Vicki Funk: Thinking Big about Collections

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This is a last in a series of posts [1,2,3] on the plant systematist Vicky Funk and her recent review article on collections-based research.  Since Funk is a research scientist and curator in the National Museum of Natural History’s (NMNH) Botany Department, it isn’t surprising that she begins a section on the future use of collections with stats on herbaria.  The NMNH, part of the Smithsonian Institution, is home to the U.S. National Herbarium, with a collection of over five million specimens.  The goal there and at many herbaria is to digitize the data for all specimens and in some cases to also image them.  If this could be done at every herbarium, the data would serve as a potent research tool not only for taxonomists but for ecologists, conservationists, and researchers in other fields who never before considered using the information about plants available in herbaria.

One burgeoning field based on the availability of digital specimen images is computer vision and machine learning techniques that make automated plant identification possible.  It is sort of face recognition for plants and is developing to the point that herbarium specimens can be sorted rather well, though the processes are hardly at the point where identification is as good as that done by taxonomists.  However, machine sorting could be employed as a way to narrow down the number of specimens a researcher would have to look at in hunting for new species.  One recent report the computer was able to distinguish between moss groups better than the human eye could.

Funk cites several successful digitization projects, noting that the Atlas of Living Australia is a particularly comprehensive one that has resulted in online access to all records of Australian plant specimens held in the country’s national herbaria.  Australia is also at the forefront in developing software tools to assist researchers in extracting as much information as possible and in the most effective ways.  However, Funk sees the future as going beyond national or even regional databases:  “A Central Portal so all resources are available to everyone is critical.  It is particularly important that these efforts are making the data and images available to researchers in the countries where the specimens were collected, thereby supporting research in those countries” (p. 185).  She is referring to the fact that the bulk of specimens collected in developing countries, particularly during their colonial pasts, are held in European and North American herbaria.  A first attempt to make these specimens broadly available was the Andrew W. Mellon Foundation funding of type specimen digitization, the results now accessible through JSTOR Global Plants along with a great deal of supporting botanical literature.

But what Funk visualizes is something more comprehensive, and as an example, she describes a project funded by the Powell Center of the US Geological Service.  It focuses on the approximately 2500 species of North American Compositae (Asteraceae) and the location data on hundreds of thousands of specimens aggregated from GBIF (includes information from institutions outside the US), BISON (from US government institutions) and iDigBio (US private institutions).  Funk notes that this data is not only aggregated but “cleaned” to make sure it is of high quality, an issue that critics of aggregation emphasize.  The data is then integrated with environmental and geophysical data on geochemistry, climate, topography, etc., as well as phylogenetics—including gene sequences from GenBank.  Think of the power of this:  linking specimens with sequence and environmental data.   This is truly a harbinger of a new age in collections-based research.  It is amazing that ten years ago, just digitizing data and imaging specimens was considered a feat, with the Paris Herbarium’s plan to digitize most of its specimens considered daring.  Now the assembly line method they used has become relatively common, and other large herbaria have substantial percentages of their collections digitized and imaged.

Linking natural history collections to genetic data banks means uniting the two great arms of bioinformatics.  It is a biologist’s dream come true, and this connection will become even more powerful when environmental data is brought into the mix—a much more complex process.  But Funk has seen the digital world burgeon and has been one of the forces behind making it applicable to systematics.  She has also helped make systematics valuable to other fields such as phylogenetics and the growing discipline of phylogenomic—being able to sequence and compare entire genomes.  This is the result of new sequencing techniques that utilize fragmented DNA, just the type available in herbarium specimens.  Drawing on an example from the Asteraceae, Funk cites a study in which the entire genomes of 93 of 95 Solidago, goldenrod, herbarium specimens were sequenced with the plants ranging in age from 5-45 years (Beck & Simple, 2015).

In closing Funk notes:  “One exciting trend is the developing field of Integrative Systematics where collections-based systematics is combined with extensive field studies, phylogenetics, phylogenomics, detailed morphological studies, biogeographic inferences and diversification analysis to present a more comprehensive global” (p. 187).  She also argues for the maintenance of collections in educational institutions to insure the instruction of future generations of systematists; the digitization of cleared leaf slides, anatomy slides, pollen images, chromosome count images, and illustrations to fill out the information available to researches; and finally a series of symposia on the Tree of Life where systematists can map out a research agenda for the rest of the 21st century.

References

Beck, J. B., & Semple, J. C. (2015). Next-Generation Sampling: Pairing Genomics with Herbarium Specimens Provides Species-Level Signal in Solidago (Asteraceae). Applications in Plant Sciences, 3(6), 1500014.

