Bayesian analysis of climate change impacts in phenology

The identification of changes in observational data relating to the climate change hypothesis remains a topic of paramount importance. In particular, scientifically sound and rigorous methods for detecting changes are urgently needed. In this paper, we develop a Bayesian approach to nonparametric function estimation. The method is applied to blossom time series of Prunus avium L., Galanthus nivalis L. and Tilia platyphyllos SCOP. The functional behavior of these series is represented by three different models: the constant model, the linear model and the one change point model. The one change point model turns out to be the preferred one in all three data sets with considerable discrimination of the other alternatives. In addition to the functional behavior, rates of change in terms of days per year were also calculated. We obtain also uncertainty margins for both function estimates and rates of change. Our results provide a quantitative representation of what was previously inferred from the same data by less involved methods.     

Flowering phenology change and climate warming in southwestern Ohio

Global surface temperature has increased markedly over the last 100 years. This increase has a variety of implications for human societies, and for ecological systems. One of the most obvious ways ecosystems are affected by global climate change is through alteration of organisms’ developmental timing (phenology). We used annual botanical surveys that documented the first flowering for an array of species from 1976 to 2003 to examine the potential implications of climate change for plant development. The overall trend for these species was a progressively earlier flowering time. The two earliest flowering taxa (Galanthus and Crocus) also exhibited the strongest shift in first flowering. We detected a significant trend in climate suggesting higher temperatures in winter and spring over the sampling interval and found a significant relationship between warming temperatures and first flowering time for some species. Although 60% of the species in our study flowered earlier over the sampling interval, the remaining species exhibited no statistically detectable change. This variation in response is ostensibly associated with among-species variation in the role of climate cues in plant development. Future work is needed to isolate specific climate cues, and to link plant phenology to the physiological processes that trigger plant development.     

Impact of climate change on plant phenology in Mediterranean ecosystems

Plant phenology is strongly controlled by climate and has consequently become one of the most reliable bioindicators of ongoing climate change. We used a dataset of more than 200 000 records for six phenological events of 29 perennial plant species monitored from 1943 to 2003 for a comprehensive assessment of plant phenological responses to climate change in the Mediterranean region. Temperature, precipitation and North Atlantic Oscillation (NAO) were studied together during a complete annual cycle before phenological events to determine their relative importance and potential seasonal carry‐over effects. Warm and dry springs under a positive phase of NAO advance flowering, leaf unfolding and fruiting dates and lengthen the growing season. Spatial variability of dates (range among sites) was also reduced during warm and dry years, especially for spring events. Climate during previous weeks to phenophases occurrence had the greatest impact on plants, although all events were also affected by climate conditions several months before. Immediate along with delayed climate effects suggest dual triggers in plant phenology. Climatic models accounted for more than 80% of variability in flowering and leaf unfolding dates, and in length of the growing season, but for lower proportions in fruiting and leaf falling. Most part of year‐to‐year changes in dates was accounted for temperature, while precipitation and NAO accounted for <10% of dates' variability. In the case of flowering, insect‐pollinated species were better modelled by climate than wind‐pollinated species. Differences in temporal responses of plant phenology to recent climate change are due to differences in the sensitivity to climate among events and species. Spring events are changing more than autumn events as they are more sensitive to climate and are also undergoing the greatest alterations of climate relative to other seasons. In conclusion, climate change has shifted plant phenology in the Mediterranean region.     

The effects of climate change on species composition,succession and phenology: a case study

Climate change and its role in altering biological interactions and the likelihood of invasion by introduced species in marine systems have received increased attention in recent years. It is difficult to forecast how climate change will influence community function or the probability of invasion as it alters multiple marine environmental parameters including rising water temperature, lower salinity and pH. In the present study, we correlate changes in environmental parameters to shifts in species composition in a subtidal community in Newcastle, NH through comparison of two, 3‐year periods separated by 23 years (1979–1981 and 2003–2005). We observed concurrent shifts in climate related factors and in groups of organisms that dominate the marine community when comparing 1979–1981 to 2003–2005. The 1979–1981 community was dominated by perennial species (mussels and barnacles). In contrast, the 2003–2005 community was dominated by annual native and invasive tunicates (sea‐squirts). We also observed a shift in the environmental factors that characterized both communities. Dissolved inorganic nitrogen and phosphate characterized the 1979–1981 community while sea surface temperature, pH, and chlorophyll a characterized the 2003–2005 community. Elongated warmer water temperatures, through the fall and early winter months of the 2000s, extended the growing season of native organisms and facilitated local dominance of invasive species. Additionally, beta‐diversity was greater between 2003–2005 than 1979–1981 and driven by larger numbers of annual species whose life‐history characteristics (e.g., timing and magnitude of recruitment, growth and mortality) are driven by environmental parameters, particularly temperature.     

