Abstract

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 practice of manually harvesting data from individual specimens, however, greatly restricts our ability to scale-up data collection. Recent investigations have demonstrated that machine-learning approaches can facilitate this effort. However, present attempts have focused largely on simplistic binary coding of reproductive phenology (e.g., presence/absence of flowers). Here, we use crowd-sourced phenological data of buds, flowers, and fruits from >3,000 specimens of six common wildflower species of the eastern United States (Anemone canadensis L., A. hepatica L., A. quinquefolia L., Trillium erectum L., T. grandiflorum (Michx.) Salisb., and T. undulatum Wild.) to train models using Mask R-CNN to segment and count phenological features. A single global model was able to automate the binary coding of each of the three reproductive stages with >87% accuracy. We also successfully estimated the relative abundance of each reproductive structure on a specimen with ≥90% accuracy. Precise counting of features was also successful, but accuracy varied with phenological stage and taxon. Specifically, counting flowers was significantly less accurate than buds or fruits likely due to their morphological variability on pressed specimens. Moreover, our Mask R-CNN model provided more reliable data than non-expert crowd-sourcers but not botanical experts, 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, thus providing high-quality data with which to investigate plant responses to ongoing climatic change.

Highlights

  • Climate change is a potent selective force that is shifting the geographic ranges of genotypes, altering population dynamics of individual species, and reorganizing entire assemblages in all environments

  • The Mean Absolute Error (MAE) was quite low for all types of reproductive structures, but this is due in large part to the fact that the median number of structures per phase and specimen is low

  • Recent efforts by Goëau et al (2020) to segment and count reproductive structures used training data collected by botanical experts from 21 herbarium specimens of a single species (S. tortuosus)

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Summary

Introduction

Climate change is a potent selective force that is shifting the geographic ranges of genotypes, altering population dynamics of individual species, and reorganizing entire assemblages in all environments. A key functional trait in this regard is phenology: the timing of life-history events, such as the onset of flowering or migration. The use of museum specimens has invigorated and enriched the investigation of phenological responses to climatic change, and is one of several research directions that has brought a renewed sense of purpose and timeliness to natural history collections (Davis et al, 2015; Willis et al, 2017; Meineke et al, 2018; Meineke et al, 2019; Hedrick et al, 2020). Herbarium specimens provide the only means of assessing phenological responses to climatic changes occurring over decades to centuries (Davis et al, 2015). A great challenge in using these specimens is accessing and rapidly assessing phenological state(s) of the world’s estimated 393 million herbarium specimens (Thiers, 2017; Sweeney et al, 2018)

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