is lacking for pollinators and it remains unknown if bees have developed strategies to mitigate fitness losses following temporal mismatches. We tested the effect of temporal mismatches on the fitness of three spring-emerging solitary bee species, including one pollen specialist. Using flight cages, we simulated (i) a perfect synchronization (from a bee perspective): bees and flowers occur simultaneously, (ii) a mismatch of 3 days and (iii) a mismatch of 6 days, with bees occurring earlier than flowers in the latter two cases. A mismatch of 6 days caused severe fitness losses in all three bee species, as few bees survived without flowers. Females showed strongly reduced activity and reproductive output compared to synchronized bees. Fitness consequences of a 3-day mismatch were species-specific. Both the early-spring species Osmia cornuta and the mid-spring species Osmia bicornis produced the same number of brood cells after a mismatch of 3 days as under perfect synchronization. However, O. cornuta decreased the number of female offspring, whereas O. bicornis spread the brood cells over fewer nests, which may increase offspring mortality, e.g. due to parasitoids. The late-spring specialist Osmia brevicornis produced fewer brood cells even after a mismatch of 3 days. Additionally, our results suggest that fitness losses after temporal mismatches are higher during warm than cold springs, as the naturally occurring temperature variability revealed that warm temperatures during starvation decreased the survival rate of O. bicornis. We conclude that short temporal mismatches can cause clear fitness losses in solitary bees. Although our results suggest that bees have evolved species-specific strategies to mitigate fitness losses after temporal mismatches, the bees were not able to completely compensate for impacts on their fitness after temporal mismatches with their food resources.

Variation in phenology and density differentially affects predator-prey interactions between salamanders.

Variation in the timing of breeding (i.e., phenological variation) can affect species interactions and community structure, in part by shifting body size differences between species. Body size differences can be further altered by density-dependent competition, though synergistic effects of density and phenology on species interactions are rarely evaluated. We tested how field-realistic variation in phenology and density affected ringed salamander (Ambystoma annulatum) predation on spotted salamanders (Ambystoma maculatum), and whether these altered salamander dynamics resulted in trophic cascades. In outdoor mesocosms, we experimentally manipulated ringed salamander density (low/high) and breeding phenology (early/late) of both species. Ringed salamander body size at metamorphosis, development, and growth were reduced at higher densities, while delayed phenology increased hatchling size and larval development, but reduced relative growth rates. Survival of ringed salamanders was affected by the interactive effects of phenology and density. In contrast, spotted salamander growth, size at metamorphosis, and survival, as well as the biomass of lower trophic levels, were negatively affected primarily by ringed salamander density. In an additional mesocosm experiment, we isolated whether ringed salamanders could deplete shared resources prior to their interactions with spotted salamanders, but instead found direct interactions (e.g., predation) were the more likely mechanism by which ringed salamanders limited spotted salamanders. Overall, our results indicate the effects of phenological variability on fitness-related traits can be modified or superseded by differences in density dependence. Identifying such context dependencies will lead to greater insight into when phenological variation will likely alter species interactions.

Community-wide changes in intertaxonomic temporal co-occurrence resulting from phenological shifts.

Global climate change is known to affect the assembly of ecological communities by altering species' spatial distribution patterns, but little is known about how climate change may affect community assembly by changing species' temporal co-occurrence patterns, which is highly likely given the widely observed phenological shifts associated with climate change. Here, we analyzed a 29-year phenological data set comprising community-level information on the timing and span of temporal occurrence in 11 seasonally occurring animal taxon groups from 329 local meteorological observatories across China. We show that widespread shifts in phenology have resulted in community-wide changes in the temporal overlap between taxa that are dominated by extensions, and that these changes are largely due to taxa's altered span of temporal occurrence rather than the degree of synchrony in phenological shifts. Importantly, our findings also suggest that climate change may have led to less phenological mismatch than generally presumed, and that the context under which to discuss the ecological consequences of phenological shifts should be expanded beyond asynchronous shifts.

Patterns of bird migration phenology in South Africa suggest northern hemisphere climate as the most consistent driver of change.

Current knowledge of phenological shifts in Palearctic bird migration is largely based on data collected on migrants at their breeding grounds; little is known about the phenology of these birds at their nonbreeding grounds, and even less about that of intra-African migrants. Because climate change patterns are not uniform across the globe, we can expect regional disparities in bird phenological responses. It is also likely that they vary across species, as species show differences in the strength of affinities they have with particular habitats and environments. Here, we examine the arrival and departure of nine Palearctic and seven intra-African migratory species in the central Highveld of South Africa, where the former spend their nonbreeding season and the latter their breeding season. Using novel analytical methods based on bird atlas data, we show phenological shifts in migration of five species - red-backed shrike, spotted flycatcher, common sandpiper, white-winged tern (Palearctic migrants), and diederik cuckoo (intra-African migrant) - between two atlas periods: 1987-1991 and 2007-2012. During this time period, Palearctic migrants advanced their departure from their South African nonbreeding grounds. This trend was mainly driven by waterbirds. No consistent changes were observed for intra-African migrants. Our results suggest that the most consistent drivers of migration phenological shifts act in the northern hemisphere, probably at the breeding grounds.