Challenges in predicting climate change impacts on pome fruit phenology

Climate projection data were applied to two commonly used pome fruit flowering models to investigate potential differences in predicted full bloom timing. The two methods, fixed thermal time and sequential chill-growth, produced different results for seven apple and pear varieties at two Australian locations. The fixed thermal time model predicted incremental advancement of full bloom, while results were mixed from the sequential chill-growth model. To further investigate how the sequential chill-growth model reacts under climate perturbed conditions, four simulations were created to represent a wider range of species physiological requirements. These were applied to five Australian locations covering varied climates. Lengthening of the chill period and contraction of the growth period was common to most results. The relative dominance of the chill or growth component tended to predict whether full bloom advanced, remained similar or was delayed with climate warming. The simplistic structure of the fixed thermal time model and the exclusion of winter chill conditions in this method indicate it is unlikely to be suitable for projection analyses. The sequential chill-growth model includes greater complexity; however, reservations in using this model for impact analyses remain. The results demonstrate that appropriate representation of physiological processes is essential to adequately predict changes to full bloom under climate perturbed conditions with greater model development needed.     

Why climate change will invariably alter selection pressures on phenology

The seasonal timing of lifecycle events is closely linked to individual fitness and hence, maladaptation in phenological traits may impact population dynamics. However, few studies have analysed whether and why climate change will alter selection pressures and hence possibly induce maladaptation in phenology. To fill this gap, we here use a theoretical modelling approach. In our models, the phenologies of consumer and resource are (potentially) environmentally sensitive and depend on two different but correlated environmental variables. Fitness of the consumer depends on the phenological match with the resource. Because we explicitly model the dependence of the phenologies on environmental variables, we can test how differential (heterogeneous) versus equal (homogeneous) rates of change in the environmental variables affect selection on consumer phenology. As expected, under heterogeneous change, phenotypic plasticity is insufficient and thus selection on consumer phenology arises. However, even homogeneous change leads to directional selection on consumer phenology. This is because the consumer reaction norm has historically evolved to be flatter than the resource reaction norm, owing to time lags and imperfect cue reliability. Climate change will therefore lead to increased selection on consumer phenology across a broad range of situations.     

Environmental controls on the phenology of moths: predicting plasticity and constraint under climate change

Ecological systems have naturally high interannual variance in phenology. Component species have presumably evolved to maintain appropriate phenologies under historical climates, but cases of inappropriate phenology can be expected with climate change. Understanding controls on phenology permits predictions of ecological responses to climate change. We studied phenological control systems in Lepidoptera by analyzing flight times recorded at a network of sites in Finland. We evaluated the strength and form of controls from temperature and photoperiod, and tested for geographic variation within species. Temperature controls on phenology were evident in 51% of 112 study species and for a third of those thermal controls appear to be modified by photoperiodic cues. For 24% of the total, photoperiod by itself emerged as the most likely control system. Species with thermal control alone should be most immediately responsive in phenology to climate warming, but variably so depending upon the minimum temperature at which appreciable development occurs and the thermal responsiveness of development rate. Photoperiodic modification of thermal controls constrains phenotypic responses in phenologies to climate change, but can evolve to permit local adaptation. Our results suggest that climate change will alter the phenological structure of the Finnish Lepidoptera community in ways that are predictable with knowledge of the proximate physiological controls. Understanding how phenological controls in Lepidoptera compare to that of their host plants and enemies could permit general inferences regarding climatic effects on mid- to high-latitude ecosystems.     

