Urbanization can affect the timing of plant reproduction (i.e. flowering and fruiting) and associated ecosystem processes. However, our knowledge of how plant phenology responds to urbanization and its associated environmental changes is limited. Herbaria represent an important, but underutilized source of data for investigating this question. We harnessed phenological data from herbarium specimens representing 200 plant species collected across 120 yr from the eastern US to investigate the spatiotemporal effects of urbanization on flowering and fruiting phenology and frost risk (i.e. time between the last frost date and flowering). Effects of urbanization on plant reproductive phenology varied significantly in direction and magnitude across species ranges. Increased urbanization led to earlier flowering in colder and wetter regions and delayed fruiting in regions with wetter spring conditions. Frost risk was elevated with increased urbanization in regions with colder and wetter spring conditions. Our study demonstrates that predictions of phenological change and its associated impacts must account for both climatic and human effects, which are context dependent and do not necessarily coincide. We must move beyond phenological models that only incorporate temperature variables and consider multiple environmental factors and their interactions when estimating plant phenology, especially at larger spatial and taxonomic scales.
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Summary Interactions between species can influence successful reproduction, resulting in reproductive character displacement, where the similarity of reproductive traits – such as flowering time – among close relatives growing together differ from when growing apart. Evidence for the overall prevalence and direction of this phenomenon, and its stability under environmental change, remains untested across large scales.
Using the power of crowdsourcing, we gathered phenological information from over 40 000 herbarium specimens, and investigated displacement in flowering time across 110 animal‐pollinated species in the eastern USA.
Overall, flowering time displacement is not common across large scales. However, displacement is generally greater among species pairs that flower close in time, regardless of direction. Furthermore, with climate change, the flowering times of closely related species are predicted, on average, to shift further apart by the mid‐21stcentury.
We demonstrate that the degree and direction of phenological displacement among co‐occurring closely related species pairs varies tremendously. However, future climate change may alter the differences in reproductive timing among many of these species pairs, which may have significant consequences for species interactions and gene flow. Our study provides one promising path towards understanding how the phenological landscape is structured and may respond to future environmental change.
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Abstract Species interactions drive ecosystem processes and are a major focus of global change research. Among the most consequential interactions expected to shift with climate change are those between insect herbivores and plants, both of which are highly sensitive to temperature. Insect herbivores and their host plants display varying levels of synchrony that could be disrupted or enhanced by climate change, yet empirical data on changes in synchrony are lacking. Using evidence of herbivory on herbarium specimens collected from the northeastern United States and France from 1900 to 2015, we provide evidence that plant species with temperature‐sensitive phenologies experience higher levels of insect damage in warmer years, while less temperature‐sensitive, co‐occurring species do not. While herbivory might be mediated by interactions between warming and phenology through multiple pathways, we suggest that warming might lengthen growing seasons for phenologically sensitive plant species, exposing their leaves to herbivores for longer periods of time in warm years. We propose that elevated herbivory in warm years may represent a previously underappreciated cost to phenological tracking of climate change over longer timescales.