Specialization and phenological synchrony of plant-pollinator interactions along an altitudinal gradient.

One of the most noticeable effects of anthropogenic climate change is the shift in timing of seasonal events towards earlier occurrence. The high degree of variation in species' phenological shifts has raised concerns about the temporal decoupling of interspecific interactions, but the extent and implications of this effect are largely unknown. In the case of plant-pollinator systems, more specialized species are predicted to be particularly threatened by phenological decoupling, since they are assumed to be less flexible in the choice of interaction partners, but until now this hypothesis has not been tested. In this paper, we studied phenology and interactions of plant and pollinator communities along an altitudinal gradient in the Alps as a model for the possible effects of climate change in time. Our results show that even relatively specialized pollinators were much more flexible in their use of plant species as floral resources than their local flower visitation suggested. We found no relationship between local specialization of pollinators and the consistency of their visitation patterns across sites, and also no relationship between specialization and phenological synchrony of pollinators with particular plants. Thus, in contrast to the conclusions of a recent simulation study, our results suggest that most pollinator species included in this study are not threatened by phenological decoupling from specific flowering plants. However, the flexibility of many rarely observed pollinator species remains unknown. Moreover, our results suggest that specialized flower visitors select plant species based on certain floral traits such as the length of the nectar holder tube. If that is the case, the observed flexibility of plant-pollinator interactions likely depends on a high degree of functional redundancy in the plant community, which may not exist in less diverse systems.

Climate-driven phenological shifts in emergence dates of British bees.

Climate change has a diverse range of impacts on wild bees, including their phenology or timing of life history events. Climate-driven phenological shifts can not only impact individuals at species level but also threaten the vital pollination service that wild bees provide to both wild plants and cultivated crops. Despite their involvement in pollination, for most bee species, especially in Great Britain, little is known about phenological shifts. This study makes use of 40 years of presence-only data for 88 species of wild bees to analyse shifts in emergence dates, both over time and in relation to temperature. The analyses reveal widespread advances in emergence dates of British wild bees, at an average rate of 0.40 ± 0.02 days per year since 1980 across all species in the study data set. Temperature is a key driver of this shift, with an average advance of 6.5 ± 0.2 days per 1°C warming. For change in emergence dates both over time and in relation to temperature, there was significant species-specific variation, with 14 species showing significant advances over time and 67 showing significant advances in relation to temperature. Traits did not appear to explain variation in individual species' responses, with overwintering stage, lecty, emergence period and voltinism considered as possible explanatory traits. Pairwise comparisons showed no differences in sensitivity of emergence dates to increasing temperature between trait groups (groups of species which share all four traits) that differed by only one trait. These results highlight not only a direct impact of temperature on the phenology of wild bees themselves but also the species-specific shifts highlight a possible impact on the temporal structure of bee communities and the pollination networks for which the wild bees are so crucial.

Which factor explains the life-history of Xanthium strumarium L., an aggressive alien invasive plant species, along its altitudinal gradient?

Invasive biology acknowledges the concept of better performance by invasive plants in the introduced range. Xanthium strumarium L. is one of the successful invasive species in Khyber Pakhtunkhwa, Pakistan. The phenological pattern, vegetative and reproductive traits plasticity analysis of the species was explored to explain the invasive success across the altitudinal gradient in the current invaded habitats. Phenological patterns and timing (seedling, vegetative growth, flowering and fruiting, drying, and seed bank) were observed during a full year for two seasons. We also examine plant functional traits at altitudes of 500, 1000, and 1500 m a.s.l. to assess traits and biomass variations. The X. strumarium exhibits late vegetative and reproductive phenology at higher altitudes, enabling them to occupy an empty niche and benefit from decreased competition for resource acquisition. The lower altitude plants show a higher growth rate (stem size increase, number of leaves, and leaf area) due to the higher nutrient availability. Higher altitude plants have the highest reproductive biomass and biomass ratio revealing plant abilities to be reproductively adapted in the higher altitudes. Among climatic variables, mean yearly temperature, mean annual yearly humidity, and mean day length in hours, while in soil variables, organic matter and nitrogen percentage significantly affect the phenological and morphological stages. Therefore, we conclude that X. strumarium can invade higher altitudes with a shift in its phenological and morphological changes making the invasion process successful.

Consistent temperature-dependent patterns of leaf lifespan across spatial and temporal gradients for deciduous trees in Europe.