Effects of recent climate change on phytoplankton phenology in a temperate lake

1. A number of long-term studies have shown that spring biological events have advanced in recent decades and that this is a response to climate change. In lentic systems, changes in phytoplankton phenology have been attributed to various directly climate-related processes including changes in the onset and duration of thermal stratification, earlier ice-break up and increased water temperature. Both indirect climatic drivers and non-climate drivers such as elevated grazing pressure and nutrient enrichment can also affect phenology.
2. This study investigated whether phenological trends in phytoplankton could be detected in a relatively short time series in a shallow, ice-free, polymictic lake with a high annual discharge and whether any such trends could be causally explained.
3. It was found that the centre of gravity of the spring chlorophyll a bloom advanced significantly by 1.6 days per year over a 15-year period. This was accompanied by a significant increase in water temperature of 0.12 °C per year which is high compared to published rates of change over longer time series. No direct effects of ice cover, stratification or water discharge rates could be linked to the advancement of the spring bloom. Instead, the shift in timing was attributed to an advance in the timing of the dominant spring diatom, Aulacoseira spp., instigated by a temperature-driven increase in replication rate leading to an earlier onset of silica (SiO₂) limitation.     

The spatial pattern of leaf phenology and its response to climate change in China

Leaf phenology has been shown to be one of the most important indicators of the effects of climate change on biological systems. Few such studies have, however, been published detailing the relationship between phenology and climate change in Asian contexts. With the aim of quantifying species’ phenological responsiveness to temperature and deepening understandings of spatial patterns of phenological and climate change in China, this study analyzes the first leaf date (FLD) and the leaf coloring date (LCD) from datasets of four woody plant species, Robinia pseudoacacia, Ulmus pumila, Salix babylonica, and Melia azedarach, collected from 1963 to 2009 at 47 Chinese Phenological Observation Network (CPON) stations spread across China (from 21° to 50° N). The results of this study show that changes in temperatures in the range of 39–43 days preceding the date of FLD of these plants affected annual variations in FLD, while annual variations in temperature in the range of 71–85 days preceding LCD of these plants affected the date of LCD. Average temperature sensitivity of FLD and LCD for these plants was ?3.93 to 3.30 days °C^?1 and 2.11 to 4.43 days °C^?1, respectively. Temperature sensitivity of FLD was found to be stronger at lower latitudes or altitude as well as in more continental climates, while the response of LCD showed no consistent pattern. Within the context of significant warming across China during the study period, FLD was found to have advanced by 5.44 days from 1960 to 2009; over the same period, LCD was found to have been delayed by 4.56 days. These findings indicate that the length of the growing season of the four plant species studied was extended by a total of 10.00 days from 1960 to 2009. They also indicate that phenological response to climate is highly heterogeneous spatially.     

The effects of climate change on the phenology of winter birds in Yokohama, Japan

Observations made largely from summer breeding sites in Europe and North America have been used to document the effects of climate change on many bird species. We extend these studies by examining 23 years of observations between 1986 and 2008 of six winter bird species made by citizens at a city park in Yokohama, Japan. Bird species arrive in autumn and spend the winter in the area, before departing in the late winter or spring. On average, birds species are arriving 9 days later than in the past and are departing on average 21 days earlier, meaning that the average duration of their stay in Yokohama is about 1 month shorter now than in the past. Patterns of changes over time varied among species, but departure dates changed for more species than did arrival dates. Dates of departure and arrival were sometimes correlated with monthly average temperatures—later arrivals and earlier departures were associated with warmer temperatures. In addition, interannual variation in arrival and departure dates were strongly correlated across species, suggesting that species were responding to the same or similar environmental cues. This study provides a clear demonstration of the value of using citizens to make observations that contribute to research in climate change biology.     

