Phenological overlap of interacting species in a changing climate: an assessment of available approaches.
ABSTRACT: Concern regarding the biological effects of climate change has led to a recent surge in research to understand the consequences of phenological change for species interactions. This rapidly expanding research program is centered on three lines of inquiry: (1) how the phenological overlap of interacting species is changing, (2) why the phenological overlap of interacting species is changing, and (3) how the phenological overlap of interacting species will change under future climate scenarios. We synthesize the widely disparate approaches currently being used to investigate these questions: (1) interpretation of long-term phenological data, (2) field observations, (3) experimental manipulations, (4) simulations and nonmechanistic models, and (5) mechanistic models. We present a conceptual framework for selecting approaches that are best matched to the question of interest. We weigh the merits and limitations of each approach, survey the recent literature from diverse systems to quantify their use, and characterize the types of interactions being studied by each of them. We highlight the value of combining approaches and the importance of long-term data for establishing a baseline of phenological synchrony. Future work that scales up from pairwise species interactions to communities and ecosystems, emphasizing the use of predictive approaches, will be particularly valuable for reaching a broader understanding of the complex effects of climate change on the phenological overlap of interacting species. It will also be important to study a broader range of interactions: to date, most of the research on climate-induced phenological shifts has focused on terrestrial pairwise resource-consumer interactions, especially those between plants and insects.
Project description:Phenological responses to climate change (e.g., earlier leaf-out or egg hatch date) are now well documented and clearly linked to rising temperatures in recent decades. Such shifts in the phenologies of interacting species may lead to shifts in their synchrony, with cascading community and ecosystem consequences. To date, single-system studies have provided no clear picture, either finding synchrony shifts may be extremely prevalent [Mayor SJ, et al. (2017) Sci Rep 7:1902] or relatively uncommon [Iler AM, et al. (2013) Glob Chang Biol 19:2348-2359], suggesting that shifts toward asynchrony may be infrequent. A meta-analytic approach would provide insights into global trends and how they are linked to climate change. We compared phenological shifts among pairwise species interactions (e.g., predator-prey) using published long-term time-series data of phenological events from aquatic and terrestrial ecosystems across four continents since 1951 to determine whether recent climate change has led to overall shifts in synchrony. We show that the relative timing of key life cycle events of interacting species has changed significantly over the past 35 years. Further, by comparing the period before major climate change (pre-1980s) and after, we show that estimated changes in phenology and synchrony are greater in recent decades. However, there has been no consistent trend in the direction of these changes. Our findings show that there have been shifts in the timing of interacting species in recent decades; the next challenges are to improve our ability to predict the direction of change and understand the full consequences for communities and ecosystems.
Project description:Climate change has caused many ecological changes around the world. Altered phenology is among the most commonly observed effects of climate change, and the list of species interactions affected by altered phenology is growing. Although many studies on altered phenology focus on single species or on pairwise species interactions, most ecological communities are comprised of numerous, ecologically similar species within trophic groups. Using a 12-year butterfly monitoring citizen science data set, we aimed to assess the degree to which butterfly communities may be changing over time. Specifically, we wanted to assess the degree to which phenological sensitivities to temperature could affect temporal overlap among species within communities, independent of changes in abundance, species richness, and evenness. We found that warming winter temperatures may be associated with some butterfly species making use of the coldest months of the year to fly as adults, thus changing temporal co-occurrence with other butterfly species. Our results suggest that changing temperatures could cause immediate restructuring of communities without requiring changes in overall abundance or diversity. Such changes could have fitness consequences for individuals within trophic levels by altering competition for resources, as well as indirect effects mediated by species interactions across trophic levels.
Project description:In response to climate change, earlier phenological events have been reported for a large range of taxa such that phenological shifts are considered as one of the fingerprints of the effect of climate change on organisms. Evidence further suggests that changes in the timing of phenological events might decouple biotic interactions due to differential phenological adjustment among interacting species, ultimately leading to population declines. Nonetheless, few studies have investigated how climate-driven changes in the timing of phenological events influence population abundances. In this study, we investigated how two environmental variables known to influence the migration timing of freshwater fish (i.e. water discharge and temperature) directly or indirectly influenced abundances of 21 fish species using daily time series gathered at four sites located in France over a period spanning from 9 to 21 years. We found no evidence for long-term trends in migration timing or fish abundances over time. Using piecewise structural equation models, we demonstrate that inter-annual variations in abundances were driven by inter-annual variations in temperature through variations in migration timing. Overall, our results suggest that climate change may concomitantly influence different biological aspects (e.g. phenology, abundance) of fish species. We argue that considering different responses to climate change is paramount if we are to improve our understanding of how organisms and populations are influenced by climate change in order to set-up efficient conservation strategies.
