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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.
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Herbarium records provide reliable phenology estimates in the understudied tropics
Plant phenology has been shifting dramatically in response to climate change, a shift that may have significant and widespread ecological consequences. Of particular concern are tropical biomes, which represent the most biodiverse and imperiled regions of the world. However, compared to temperate floras, we know little about phenological responses of tropical plants because long-term observational datasets from the tropics are sparse. Herbarium specimens have greatly increased our phenological knowledge in temperate regions, but similar data have been underutilized in the tropics and their suitability for this purpose has not been broadly validated. Here, we compare phenological estimates derived from field observational data (i.e., plot surveys) and herbarium specimens at various spatial and taxonomic scales to determine whether specimens can provide accurate estimations of reproductive timing and its spatial variation. Here we demonstrate that phenological estimates from field observations and herbarium specimens coincide well. Fewer than 5% of the species exhibited significant differences between flowering periods inferred from field observations versus specimens regardless of spatial aggregation. In contrast to studies based on field records, herbarium specimens sampled much larger geographic and climatic ranges, as has been documented previously for temperate plants, and effectively captured phenological responses across varied environments. Herbarium specimens are verified to be a vital resource for closing the gap in our phenological knowledge of tropical systems. Tropical plant reproductive phenology inferred from herbarium records are widely congruent with field observations, suggesting that they can (and should) be used to investigate phenological variation and their associated environmental cues more broadly across tropical biomes.
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- Award ID(s):
- 1754584
- PAR ID:
- 10354820
- Date Published:
- Journal Name:
- bioRxiv
- Volume:
- 2022.08.19.504574
- ISSN:
- 2692-8205
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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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null (Ed.)Abstract Background and Aims Fruiting remains under-represented in long-term phenology records, relative to leaf and flower phenology. Herbarium specimens and historical field notes can fill this gap, but selecting and synthesizing these records for modern-day comparison requires an understanding of whether different historical data sources contain similar information, and whether similar, but not equivalent, fruiting metrics are comparable with one another. Methods For 67 fleshy-fruited plant species, we compared observations of fruiting phenology made by Henry David Thoreau in Concord, Massachusetts (1850s), with phenology data gathered from herbarium specimens collected across New England (mid-1800s to 2000s). To identify whether fruiting times and the order of fruiting among species are similar between datasets, we compared dates of first, peak and last observed fruiting (recorded by Thoreau), and earliest, mean and latest specimen (collected from herbarium records), as well as fruiting durations. Key Results On average, earliest herbarium specimen dates were earlier than first fruiting dates observed by Thoreau; mean specimen dates were similar to Thoreau’s peak fruiting dates; latest specimen dates were later than Thoreau’s last fruiting dates; and durations of fruiting captured by herbarium specimens were longer than durations of fruiting observed by Thoreau. All metrics of fruiting phenology except duration were significantly, positively correlated within (r: 0.69–0.88) and between (r: 0.59–0.85) datasets. Conclusions Strong correlations in fruiting phenology between Thoreau’s observations and data from herbaria suggest that field and herbarium methods capture similar broad-scale phenological information, including relative fruiting times among plant species in New England. Differences in the timing of first, last and duration of fruiting suggest that historical datasets collected with different methods, scales and metrics may not be comparable when exact timing is important. Researchers should strongly consider matching methodology when selecting historical records of fruiting phenology for present-day comparisons.more » « less
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Premise of the StudyPhenological annotation models computed on large‐scale herbarium data sets were developed and tested in this study. MethodsHerbarium specimens represent a significant resource with which to study plant phenology. Nevertheless, phenological annotation of herbarium specimens is time‐consuming, requires substantial human investment, and is difficult to mobilize at large taxonomic scales. We created and evaluated new methods based on deep learning techniques to automate annotation of phenological stages and tested these methods on four herbarium data sets representing temperate, tropical, and equatorial American floras. ResultsDeep learning allowed correct detection of fertile material with an accuracy of 96.3%. Accuracy was slightly decreased for finer‐scale information (84.3% for flower and 80.5% for fruit detection). DiscussionThe method described has the potential to allow fine‐grained phenological annotation of herbarium specimens at large ecological scales. Deeper investigation regarding the taxonomic scalability of this approach is needed.more » « less
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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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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1101/2022.08.19.504574