Shifts in phenology due to global climate change: the need for a yardstick

Climate change has led to shifts in phenology in many species distributed widely across taxonomic groups. It is, however, unclear how we should interpret these shifts without some sort of a yardstick: a measure that will reflect how much a species should be shifting to match the change in its environment caused by climate change. Here, we assume that the shift in the phenology of a species' food abundance is, by a first approximation, an appropriate yardstick. We review the few examples that are available, ranging from birds to marine plankton. In almost all of these examples, the phenology of the focal species shifts either too little (five out of 11) or too much (three out of 11) compared to the yardstick. Thus, many species are becoming mistimed due to climate change. We urge researchers with long-term datasets on phenology to link their data with those that may serve as a yardstick, because documentation of the incidence of climate change-induced mistiming is crucial in assessing the impact of global climate change on the natural world.     

The effects of climate change on the phenology of selected Estonian plant, bird and fish populations

This paper summarises the trends of 943 phenological time-series of plants, fishes and birds gathered from 1948 to 1999 in Estonia. More than 80% of the studied phenological phases have advanced during springtime, whereas changes are smaller during summer and autumn. Significant values of plant and bird phases have advanced 5–20 days, and fish phases have advanced 10–30 days in the spring period. Estonia’s average air temperature has become significantly warmer in spring, while at the same time a slight decrease in air temperature has been detected in autumn. The growing season has become significantly longer in the maritime climate area of Western Estonia. The investigated phenological and climate trends are related primarily to changes in the North Atlantic Oscillation Index (NAOI) during the winter months. Although the impact of the winter NAOI on the phases decreases towards summer, the trends of the investigated phases remain high. The trends of phenophases at the end of spring and the beginning of summer may be caused by the temperature inertia of the changing winter, changes in the radiation balance or the direct consequences of human impacts such as land use, heat islands or air pollution.     

Predicting adaptation of phenology in response to climate change, an insect herbivore example

Climate change has led to an advance in phenology in many species. Synchrony in phenology between different species within a food chain may be disrupted if an increase in temperature affects the phenology of the different species differently, as is the case in the winter moth egg hatch–oak bud burst system. Operophtera brumata (winter moth) egg hatch date has advanced more than Quercus robur (pedunculate oak) bud burst date over the past two decades. Disrupted synchrony will lead to selection, and a response in phenology to this selection may lead to species genetically adapting to their changing environment. However, a prerequisite for such genetic change is that there is sufficient genetic variation and severe enough fitness consequences. So far, examples of observed genetic change have been few. Using a half-sib design, we demonstrate here that O. brumata egg-hatching reaction norm is heritable, and that genetic variation exists. Fitness consequences of even a few days difference between egg hatch and tree bud opening are severe, as we experimentally determined. Estimates of genetic variation and of fitness were then combined with a climate scenario to predict the rate and the amount of change in the eggs' response to temperature. We predict a rapid response to selection, leading to a restoration of synchrony of egg hatch with Q. robur bud opening. This study shows that in this case there is a clear potential to adapt – rapidly – to environmental change. The current observed asynchrony is therefore not due to a lack of genetic variation and at present it is unclear what is constraining O. brumata to adapt. This kind of model may be particularly useful in gaining insight in the predicted amount and rate of change due to environmental changes, given a certain genetic variation and selection pressure.     

Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change

Anthropogenic climate change has already altered the timing of major life-history transitions, such as the initiation of reproduction. Both phenotypic plasticity and adaptive evolution can underlie rapid phenological shifts in response to climate change, but their relative contributions are poorly understood. Here, we combine a continuous 38 year field survey with quantitative genetic field experiments to assess adaptation in the context of climate change. We focused on Boechera stricta (Brassicaeae), a mustard native to the US Rocky Mountains. Flowering phenology advanced significantly from 1973 to 2011, and was strongly associated with warmer temperatures and earlier snowmelt dates. Strong directional selection favoured earlier flowering in contemporary environments (2010-2011). Climate change could drive this directional selection, and promote even earlier flowering as temperatures continue to increase. Our quantitative genetic analyses predict a response to selection of 0.2 to 0.5 days acceleration in flowering per generation, which could account for more than 20 per cent of the phenological change observed in the long-term dataset. However, the strength of directional selection and the predicted evolutionary response are likely much greater now than even 30 years ago because of rapidly changing climatic conditions. We predict that adaptation will likely be necessary for long-term in situ persistence in the context of climate change.     