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Vicki Funk: The Age of Tree Thinking

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In the last post, I began my discussion of Vicki Funk’s (2018) recent article on “Collections-Based Science in the 21st Century” that I’ll continue here.  In this review, she terms the first 15 years of the 21st century “An Age of Tree Thinking,” in other words a time of investigating evolutionary relationships and the use of phylogenies.  This is a major interest of Pam and Douglas Soltis of the University of Florida, two other leaders in the field of collections-based research (Allen et al., 2019).   Funk gives examples of what she means by this term, beginning with evolutionary medicine.  This field’s work includes tracing changes in viruses as they are transmitted through a population and even within one body over time.  Funk notes that museum specimens of woodrats have been found to harbor viruses similar to those causing Chagas disease.  She also touches on food safety, beginning with GenomeTrakr a pathogen database set up by the Food and Drug Administration.  It hosts whole genome sequences for pathogens, mostly those implicated in food poisoning.  When an outbreak occurs, the pathogen involved can now be quickly sequenced, and then compared to sequences in the database; this helps to identify the source of contamination and speed control of the outbreak.

Moving on to evolutionary ecology, Funk cites a number of examples of how phylogenetics can illuminate ecological questions.  For example, DNA was sequenced from ragweed (Ambrosia artemisiifolia) specimens collected through time, both before and after deforestation in particular areas.  Pollen core data suggest that ragweed, an aggressive weed, was uncommon before deforestation.  The DNA sequencing data indicates that there was a hybridization before deforestation that may have permitted the hybrid to grow more aggressively when trees were removed.  This is a good example of pairing historical data with molecular analysis.

Funk’s paper also explores the idea of DNA barcoding, a technique that her colleague John Kress at the Smithsonian has fostered.  For plants, it involves sequencing two regions of the chloroplast genome that serve as a fingerprint for species identification.  Kress and his colleagues (2009) barcoded all tree species growing in a plot on Barro Colorado Island in Panama, a long-term Smithsonian study site.  The resulting phylogenies are being employed to investigate the relationship between habitat and community structure.  Barcodes are also used to monitor illegal traffic in endangered species, for example, as a way to identify illegal shipments of rare woods.  Since her article’s title, “Collections-Based Science in the 21st Century,” doesn’t limit Funk to only plants, she slips in a reference to molecular phylogenetics in human evolution studies, noting how DNA extracts from fossils of Neandertals and of a hominin population called the Denisovans found in the Siberian Altai Mountains, as well as from present-day humans, were employed to work out the relationship among them, with Neanderthals and today’s humans more closely related to each other than to Denisovans.  In an example relevant to botany, medically important plants have been barcoded over the past ten years, and molecular phylogenetics can be used to test the purity of ingredients in herbal medicines.  This is a perennial problem due to varying levels of quality control for these materials, resulting in impure or ineffective products.

What these examples of tree thinking have in common is that they involve DNA sequencing and the storage of that information so it can be used in future studies.  In other words, there is a summative process going on here, and these databases, if properly maintained and utilized will only become more and more valuable and effective.  In the next section of her article, Funk deals with the future, and calls it “An Age of Thinking Big.”  This theme is also taken up by a group of European researchers (Besnard et al., 2018).  Funk discusses not only collections of DNA sequences, and the voucher specimens that back them up, but also the increasing availability of online data about natural history specimens as well as images of them.  Digitization has been going on for years, especially since the development of BISON, which is a database for specimens from US government facilities such as the Smithsonian, and iDigBio, for private research and educational collections.  While more and more information is coming online, there is still a great deal to do.  To date, less than half of all plant specimens are databased, and that percentage is even lower for animals—there are an awful lot of insects out there, which were relatively easy to collect, but not so easy to image, to say nothing of jellyfish, etc.

Funk considers some of the questions that could be tackled if all specimen data were available to researchers:  “What parts of the world need additional collecting expeditions?  How many species are rare?  How many species have not been collected in the last 50 years and may be extinct?  Are there certain areas that have a lot of rarely collected species and are these areas endangered ecosystems?  How fast have invasive species moved into new areas?  How has community composition changed through time?” (p. 182).  This list is reminiscent of Funk’s “100 Uses for an Herbarium.”  With her vast experience she is very good at thinking about why collections are valuable as research tools, and this analysis is especially useful today as many collections are facing uncertain futures.  In an earlier post I cited one example of Funk’s writing on this topic.  Here I’ll end with another citation, a review article she wrote with several of her colleagues on what collection based systematics should look like in 2050 (Wen et al., 2015).  Her answers to this question will be covered in the next and last post in these series.

References

Allen, J. M., Folk, R. A., Soltis, P. S., Soltis, D. E., & Guralnick, R. P. (2019). Biodiversity synthesis across the green branches of the tree of life. Nature Plants, 5(1), 11–13.

Besnard, G., Gaudeul, M., Lavergne, S., Muller, S., Rouhan, G., Sukhorukov, A. P., … Jabbour, F. (2018). Herbarium-based science in the twenty-first century. Botany Letters, 165(3–4), 323–327.

