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Title: Machine Learning Using Digitized Herbarium Specimens to Advance Phenological Research
Abstract Machine learning (ML) has great potential to drive scientific discovery by harvesting data from images of herbarium specimens—preserved plant material curated in natural history collections—but ML techniques have only recently been applied to this rich resource. ML has particularly strong prospects for the study of plant phenological events such as growth and reproduction. As a major indicator of climate change, driver of ecological processes, and critical determinant of plant fitness, plant phenology is an important frontier for the application of ML techniques for science and society. In the present article, we describe a generalized, modular ML workflow for extracting phenological data from images of herbarium specimens, and we discuss the advantages, limitations, and potential future improvements of this workflow. Strategic research and investment in specimen-based ML methods, along with the aggregation of herbarium specimen data, may give rise to a better understanding of life on Earth.  more » « less
Award ID(s):
1754584 1802209 1902064 1902078
NSF-PAR ID:
10164955
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ;
Date Published:
Journal Name:
BioScience
ISSN:
0006-3568
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
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  1. 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. 
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  2. 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. 
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  3. Premise of the Study

    Phenological annotation models computed on large‐scale herbarium data sets were developed and tested in this study.

    Methods

    Herbarium 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.

    Results

    Deep 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).

    Discussion

    The 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.

     
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  4. Premise

    Herbarium specimens represent an outstanding source of material with which to study plant phenological changes in response to climate change. The fine‐scale phenological annotation of such specimens is nevertheless highly time consuming and requires substantial human investment and expertise, which are difficult to rapidly mobilize.

    Methods

    We trained and evaluated new deep learning models to automate the detection, segmentation, and classification of four reproductive structures ofStreptanthus tortuosus(flower buds, flowers, immature fruits, and mature fruits). We used a training data set of 21 digitized herbarium sheets for which the position and outlines of 1036 reproductive structures were annotated manually. We adjusted the hyperparameters of amask R‐CNN(regional convolutional neural network) to this specific task and evaluated the resulting trained models for their ability to count reproductive structures and estimate their size.

    Results

    The main outcome of our study is that the performance of detection and segmentation can vary significantly with: (i) the type of annotations used for training, (ii) the type of reproductive structures, and (iii) the size of the reproductive structures. In the case ofStreptanthus tortuosus, the method can provide quite accurate estimates (77.9% of cases) of the number of reproductive structures, which is better estimated for flowers than for immature fruits and buds. The size estimation results are also encouraging, showing a difference of only a few millimeters between the predicted and actual sizes of buds and flowers.

    Discussion

    This method has great potential for automating the analysis of reproductive structures in high‐resolution images of herbarium sheets. Deeper investigations regarding the taxonomic scalability of this approach and its potential improvement will be conducted in future work.

     
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  5. Abstract

    The widespread digitization of natural history collections, combined with novel tools and approaches is revolutionizing biodiversity science. The ‘extended specimen’ concept advocates a more holistic approach in which a specimen is framed as a diverse stream of interconnected data. Herbarium specimens that by their very nature capture multispecies relationships, such as certain parasites, fungi and lichens, hold great potential to provide a broader and more integrative view of the ecology and evolution of symbiotic interactions. This particularly applies to parasite–host associations, which owing to their interconnectedness are especially vulnerable to global environmental change.

    Here, we present an overview of how parasitic flowering plants is represented in herbarium collections. We then discuss the variety of data that can be gathered from parasitic plant specimens, and how they can be used to understand global change impacts at multiple scales. Finally, we review best practices for sampling parasitic plants in the field, and subsequently preparing and digitizing these specimens.

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    Parasitic plant specimens are primed to serve as ideal examples of extended specimen concept and help motivate the next generation of creative and impactful collection‐based science. Continued digitization efforts and improved curatorial practices will contribute to opening these specimens to a broader audience, allowing integrative research spanning multiple domains and offering novel opportunities for education.

     
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