Investigating the impact of climate change on crop phenological events in Europe with a phenology model

Predicting regional and global carbon and water dynamics requires a realistic representation of vegetation phenology. Vegetation models including cropland models exist (e.g. LPJmL, Daycent, SIBcrop, ORCHIDEE-STICS, PIXGRO) but they have various limitations in predicting cropland phenological events and their responses to climate change. Here, we investigate how leaf onset and offset days of major European croplands responded to changes in climate from 1971 to 2000 using a newly developed phenological model, which solely relies on climate data. Net ecosystem exchange (NEE) data measured with eddy covariance technique at seven sites in Europe were used to adjust model parameters for wheat, barley, and rapeseed. Observational data from the International Phenology Gardens were used to corroborate modeled phenological responses to changes in climate. Enhanced vegetation index (EVI) and a crop calendar were explored as alternative predictors of leaf onset and harvest days, respectively, over a large spatial scale. In each spatial model simulation, we assumed that all European croplands were covered by only one crop type. Given this assumption, the model estimated that the leaf onset days for wheat, barley, and rapeseed in Germany advanced by 1.6, 3.4, and 3.4 days per decade, respectively, during 1961–2000. The majority of European croplands (71.4%) had an advanced mean leaf onset day for wheat, barley, and rapeseed (7.0% significant), whereas 28.6% of European croplands had a delayed leaf onset day (0.9% significant) during 1971–2000. The trend of advanced onset days estimated by the model is similar to observations from the International Phenology Gardens in Europe. The developed phenological model can be integrated into a large-scale ecosystem model to simulate the dynamics of phenological events at different temporal and spatial scales. Crop calendars and enhanced vegetation index have substantial uncertainties in predicting phenological events of croplands. Caution should be exercised when using these data.     

Spatiotemporal variation in avian migration phenology: citizen science reveals effects of climate change

A growing number of studies have documented shifts in avian migratory phenology in response to climate change, and yet there is a large amount of unexplained variation in the magnitude of those responses across species and geographic regions. We use a database of citizen science bird observations to explore spatiotemporal variation in mean arrival dates across an unprecedented geographic extent for 18 common species in North America over the past decade, relating arrival dates to mean minimum spring temperature. Across all species and geographic locations, species shifted arrival dates 0.8 days earlier for every °C of warming of spring temperature, but it was common for some species in some locations to shift as much as 3-6 days earlier per °C. Species that advanced arrival dates the earliest in response to warming were those that migrate more slowly, short distance migrants, and species with broader climatic niches. These three variables explained 63% of the interspecific variation in phenological response. We also identify a latitudinal gradient in the average strength of phenological response, with species shifting arrival earlier at southern latitudes than northern latitudes for the same degree of warming. This observation is consistent with the idea that species must be more phenologically sensitive in less seasonal environments to maintain the same degree of precision in phenological timing.     

Influence of climate change on the abundance, distribution and phenology of woodland bird species in temperate regions

There is now overwhelming evidence that an increase in the concentration of greenhouse gases in the Earth's atmosphere has caused global temperatures to increase by 0.6 °C since 1900 and further increases of between 1.4 and 5.8 °C are predicted over the next century. Changes in climatic conditions have already influenced the demography, phenology and distribution of a wide range of plant and animal taxa. This review focuses on the impacts, both observed and potential, of climate change on birds breeding in temperate woodlands of the Western Palaearctic, a significant proportion of which are currently declining. Changes in ambient temperatures and patterns of precipitation may have direct and indirect effects on the survival rates and productivity of bird species, thus influencing population sizes. For some species or populations, the timing of events such as egg-laying and return from the wintering grounds is also changing in relation to shifts in the peak of food availability during the breeding season. The degree to which different individuals are able to track these temporal changes will have a significant bearing on population sizes and distributions in the future. Unless active management steps are taken, the relatively low dispersal rates of tree species may lead to a decrease in the total area of some woodland habitat types as losses at the southern edge of the range are likely to occur much more quickly than expansion at the northern edge. In addition, the dispersal rates of many woodland birds are themselves low, which could affect their ability to move to new habitat patches if currently occupied areas become unsuitable. Thus, woodland birds may be particularly susceptible to the impacts of climate change.