The unrealized potential of herbaria for global change biology

Abstract

Plant and fungal specimens in herbaria are becoming primary resources for investigating how plant phenology and geographic distributions shift with climate change, greatly expanding inferences across spatial, temporal, and phylogenetic dimensions. However, these specimens contain a wealth of additional data, including nutrients, defensive compounds, herbivore damage, disease lesions, and signatures of physiological processes, that capture ecological and evolutionary responses to the Anthropocene but which are less frequently utilized. Here, we outline the diversity of herbarium data, global change topics to which they have been applied, and new hypotheses they could inform. We find that herbarium data have been used extensively to study impacts of climate change and invasive species, but that such data are less commonly used to address other drivers of biodiversity loss, including habitat conversion, pollution, and overexploitation. In addition, we note that fungal specimens are under‐explored relative to vascular plants. To facilitate broader application of plant and fungal specimens in global change research, we consider the limitations of these data and modern sampling and statistical tools that may be applied to surmount challenges they present. Using a case study of insect herbivory, we illustrate how novel herbarium data may be employed to test hypotheses for which few data exist. With the goal of positioning herbaria as hubs for global change research, we suggest future research directions and curation priorities.

Herbarium specimens reveal increasing herbivory over the past century

“…We differentiated between damage by herbivores within herbaria and damage by herbivores on living specimens by the morphology of the damage. We found in this analysis and in a previous study (Meineke et al, ) that live plants generally form toughened, necrotic wounds around herbivore damage, but this is not present on specimens damaged indoors postcollection. For examples of outdoor damage to live plants (the type of damage of interest in this study) and indoor insect damage to specimens after collection, see Figure .…”

“…Field warming experiments are also typically short‐term and often address effects on herbivores rather than herbivory (but for one exception, see Jamieson, Schwartzberg, Raffa, Reich, & Lindroth, ). We suggest that data from herbarium specimens may provide opportunities to assess herbivory across unprecedented temporal, spatial, and phylogenetic scales (for a more detailed discussion of herbarium data for studying global change, see Meineke et al, ). In addition, equivalent data from herbarium specimens on plant–pollinator interactions (e.g., from pollen preserved in specimens; Pauw & Hawkins, ) and plant–pathogen interactions (e.g., from pathogen DNA or morphology; Antonovics, Hood, Thrall, Abrams, & Duthie, ) may be used to further tailor land management strategies to changing environmental conditions.…”

“…We scored herbivory by overlaying a grid of 5 cm by 5 cm cells, and scoring presence (1) or absence (0) of damage in five randomly selected grid cells, ensuring that selected cells had at least one‐fourth leaf cover (Meineke, Davis, & Davies, ). We focused on “chewing”—leaf removal by herbivores with mandibles, likely including Lepidoptera (butterflies and moths), Coleoptera (beetles), and Orthoptera (grasshoppers and their relatives)—because it was the most common type of herbivory on specimens and is the subject of most ecological studies on herbivory (Turcotte et al, ).…”

Using herbaria to study global environmental change

“…Even though herbaria were used as early as in the 1960s to study global change (e.g. Ruhling & Tyler, , ), and are in the process of being made available online via digitization (> 46 700 000 specimens in the Integrated Digitized Biocollections portal alone; as of 18 July 2018 https://www.idigbio.org/portal/ (search terms: type of record – PreservedSpecimen, kingdom – Plantae)), the community has not fully adopted herbaria as valuable ‘time machines’ to the past (Lavoie, ; Meineke et al ., ). Especially with the advent of high‐throughput methods and recent technical developments in image analysis, the value of these collections is now more apparent than ever (Munson & Long, ).…”

Toward a large‐scale and deep phenological stage annotation of herbarium specimens: Case studies from temperate, tropical, and equatorial floras

“…These plant specimens provide crucial data for the study of plant diversity, ecology, evolution, genetics, and biodiversity, to name only a few (Graham et al., ). When herbarium specimens are “digitized”—converted into a digital format by imaging and transcription of label data—they have even greater potential for answering major research questions related to the recent impact of humanity on biodiversity (Davis et al., ; Soltis, ; James et al., ; Meineke et al., ; Soltis et al., ). These millions of herbarium records have accumulated a valuable heritage and knowledge of plants over centuries, across all continents.…”