Temperature affects leaf lifespan (LL) across either space or time, driving long-term adaptation and short-term thermal acclimation, respectively. However, a comprehensive understanding of the phenomenon and the underlying phenological mechanisms remain poorly understood. The present study investigated the relationship between LL and temperature in six common deciduous trees across both spatial and temporal gradients, then explained the LL variation patterns based on phenological shifts. Using long-term (1971-2000) phenological records of six deciduous tree species at 54 sites across central Europe, we analyzed spatial and temporal variations of LL and leaf phenology along temperature gradients. We assessed the relative contribution of phenological shifts to LL variations by comparing absolute changes in leaf-out and leaf fall. We reported positive LL-temperature relationships across all observations along both spatial (+3.32 days/°C) and temporal (+4.43 days/°C) gradients. The paired t-test of the six deciduous tree species showed no significant difference in regression slopes of LL- temperature between the two gradients (t = -1.50, df = 5, P = 0.194). Prolonged LL can be explained mainly by earlier leaf-out induced by warmer temperatures both spatially (-3.22 days/°C) and temporally (-4.08 days/°C). The converging temperature-dependent patterns of LL across time and space indicate that short-term thermal acclimation keeps pace with long-term genetic adaptation for deciduous trees in Europe. Earlier leaf-out is the key force shaping the LL-temperature relationship. These results provide insights for predicting future vegetation dynamics under global warming.

Machine Learning Undercounts Reproductive Organs on Herbarium Specimens but Accurately Derives Their Quantitative Phenological Status: A Case Study of Streptanthus tortuosus.

Machine learning (ML) can accelerate the extraction of phenological data from herbarium specimens; however, no studies have assessed whether ML-derived phenological data can be used reliably to evaluate ecological patterns. In this study, 709 herbarium specimens representing a widespread annual herb, Streptanthus tortuosus, were scored both manually by human observers and by a mask R-CNN object detection model to (1) evaluate the concordance between ML and manually-derived phenological data and (2) determine whether ML-derived data can be used to reliably assess phenological patterns. The ML model generally underestimated the number of reproductive structures present on each specimen; however, when these counts were used to provide a quantitative estimate of the phenological stage of plants on a given sheet (i.e., the phenological index or PI), the ML and manually-derived PI's were highly concordant. Moreover, herbarium specimen age had no effect on the estimated PI of a given sheet. Finally, including ML-derived PIs as predictor variables in phenological models produced estimates of the phenological sensitivity of this species to climate, temporal shifts in flowering time, and the rate of phenological progression that are indistinguishable from those produced by models based on data provided by human observers. This study demonstrates that phenological data extracted using machine learning can be used reliably to estimate the phenological stage of herbarium specimens and to detect phenological patterns.

Seasonal windows of opportunity in milkweed-monarch interactions.

Many organisms experience seasonal windows of opportunity for growth and reproduction. These windows represent intervals in time when organisms experience improved prospects for advancing their life history objectives, constrained by the combined effects of seasonally variable biotic and abiotic conditions acting independently or in combination. Although seasonal windows of opportunity are likely to be widespread in nature, relatively few studies have conducted the repeated observations necessary to identify them or suggest the factors that structure them in time. Here, we present the results of three experimental studies conducted at different field sites in three different years in which we manipulated the phenology of monarch caterpillars (Danaus plexippus) throughout the growing season. The primary aims of these experiments were (1) to identify seasonal windows of opportunity for successful larval development on milkweed (Asclepias spp.), and (2) to suggest which factors are most likely to constrain these windows of opportunity in time. We found strong seasonal windows of opportunity in the developmental success of monarchs, with distinct periods of higher developmental prospects during each study year. We evaluated the role of seasonal variation in abiotic thermal stress, host plant density, host plant defensive traits, and natural enemy risk as potential factors that may limit seasonal windows of opportunity. By comparing the seasonal patterns of larval success and potential explanatory factors across all 3 yr, we find patterns that are consistent with seasonally variable abiotic conditions, host plant availability, host plant traits, and natural enemy risk factors. These results suggest the potential for seasonal variation in the factors that limit monarch larval development and population growth. More generally, this study also highlights the value of temporally explicit experimental studies that can identify and examine seasonal patterns in species interactions.

Phenological shifts in conifer species stressed by spruce budworm defoliation.

Synchrony between host budburst and insect emergence greatly influences the time window for insect development and survival. A few alterations of bud phenology have been reported under defoliation without clear consensus regarding the direction of effects, i.e., advance or delay. Here, we compared budburst phenology between conifers in defoliation and control treatments, and measured carbon allocation as a potential mechanistic explanation of changes in phenology. In a 2-year greenhouse experiment, saplings of balsam fir, black spruce and white spruce of two different provenances (north and south) were subjected to either control (no larvae) or natural defoliation treatment (larvae added) by spruce budworm. Bud and instar phenology, primary and secondary growth, defoliation and non-structural carbohydrates were studied during the growing season. No differences were observed in bud phenology during the first year of defoliation. After 1 year of defoliation, bud phenology advanced by 6-7 days in black spruce and balsam fir and by 3.5 days in white spruce compared with the control. Because of this earlier bud break, apical and shoot growth exceeded 50% of its final length before mature instar defoliation occurred, which decreased the overall level of damage. A sugar-mediated response, via earlier starch breakdown, and higher sugar availability to buds explains the advanced budburst in defoliated saplings. The advanced phenological response to defoliation was consistent across the conifer species and provenances except for one species × provenance combination. Allocation of carbon to buds and shoots growth at the expense of wood growth in the stem and reserve accumulation represents a shift in the physiological resources priorities to ensure tree survival. This advancement in bud phenology could be considered as a physiological response to defoliation based on carbohydrate needs for primary growth, rather than a resistance trait to spruce budworm.