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Free, publicly-accessible full text available May 1, 2024
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PREMISE Quantifying how closely related plant species differ in susceptibility to insect herbivory is important for our understanding of variation in plant-insect ecological interactions and evolutionary pressures on plant functional traits. However, empirically measuring in situ variation in herbivory over the entire geographic range where a plant-insect complex occurs is logistically difficult. Recently, new methods have been developed to use herbarium specimens to investigate patterns in plant-insect interactions across geographic areas, and during periods of accelerating anthropogenic change. Such investigations can provide insights into changes in herbivory intensity and phenology in plants that are of ecological and agricultural importance. METHODS Here, we analyze 274 pressed herbarium samples from all 14 species in the economically important plant genus Cucurbita (Cucurbitaceae) to investigate variation in herbivory damage. This collection is comprised of specimens of wild, undomesticated Cucurbita that were collected from across their native range in the Neotropics and subtropics, and Cucurbita cultivars that were collected from both within their native range and from locations where they have been introduced for agriculture in temperate Eastern North America. RESULTS We find that herbivory is common on individuals of all Cucurbita species collected from throughout their geographic ranges; however, estimates of herbivory varied considerably among individuals, with greater damage observed in specimens collected from unmanaged habitat. We also find evidence that mesophytic species accrue more insect damage than xerophytic species. CONCLUSIONS Our study demonstrates that herbarium specimens are a useful resource for understanding ecological interactions between domesticated crop plants and co-evolved insect herbivores.more » « less
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Reproductive character displacement has long been hypothesized to be a key determinant of speciation and co-existence in flowering plants. A central tenet of this hypothesis is that reproductive traits of close relatives growing in sympatry diverge more than they do where close relatives do not grow together. However, this idea remains untested across taxa and at large spatial scales. Here, we use data collected from tens of thousands of herbarium specimens to examine evidence for character displacement in flowering time for 91 closely-related pairs of animal-pollinated angiosperm species in the eastern USA. We see no evidence for overall phenological divergence in sympatry across regions, clades, or life histories. Rather our results indicate widespread convergence of flowering times in sympatry for species pairs that generally tend to flower close in time. We also find that climate change could alter the nature of these convergent flowering events by shifting them further apart in a majority species pair comparisons. Specifically, congeneric species in New England and the Atlantic Coastal Plain are projected to flower 2–4 days further apart, on average, by the mid-21st century as warming temperatures drive species-specific phenological shifts within genera. This may have significant consequences for species interactions and gene flow, especially if current sympatric convergence in flowering times has resulted from facilitative interactions between species.more » « less
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Phenology––the timing of life-history events––is a key trait for understanding responses of organisms to climate. The digitization and online mobilization of herbarium specimens is rapidly advancing our understanding of plant phenological response to climate and climatic change. The current common practice of manually harvesting data from individual specimens greatly restricts our ability to scale data collection to entire collections. Recent investigations have demonstrated that machine-learning models can facilitate data collection from herbarium specimens. However, present attempts have focused largely on simplistic binary coding of reproductive phenology (e.g., flowering or not). Here, we use crowd-sourced phenological data of numbers of buds, flowers, and fruits of more than 3000 specimens of six common wildflower species of the eastern United States (Anemone canadensis, A. hepatica, A. quinquefolia, Trillium erectum, T. grandiflorum, and T. undulatum} to train a model using Mask R-CNN to segment and count phenological features. A single global model was able to automate the binary coding of reproductive stage with greater than 90% accuracy. Segmenting and counting features were also successful, but accuracy varied with phenological stage and taxon. Counting buds was significantly more accurate than flowers or fruits. Moreover, botanical experts provided more reliable data than either crowd-sourcers or our Mask R-CNN model, highlighting the importance of high-quality human training data. Finally, we also demonstrated the transferability of our model to automated phenophase detection and counting of the three Trillium species, which have large and conspicuously-shaped reproductive organs. These results highlight the promise of our two-phase crowd-sourcing and machine-learning pipeline to segment and count reproductive features of herbarium specimens, providing high-quality data with which to study responses of plants to ongoing climatic change.more » « less
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Phenology is a key biological trait of an organism’s success and is one of the best indicators of its response to recent climate change. Plants are among the most well-studied organisms in this regard, but observational data bearing on this topic are largely restricted to woody species of the northern hemisphere, mostly from ca. the last three decades. Recent research has demonstrated that mobilized online herbarium specimens provide important, albeit mostly neglected, information on plant phenology. Here, we use the web tool CrowdCurio to crowdsource phenological data from more than 10,000 herbarium specimens representing 30 flowering plant species broadly distributed across the eastern United States. Our results, spanning 120 years and generated from over 2,000 crowdsourcers, clarify numerous aspects of plant phenology. First, they reveal that plant reproductive phenology is significantly advancing in response to warming, which is consistent with previous studies. Second, among those species with broad latitudinal ranges, populations from more southern latitudes are significantly more phenologically sensitive to temperature than those from northern populations. Last, contrary to some recent findings, plants in warmer, less variable climates may be much more dynamic, on average, in their phenological sensitivity. Our results are robust to a variety of confounding factors and span large phylogenetic distances and myriad life histories. These may represent more global trends in the latitudinal gradient of phenological response with myriad potential ecological and evolutionary consequences, and leads us to hypothesize that phenological sensitivity across species' ranges is driven by adaptation to local climates.more » « less