Kress, W. J., Erickson, D. L., Jones, F. A., Swenson, N. G., Perez, R., Sanjur, O., & Bermingham, E. (2009). Plant DNA barcodes and a community phylogeny of a tropical forest dynamics plot in Panama. Proceedings of the National Academy of Sciences, 106(44), 18621–18626.

Wen, J., Ickert‐Bond, S. M., Appelhans, M. S., Dorr, L. J., & Funk, V. A. (2015). Collections-based systematics: Opportunities and outlook for 2050. Journal of Systematics and Evolution, 53(6), 477–488.

Vicki Funk: The History of Collections-Based Science

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In the last post, I introduced Vicki Funk, a plant systematist who is a research scientist and curator at the U.S. National Herbarium, part of the Smithsonian Institution’s National Museum of Natural History.  There I mentioned that Funk had recently published a review article called “Collections-Based Science in the 21 Century,” published in the May 2018 issue of the Journal of Systematics and Evolution.  As with most review articles, it begins with a historical perspective.  The first sentence is a bold claim:  “Major revolutions in scientific thought have occurred because of collections-based research” (p. 175).  Funk is in a position to know both because she works in an institution with a premier natural history collection, and because she herself has contributed to today’s revolution in how collections are accessed and utilized.

Funk begins with the age of classification and Carl Linnaeus’s heavy reliance on natural history collections in creating his artificial system of classification and nomenclatural reform.  Michel Adanson and Antoine Laurent de Jussieu, working at the botanical garden in Paris with its notable herbarium, devised natural classification schemes that in various forms eventually replaced the Linnaean artificial system.  The 19th century, Funk notes, began with Alexander von Humboldt’s expedition to Latin America that gave him the perspective to develop the field of biological and physical geography, along with ecology and meteorology.  He and his traveling partner Aimée Bonpland collected 50,000 specimens, documenting many new genera and species as well as the relationship between geography and species distributions.  Later, Charles Darwin, Joseph Dalton Hooker, and Alfred Russel Wallace not only collected specimens but used them to build on Humboldt’s work and to document the concept of species change.  With examples like this Funk makes clear the connection between collection and theory building, as well as the importance of great natural history museum collections, many of which were built in the 19th century.

Funk terms the 20th century the “Age of Synthesis” in reference to the evolutionary synthesis that developed at mid-century and to “four collection-based ideas and methods that changed . . . the way we do science” (p. 178).  The first was the concept of continental drift and with it the idea that land bridges between continents had existed in the past.  Both Humboldt and J.D. Hooker argued for these from the similarities among organisms in areas that are now separated by great distances.  Second was the development of phylogenetic systematics or cladistics, a field to which Funk has contributed a good deal both theoretically (1991) and in terms of her research, especially on the Asteraceae.  Cladistics deals with using derived characters to objectively construct relationships, then grouping taxa so all are descended from a single common ancestor without omitting any of its descendants.  This is a complex field, and as a recent issue of the American Journal of Botany (August 2018) on fossil plants reveals, there are problems that arise when only living species are used in creating monophyletic groups, so fossil collections are crucial to the process.

Under the third 20th-century trend, Funk lists databasing collections, biodiversity science, and niche modeling.  This is a huge triumvirate, but with its parts closely tied together.  Databasing collection data—specimen identification as well as place and time of collection—makes it possible to more easily assess data on the biodiversity of a region as well as on how it may be changing over time.  It also allows rigorous niche modeling, a term for techniques employing occurrence data to model the possible spatial extent of a species based on geographical and climatic data.  Ecology has always been a field using sophisticated mathematical models but the availability of digital data and high-speed computing have caused an explosion in research.  And this is really only the beginning, as more collection data and analytic tools come online.

The final concept Funk cites as developing in the 20th century is molecular phylogenetics, the analysis of gene sequences as a way to discover phylogenetic relationships.  She writes:  “Collections are an excellent source of material for the extraction of DNA, but they are also important because they provide the vouchers of the DNA sequences, and their presence allows us to check the identification of samples and to gather the data needed to ask questions about character evolution and modes of speciation” (p. 180).  These vouchers usually contain at least some geographic information, bringing in the biogeography she mentioned earlier.  Molecular systematics helped to clear up some arguments about derived characters used in cladistics and resulted in a major reorganization of plant phylogenetics.  As will become apparent in the next two posts, sequencing techniques have changed rapidly during the latter part of the 20th and into the 21st century, increasing the efficacy of DNA analysis with herbarium specimens.  These tools now allow sequencing of species for which no fresh material is available because the species are rare, inaccessible, or even extinct.  If historical material is available, they also enable work on how the genetics of a species may have changed over the last few hundred years.

