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Editorial ARTICLE

Front. Plant Sci., 21 August 2020 | https://doi.org/10.3389/fpls.2020.01319

Editorial: Integrative and Translational Uses of Herbarium Collections Across Time, Space, and Species

  • 1Science and Conservation, National Tropical Botanical Garden, Kalaheo, HI, United States
  • 2Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark
  • 3Comparative Plant & Fungal Biology, Royal Botanic Gardens, Kew, Surrey, United Kingdom
  • 4Department of Life Sciences, The Natural History Museum, London, United Kingdom

This Research Topic is dedicated to the legacy of Vicki Funk [1947-2019], who was a Senior Research Botanist and Curator at the Smithsonian’s National Museum for 38 years, and a strong advocate for collections-based research. In 2004, Vicki compiled an inspirational list of uses of herbaria entitled ‘100 Uses for an Herbarium (Well at Least 72)’ (Funk, 2004), a study motivated by her appreciation of the potential for herbaria to make a unique contribution to a remarkable and growing array of research questions, at a time when the long-term survival of many such collections was under threat. The intervening decade and a half has seen that list of uses increase with new and unexpected techniques for the analysis of herbarium specimens and of the data derived from them.

Herbarium collections provide a unique record of our global biodiversity and natural history amassed over centuries. According to Index Herbariorum (Thiers, 2020), a global database of herbaria, as of December 2019, there are 3324 active herbaria in the world that collectively are estimated to hold nearly 400 million specimens. They offer a verifiable source of specimens for a plethora of research questions from taxonomy to evolution and change through time. They are being used to help tackle global societal challenges, and their value is currently increasingly realized and explored (Funk, 2002; Funk, 2004; Bebber et al., 2010; Funk, 2018; James et al., 2018; Meineke et al., 2018). Such impact will deepen as herbarium collections become more accessible both in digital and physical forms, and stories of the specimens and collectors are brought to light. Indeed, current global efforts to digitize herbarium collections are continuously increasing the number of available images and data through portals such as JSTOR Global Plants (www.plants.jstor.org), Global Biodiversity Information Facility (www.GBIF.org), and iDigBio (Integrated Digitized Biocollections; www.idigbio.org) (Soltis, 2017).

As scientists based at three of the world’s oldest and largest herbaria: the Royal Botanic Gardens Kew (K; founded 1852; 8,125,000 specimens), The Natural History Museum, London (BM; founded 1753; 5,200,000 specimens), The Natural History Museum of Denmark (C; founded 1759; 2,900,000 specimens), and one smaller and younger herbarium at the National Tropical Botanical Garden, USA (PTBG; founded 1971; 88,870 specimens), we encourage the continued use and exploration of the unique heritage and resources held in the world’s herbaria.

This Research Topic aims to synthesize and inspire the frontier of integrative and translational research using herbarium collections to highlight their unharvested potential for addressing outstanding research questions and societal challenges. The articles published in this Research Topic provide a selection of examples and new approaches illustrating trends and opportunities in this expanding field.

Though an inherently biased sample of biodiversity through time — shaped by historical and contemporary collecting practices and by colonialism and trade — herbarium specimens provide a verifiable record that a species occurred at a particular place at a particular time, and they represent several hundred years of collection history across the globe (López and Sassone; Romeiras et al.). Their imperfections extend to problems with erroneous identifications and with biased digitization efforts (e.g. Smith and Blagoderov, 2012), but careful assessment of data quality significantly improves their value (Goodwin et al., 2015; Maldonado et al., 2015), as do efforts to evaluate collection history and association with additional data sources (Allasi Canales et al., 2020; López and Sassone; Romeiras et al.; Stefanaki et al., 2019).

These challenges notwithstanding, herbaria provide a unique record of changes in distributions, of extinction and of habitats that have now disappeared. Specimens in herbaria provide readily available information and research possibilities extending far beyond the use of contemporary samples (Greve et al., 2016; Silva et al., 2017; Cardoso et al., 2018) and, indeed, far beyond the scope of what their original collectors may ever have envisaged (Heberling and Isaac, 2017; Heberling et al., 2019).

Herbaria present a time window into the past allowing exploration of changes in composition of floras (Calinger, 2015), of distribution of invasive weeds or threatened species (Stadler et al., 2002; Rivers et al., 2011; Hardion et al., 2014; Martin et al., 2016), changes in flowering times (Davis et al., 2015; Willis et al., 2017), leaf-out times (Everill et al., 2014) or of stomatal densities through time (Large et al., 2017) in response to environmental change, and they can be used to model predictions of future trends (James et al., 2018). Increasingly, they are being used to investigate not just the plant itself but other, associated organisms, in studies of trophic interactions, to infer relationships with associated insects including pollinators and herbivores and with microorganisms including those causing diseases (Martin et al., 2013; Yoshida et al., 2014; Meineke and Davies, 2018; Vega et al.).