Project description:Climate change is expected to alter biotic interactions, and may lead to temporal and spatial mismatches of interacting species. Although the importance of interactions for climate change risk assessments is increasingly acknowledged in observational and experimental studies, biotic interactions are still rarely incorporated in species distribution models. We assessed the potential impacts of climate change on the obligate interaction between Aeshna viridis and its egg-laying plant Stratiotes aloides in Europe, based on an ensemble modelling technique. We compared three different approaches for incorporating biotic interactions in distribution models: (1) We separately modelled each species based on climatic information, and intersected the future range overlap ('overlap approach'). (2) We modelled the potential future distribution of A. viridis with the projected occurrence probability of S. aloides as further predictor in addition to climate ('explanatory variable approach'). (3) We calibrated the model of A. viridis in the current range of S. aloides and multiplied the future occurrence probabilities of both species ('reference area approach'). Subsequently, all approaches were compared to a single species model of A. viridis without interactions. All approaches projected a range expansion for A. viridis. Model performance on test data and amount of range gain differed depending on the biotic interaction approach. All interaction approaches yielded lower range gains (up to 667% lower) than the model without interaction. Regarding the contribution of algorithm and approach to the overall uncertainty, the main part of explained variation stems from the modelling algorithm, and only a small part is attributed to the modelling approach. The comparison of the no-interaction model with the three interaction approaches emphasizes the importance of including obligate biotic interactions in projective species distribution modelling. We recommend the use of the 'reference area approach' as this method allows a separation of the effect of climate and occurrence of host plant.
Project description:Climate change-induced shifts in phenology have important demographic consequences, and are frequently used to assess species' sensitivity to climate change. Therefore, developing accurate phenological predictions is an important step in modeling species' responses to climate change. The ability of such phenological models to predict effects at larger spatial and temporal scales has rarely been assessed. It is also not clear whether the most frequently used phenological index, namely the average date of a phenological event across a population, adequately captures phenological shifts in the distribution of events across the season. We use the long-tailed tit Aegithalos caudatus (Fig. 1) as a case study to explore these issues. We use an intensive 17-year local study to model mean breeding date and test the capacity of this local model to predict phenology at larger spatial and temporal scales. We assess whether local models of breeding initiation, termination, and renesting reveal phenological shifts and responses to climate not detected by a standard phenological index, that is, population average lay date. These models take predation timing/intensity into account. The locally-derived model performs well at predicting phenology at the national scale over several decades, at both high and low temperatures. In the local model, a trend toward warmer Aprils is associated with a significant advance in termination dates, probably in response to phenological shifts in food supply. This results in a 33% reduction in breeding season length over 17 years - a substantial loss of reproductive opportunity that is not detected by the index of population average lay date. We show that standard phenological indices can fail to detect patterns indicative of negative climatic effects, potentially biasing assessments of species' vulnerability to climate change. More positively, we demonstrate the potential of detailed local studies for developing broader-scale predictive models of future phenological shifts.
Project description:Climate change may alter the timing of flowering and pollinator activity to differing degrees, resulting in phenological mismatches between mutualistic partners. Assessing the potential for such mismatches requires an understanding of the environmental factors that cue flowering and pollinator activity. Biological context is key to determining specific impacts of climate change, and therefore it is important to study mutualisms with pollinators of different nesting biologies. Our study focused on the phenology of two mutualists native to the coastal dunes of northwestern California: the silky beach pea (Lathyrus littoralis) and its main pollinator, the ground-nesting solitary silver bee (Habropoda miserabilis). We measured the current phenological overlap between the two species and took advantage of local fine-scale spatial variation in the timing of flowering and bee nesting activity to develop predictive models of flowering and flight period timing based on variation in soil temperature and moisture. Temperature best predicted both flowering and bee activity, although soil moisture influenced the timing as well. Comparison of linear regression slopes of phenology against temperature suggests that bee nesting time is more sensitive to differences in seasonal maximum temperatures, and may advance more rapidly than flowering with temperature increases. Although the current phenological overlap between the two species is high, this differential response to temperature could result in a decrease in overlap with climate warming. Our results highlight that nesting biology may be critical in determining impacts of climate change on pollination mutualisms, as ground-nesting bees may respond differently than other bee species. In addition, this work reveals the utility of studying bee species that nest in aggregations for understanding ground-nesting bee phenology.