Destructive sampling of herbarium samples must always be done with due care and for good scientific reason, but small amounts of material can now be used for a diversity of studies including exploring the viability of seeds from old herbarium specimens for conservation purposes (Godefroid et al., 2011; Porteous et al.; Wolkis and Deans, 2019). As the technical difficulties of extracting high quality DNA from historical materials are being overcome (Wales et al., 2014; Bieker and Martin, 2018) and new high-throughput methods are being developed including a customized Angiosperms353 probe set (Brewer et al.; Johnson et al., 2019), herbarium samples are increasingly being used in genomic studies—often termed Museomics—at all scales, from populations to phylogenies (Kuzmina et al., 2017; Bieker and Martin, 2018; Malakasi et al.) as well as to studies of genome duplications (Viruel et al.), domestication history (Kistler et al., 2018; Ramos-Madrigal et al., 2019), and plant pathogens (Yoshida et al., 2014). Herbarium materials can be a resource of chemical data for chemotaxonomy (Cook et al., 2009; Jafari Foutami et al., 2018; Allasi Canales et al., 2020), chemical ecology (Zangerl and Berenbaum, 2005), environmental bio-indicators (Foan et al., 2010; Monforte et al., 2015; Martinez-Swatson et al.) as well as drug discovery and authentication (Saslis-Lagoudakis et al., 2015; Rønsted et al., 2017).

Concluding Remarks

Herbaria are a unique resource for understanding global biodiversity and for addressing societal challenges. Their traditional use for taxonomy—for documenting and describing biodiversity – is as important today as it has ever been but that function is being supplemented by an increasing array of questions that herbaria are being used to address. We hope the articles in this Research Topic will inspire new integrative and translational uses of herbarium collections as well as highlight the need for continuous preservation, curation, and expansion of the collections, accompanied by detailed collecting data.

Author Contributions

NR drafted the editorial with contributions from OG and MC. The authors all contributed to the Research Topic assembly and editing.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

We thank all authors who have contributed to this special Topic and all reviewers for their efforts to ensure the high quality of the contributed papers.

References

Allasi Canales, N., Gress Hansen, T. N., Cornett, C., Walker, K., Driver, F., Antonelli, A., et al. (2020). Historical chemical annotations of Cinchona bark collections are comparable to results from current day high-pressure liquid chromatography technologies. J. Ethnopharmacol. 249, 112375. doi: 10.1016/j.jep.2019.112375

PubMed Abstract | CrossRef Full Text | Google Scholar

Bebber, D. P., Carine, M. A., Wood, J. R., Wortley, A. H., Harris, D. J., Prance, G. T., et al. (2010). Herbaria are a major frontier for species discovery. Proc. Natl. Acad. Sci. U. S. A. 107, 22169–22171. doi: 10.1073/pnas.1011841108

PubMed Abstract | CrossRef Full Text | Google Scholar

Bieker, V. C., Martin, M. D. (2018). Implications and future prospects for evolutionary analyses of DNA in historical herbarium collections. Bot Lett. 3, (3–4), 409–418. doi: 10.1080/23818107.2018.1458651

CrossRef Full Text | Google Scholar

Calinger, K. M. (2015). A functional group analysis of change in the abundance and distribution of 207 plant species across 115 years in north-central North America. Biodivers. Conserv. 24, 2439–2457. doi: 10.1007/s10531-015-0936-2

CrossRef Full Text | Google Scholar

Cardoso, D., Särkinen, T., Alexander, S., Amorim, A. M., Bittrich, V., Celis, M., et al. (2018). Amazon plant diversity revealed by a taxonomically verified species list. Proc. Natl. Acad. Sci. U. S. A. 114, 10695–10700. doi: 10.1073/pnas.1706756114

CrossRef Full Text | Google Scholar

Cook, D., Gardner, D. R., Pfister, J. A., Welch, K. D., Green, B. T, Lee, S. T. (2009). The biogeographical distribution of Duncecap Larkspur (Delphinium occidentale) chemotypes and their potential toxicity. J. Chem. Ecol. 35, 643–652. doi: 10.1007/s10886-009-9637-1

PubMed Abstract | CrossRef Full Text | Google Scholar

Davis, C. C., Willis, C. G., Connolly, B., Kelly, C., Ellison, A. (2015). Herbarium records are reliable sources of phenological change driven by climate and provide novel insights into species’ phenological cueing mechanisms. Am. J. Bot. 102, 1599–1609. doi: 10.3732/ajb.1500237

PubMed Abstract | CrossRef Full Text | Google Scholar

Everill, P. H., Primack, R. B., Ellwood, E. R., Melaas, E. K. (2014). Determining past leaf-out times of New England’s deciduous forests from herbarium specimens. Am. J. Bot. 101, 1293–1300. doi: 10.3732/ajb.1400045

PubMed Abstract | CrossRef Full Text | Google Scholar

Foan, L., Sablayrolles, C., Elustondo, D., Lasheras, E., González, L., Ederra, A., et al. (2010). Reconstructing historical trends of polycyclic aromatic hydrocarbon deposition in a remote area of Spain using herbarium moss material. Atmos. Environ. 44, 3207–3214. doi: 10.1016/j.atmosenv.2010.05.019

CrossRef Full Text | Google Scholar

Funk, V. A. (2002). The Importance of Herbaria. Plant Sci. Bull. 49, 94–95.

Google Scholar

Funk, V. A. (2004). 100 Uses for an Herbarium (Well at Least 72). ASPT Newslett. 17, 17–19.

Google Scholar

Funk, V. A. (2018). Collections-based science in the 21st Century. J. Syst. Evol. 56, 175–193. doi: 10.1111/jse.12315

CrossRef Full Text | Google Scholar

Godefroid, S., Van der Vyver, A., Stoffelen, P., Robbrecht, E., Vanderborght, T. (2011). Testing the viability of seeds from old herbarium specimens for conservation purposes. Taxon 60, 565–569. doi: 10.1002/tax.602022

CrossRef Full Text | Google Scholar

Goodwin, Z. A., Harris, D. J., Filer, D., Wood, J. R., Scotland, R. W. (2015). Widespread mistaken identity in tropical plant collections. Curr. Biol. 25, R1066–R1067. doi: 10.1016/j.cub.2015.10.002

PubMed Abstract | CrossRef Full Text | Google Scholar

Greve, M., Lykke, A. M., Fagg, C. W., Gereau, R. E., Lewis, G. P., Marchant, R., et al. (2016). Realising the potential of herbarium records for conservation biology. South Afr. J. Bot. 105, 317–323. doi: 10.1016/j.sajb.2016.03.017

CrossRef Full Text | Google Scholar

Hardion, L., Verlaque, R., Saltonstall, K., Leriche, A., Vila, B. (2014). Origin of the invasive Arundo donax (Poaceae): a trans-Asian expedition in herbaria. Ann. Bot. 114, 455–462. doi: 10.1093/aob/mcu143

PubMed Abstract | CrossRef Full Text | Google Scholar

Heberling, J. M., Isaac, B. L. (2017). Herbarium specimens as exaptations: New uses for old collections. Am. J. Bot. 104, 963–965. doi: 10.3732/ajb.1700125

PubMed Abstract | CrossRef Full Text | Google Scholar

Heberling, M., Prather, L. A., Tonsor, S. (2019). The changing uses of herbarium data in an era of global change: An overview using automated content analysis. BioScience 69, 812–822. doi: 10.1093/biosci/biz094

CrossRef Full Text | Google Scholar

Jafari Foutami, I., Mariager, T., Rinnan, R., Barnes, C. J., Rønsted, N. (2018). Hundred fifty years of herbarium collections provide a reliable resource of volatile terpenoid profiles showing strong species effect in four medicinal species of Salvia across the Mediterranean. Front. Plant Sci. 18 (9), 1877. doi: 10.3389/fpls.2018.01877

CrossRef Full Text | Google Scholar

James, S. A., Soltis, P. S., Belbin, L., Chapman, A. D., Nelson, G., Paul, D. L., et al. (2018). Herbarium data: global biodiversity and societal botanical needs for novel research. Appl. Plant Sci. 6, e1024. doi: 10.1002/aps3.1024

PubMed Abstract | CrossRef Full Text | Google Scholar

Johnson, M. G., Pokorny, L., Dodsworth, S., Botigué, L. R., Cowan, R. S., Devault, A., et al. (2019). Universal probe set for targeted sequencing of 353 nuclear genes from any flowering plant designed using k-medoids clustering. Syst. Biol. 68, 594–606. doi: 10.1093/sysbio/syy086

PubMed Abstract | CrossRef Full Text | Google Scholar

Kistler, L., Yoshi Maezumi, S., de Souza, J. G., Przelomska, N. A. S., Malaquias Costa, F., Smith, O., et al. (2018). Multiproxy evidence highlights a complex evolutionary legacy of maize in South America. Science 362, 1309–1313. doi: 10.1126/science.aav0207