Project description:Climate warming strongly influences reproductive phenology of plants in alpine and Arctic ecosystems. Here, we focus on phenological shifts caused by experimental warming in a typical alpine meadow on the Tibetan Plateau. Under soil water stress caused by warming, most plants in the alpine meadow advanced or delayed their reproductive events to be aligned with the timing of peak rainfall. As a result, warming significantly increased the temporal overlap among reproductive stages of early- and late-flowering species. In addition, we found that some species, for example the late-flowering species, were unable to produce flowers and fruits under warming with failed monsoon rains. The potentially warmer- and drier-growing seasons under climate change may similarly shift the phenological patterns and change species composition of these alpine systems.
Project description:Climate-induced changes in spatial and temporal occurrence of species, as well as species traits such as body size, each have the potential to decouple symbiotic relationships. Past work has focused primarily on direct interactions, particularly those between predators and prey and between plants and pollinators, but studies have rarely demonstrated significant fitness costs to the interacting, coevolving organisms. Here, we demonstrate that changing phenological synchrony in the latter part of the 20th century has different fitness outcomes for the actors within a Batesian mimicry complex, where predators learn to differentiate harmful "model" organisms (stinging Hymenoptera) from harmless "mimics" (hoverflies, Diptera: Syrphidae). We define the mimetic relationships between 2,352 pairs of stinging Hymenoptera and their Syrphidae mimics based on a large-scale citizen science project and demonstrate that there is no relationship between the phenological shifts of models and their mimics. Using computer game-based experiments, we confirm that the fitness of models, mimics, and predators differs among phenological scenarios, creating a phenologically antagonistic system. Finally, we show that climate change is increasing the proportion of mimetic interactions in which models occur first and reducing mimic-first and random patterns of occurrence, potentially leading to complex fitness costs and benefits across all three actors. Our results provide strong evidence for an overlooked example of fitness consequences from changing phenological synchrony.
Project description:The temporal overlap of phenological stages, phenological synchrony, crucially influences ecosystem functioning. For flowering, among-individual synchrony influences gene flow. For leaf-out, it affects interactions with herbivores and competing plants. If individuals differ in their reaction to the ongoing change in global climate, this should affect population-level synchrony. Here, we use climate-manipulation experiments, Pan-European long-term (>15 years) observations, and common garden monitoring data on up to 72 woody and herbaceous species to study the effects of increasing temperatures on the extent of leaf-out and flowering synchrony within populations. Warmer temperatures reduce in situ leaf-out and flowering synchrony by up to 55%, and experiments on European beech provide a mechanism for how individual differences in day-length and/or chilling sensitivity may explain this finding. The rapid loss of reproductive and vegetative synchrony in European plants predicts changes in their gene flow and trophic interactions, but community-wide consequences remain largely unknown. Editorial note:This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (see decision letter).
Project description:Changes in plant phenology associated with climate change have been observed globally. What is poorly known is whether and how phenological responses to climate warming will differ from year to year, season to season, habitat to habitat, or species to species. Here, we present 5 y of phenological responses to experimental warming for 10 subboreal tree species. Research took place in the open-air B4WarmED experiment in Minnesota. The design is a two habitat (understory and open) × three warming treatments (ambient, +1.7 °C, +3.4 °C) factorial at two sites. Phenology was measured twice weekly during the growing seasons of 2009 through 2013. We found significant interannual variation in the effect of warming and differences among species in response to warming that relate to geographic origin and plant functional group. Moreover, responses to experimental temperature variation were similar to responses to natural temperature variation. Warming advanced the date of budburst more in early compared to late springs, suggesting that to simulate interannual variability in climate sensitivity of phenology, models should employ process-based or continuous development approaches. Differences among species in timing of budburst were also greater in early compared to late springs. Our results suggest that climate change-which will make most springs relatively "early"-could lead to a future with more variable phenology among years and among species, with consequences including greater risk of inappropriately early leafing and altered interactions among species.