PubMed Abstract | CrossRef Full Text | Google Scholar

Kuzmina, M. L., Braukmann, T. W. A., Fazekas, A. J., Graham, S. W., Dewaard, S. L., Rodrigues, A., et al. (2017). Using herbarium-derived DNAs to assemble a large-scale DNA barcode library for the vascular plants of Canada. Appl. Plant Sci. 5, 1700079. doi: 10.3732/apps.1700079

CrossRef Full Text | Google Scholar

Large, M. F., Nessia, H. R., Cameron, E. K., Blanchon, D. J. (2017). Changes in Stomatal Density over Time, (1769–2015) in the New Zealand Endemic Tree Corynocarpus laevigatus J. R. Forst. & G. Forst. (Corynocarpaceae). Pac. Sci. 71 (3), 319–328. doi: 10.2984/71.3.6

CrossRef Full Text | Google Scholar

Lavoie, C. (2012). Biological collections in an ever changing world: Herbaria as tools for biogeographical and environmental studies. Perspect. Plant Ecol. Evol. Syst. 15, 68–76. doi: 10.1016/j.ppees.2012.10.002

CrossRef Full Text | Google Scholar

Maldonado, C., Molina, C., II, Zizka, A., Persson, C., Taylor, C. M., Albán, J., et al. (2015). Species diversity and distribution in the era of Big Data. Glob. Ecol. Biogeogr. 24, 973–984. doi: 10.1111/geb.12326

PubMed Abstract | CrossRef Full Text | Google Scholar

Martin, M., Cappellini, E., Samaniego, J., Zepeda, M. L., Campos, P. F., Seguin-Orlando, A., et al. (2013). Reconstructing genome evolution in historic samples of the Irish potato famine pathogen. Nat. Commun. 4, 2172. doi: 10.1038/ncomms3172

PubMed Abstract | CrossRef Full Text | Google Scholar

Martin, M. D., Olsen, M. T., Samaniego, J., Zimmer, E. A., Gilbert, M. T. P. (2016). The population genomic basis of geographic differentiation in North American common ragweed (Ambrosia artemisiifolia L.). Ecol. Evol. 6, 3760–3771. doi: 10.1002/ece3.2143

PubMed Abstract | CrossRef Full Text | Google Scholar

Meineke, E. K., Davies, T. J. (2018). Museum specimens provide novel insights into changing plant-herbivore interactions. Philos. Trans. R. Soc Lond. B. Biol. Sci. 374 (1763), 20170393. doi: 10.1098/rstb.2017.0393

PubMed Abstract | CrossRef Full Text | Google Scholar

Meineke, E. K., Davies, T. J., Daru, B. H., Davis, C. C. (2018). Biological collections for understanding biodiversity in the Anthropocene. Philos. Trans. R. Soc Lond. B. Biol. Sci. 374, 20170386. doi: 10.1098/rstb.2017.0386

PubMed Abstract | CrossRef Full Text | Google Scholar

Monforte, L., Tomás-Las-Heras, R., Del-Castillo-Alonso, M.Á., Martínez-Abaigar, J., Núñez-Olivera, E. (2015). Spatial variability of ultraviolet-absorbing compounds in an aquatic liverwort and their usefulness as biomarkers of current and past UV radiation: a case study in the Atlantic-Mediterranean transition. Sci. Total Environ. 518–519, 248–257. doi: 10.1016/j.scitotenv.2015.03.006

PubMed Abstract | CrossRef Full Text | Google Scholar

Ramos-Madrigal, J., Runge, A. K. W., Bouby, L., Lacombe, T., Samaniego Castruita, J. A., Adam-Blondon, A. F., et al. (2019). Palaeogenomic insights into the origins of French grapevine diversity. Nat. Plants 5, 595–603. doi: 10.1038/s41477-019-0437-5

PubMed Abstract | CrossRef Full Text | Google Scholar

Rivers, M. C., Taylor, L., Brummitt, N. A., Meagher, T. R., Roberts, D. L., Nic Lughadha, E. (2011). How many herbarium specimens are needed to detect threatened species? Biol. Conserv. 144, 2541–2547. doi: 10.1016/j.biocon.2011.07.014

CrossRef Full Text | Google Scholar

Rønsted, N., Iwanycki, N. E., Maldonado, C., Hassemer, G., Martinez-Swatson, K. A., Saslis-Lagoudakis, H., et al. (2017). The future of drug discovery – are collections needed? Sci. Danica. Ser. B. Biol. 6, 253–266.

Google Scholar

Saslis-Lagoudakis, C. H., Iwanycki, N., Bruun-Lund, S., Petersen, G., Seberg, O., Jäger, A. K., et al. (2015). Identification of common horsetail (Equisetum arvense L.; Equisetaceae) using thin layer chromatography versus DNA barcoding. Sci. Rep. 5, 11942. doi: 10.1038/srep11942

PubMed Abstract | CrossRef Full Text | Google Scholar

Silva, C., Besnard, G., Piot, A., Razanatsoa, J., Oliveira, R. P., Vorontsova, M. S. (2017). Museomics resolve the systematics of an endangered grass lineage endemic to north-western Madagascar. Ann. Bot. 119, 339–351. doi: 10.1093/aob/mcw208

PubMed Abstract | CrossRef Full Text | Google Scholar

Smith, V. S., Blagoderov, V. (2012). Bringing collections out of the dark. ZooKeys 209, 1–6. doi: 10.3897/zookeys.209.3699

CrossRef Full Text | Google Scholar

Soltis, P. S. (2017). Digitization of herbaria enables novel research. Am. J. Bot. 104, 1281–1284. doi: 10.3732/ajb.1700281

PubMed Abstract | CrossRef Full Text | Google Scholar

Stadler, J., Mungai, G., Brandl, R. (2002). Weed invasion in East Africa: insights from herbarium records. Afr. J. Ecol. 36, 15–22. doi: 10.1046/j.1365-2028.1998.115-89115.x

CrossRef Full Text | Google Scholar

Stefanaki, A., Porck, H., Grimaldi, I. M., Thurn, N., Pugliano, V., Kardinaal, A., et al. (2019). Breaking the silence of the 500-year-old smiling garden of everlasting flowers: The En Tibi book herbarium. PLoS One 14, e0217779. doi: 10.1371/journal.pone.0217779

PubMed Abstract | CrossRef Full Text | Google Scholar

Thiers, B. M. (2020). The Worlds herbaria 2019. A summary report based on data from index herbariorum . http://sweetgum.nybg.org/science/ih/ (Accessed June 30th, 2020).

Google Scholar

Wales, N., Andersen, K., Cappellini, E., Ávila-Arcos, M. C., Gilbert, M. T. P. (2014). Optimization of DNA recovery and amplification from non-carbonized archaeobotanical remains. PLoS One 9, e86827. doi: 10.1371/journal.pone.0086827

PubMed Abstract | CrossRef Full Text | Google Scholar

Willis, C. G., Ellwood, E. R., Primack, R. B., Davis, C. C., Pearson, K. D., Gallinat, A. S., et al. (2017). Old plants, new tricks: Phenological research using herbarium specimens. Trends Ecol. Evol. 32, 531–546. doi: 10.1016/j.tree.2017.03.015

PubMed Abstract | CrossRef Full Text | Google Scholar

Wolkis, D., Deans, S. (2019). Picking from the past in preparation for a pest: assessing the potential for herbaria to serve as novel sources for ‘ōhi‘a seed preservation. Biopreserv. Biobank. 17, 6. doi: 10.1089/bio.2019.0044

CrossRef Full Text | Google Scholar

Yoshida, K, Burbano, H. A., Krause, J., Thines, M., Weigel, D., Kamoun, S. (2014). Mining herbaria for plant pathogen genomes: Back to the future. PLoS Pathogens. 10, e1004028. doi: 10.1371/journal.ppat.1004028

PubMed Abstract | CrossRef Full Text | Google Scholar

Zangerl, A. R, Berenbaum, M. R. (2005). Increase in toxicity of an invasive weed after reassociation with its coevolved herbivore. Proceedings of the National Academy of Sciences of the United States of America. 102, (43) 15529–15532. doi: 10.1073/pnas.0507805102

PubMed Abstract | CrossRef Full Text | Google Scholar

Keywords: herbarium collections, historical trends, museomics, plant tree of life, uses of herbaria

Citation: Rønsted N, Grace OM and Carine MA (2020) Editorial: Integrative and Translational Uses of Herbarium Collections Across Time, Space, and Species. Front. Plant Sci. 11:1319. doi: 10.3389/fpls.2020.01319

Received: 08 July 2020; Accepted: 11 August 2020;
Published: 21 August 2020.

Edited and reviewed by: Kathleen Pryer, Duke University, United States

Copyright © 2020 Rønsted, Grace and Carine. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Nina Rønsted, nronsted@ntbg.org; Olwen M. Grace, o.grace@kew.org; Mark A. Carine, M.Carine@nhm.ac.uk