Vicki Funk and the Uses for a Herbarium

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Montanoa hibiscifolia, photo by Forest & Kim Starr.

Early in my romance with herbaria I came across an article by Vicki Funk called “100 Uses for an Herbarium (Well at Least 72).”  Learning about the many ways plant collections can be utilized got me even more excited about them.  I also felt I had met a friendly member of the herbarium community, someone with a sense of humor.  She came up with a great title for her piece and then stuck with it even though she didn’t quite get to the magic number her title promised.  In the piece, Funk lists herbarium functions from verifying plant Latin names in issues of nomenclature, to serving as a repository for voucher specimens, to making specimens available to students and interested members of the public.  This article was written in 2004, and I am sure that Funk could come up with many more roles today.  She in fact does move in that direction in a major review article she recently published on “Collections-Based Science in the 21st Century” (2018).  I plan to use that article as the basis for this series of posts, but first I’ll say a little more about Vicky Funk, who seems to me to be the epitome of a plant systematist in the 21st century.

Focusing on Funk’s work right now is particularly timely because she has won the 2018 Asa Gray Award, the American Society of Plant Taxonomists’ highest honor.  The fact that her nomination was accompanied by 18 letters of support suggests just how deserved this recognition is.  Funk is a research scientist and curator at the U.S. National Herbarium in the Department of Botany at the National Museum of Natural History, part of the Smithsonian Institution.  She is an expert on the Asteraceae or Compositae and is lead editor for the 2009 Compositae: Systematics, Evolution, and Biogeography of the Compositae.  This is a massive work in every sense of the term because it treats one of the largest flowering plant families.  She has also been involved in the creation of the digital Global Compositae Checklist.

Funk received her Ph.D. from Ohio State University for work on Montanoa, a genus of plants with daisy-like flowers in the Heliantheae or sunflower tribe of the Asteraceae.  They are native to Central and South America, but since then Funk has worked in Hawaii, Guyana, and a number of other places, and perhaps most importantly in the developing field of phylogenetics.  She has also been an important figure in the development of plant cladistics and is coauthor of the classic, The Compleat Cladist.  While doing all this research, she has been a good citizen of the plant systematics community as president of both the American Society of Plant Taxonomists and the International Association of Plant Taxonomists.  I have yet to meet Funk, in part because I am in awe of her.  However I have heard her speak; her passion, intelligence, and good sense come through along with her deep and comprehensive knowledge of the field.

Funk has also been a hard working member of the Smithsonian scientific community.  I keep up with her through the pages of the U.S. National Herbarium’s newsletter that has the great title The Plant Press and is available online.  The first issue I read was from 2007 when she had the lead article on the 20-year project of the National Museum of Natural History called the Biological Diversity of the Guiana Shield program.  As Funk describes it, the shield is a geological formation of igneous and metamorphic rock that underlies the northeast corner of South America and includes parts of Venezuela, Guyana, Surinam, French Guiana, Brazil, and Columbia.   At the point when she was writing, the Shield plants checklist, of which she was an editor, was in press.  It has proven to be an important resource since its publication in 2007.  I should note that her article includes a photo of herself and two colleagues doing what is stated to be their “best” imitation of a jacana, a South American marsh bird, standing on one leg.  In a later issue of The Plant Press, (April-June 2011), she is pictured more sedately with the University of the District of Columbia students she was mentoring.  In most photos Funk is wearing Hawaiian patterned shirts replete with large tropical blooms, seemingly to remind herself of her work on Hawaiian plants and to provide others with a pleasant aesthetic experience.

But while Funk can be light-hearted, she can also be deadly serious, as she was in the October 2014 issue of The Plant Press with the opening lead article:  “The Erosion of Collections-Based Science: Alarming Trend or Coincidence?”  She unfortunately sides with the first alternative, citing a number of disturbing cases over the prior years, including elimination of the science program at the Milwaukee Public Museum, dwindling support for scientific research at Fairchild Tropical Botanic Garden in Florida, closing of the science program at the Brooklyn Botanic Garden, and diminishment of programs and staff at the California Academy of Sciences, the Field Museum in Chicago, and the Royal Botanic Gardens, Kew.  Funk then goes on to outline the results of these cuts:  less projects in developing nations to assist in their scientific and economic development, weakening of education programs in the life sciences, and reduction in research on such crucial topics as climate change.  As the following posts will illustrate, these were hardly Funk’s last words on these topics.  She is in the forefront of the effort to support the future of systematics and environmental studies.

References

Funk, V. A., & International Association for Plant Taxonomy. (2009). Systematics, evolution, and biogeography of Compositae. Vienna, Austria: International Association for Plant Taxonomy, Institute of Botany, University of Vienna.

The Myriad Uses of a Herbarium

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Type specimen of Altamiranoa elongata from the US Herbarium, Smithsonian Institution

When it comes to discussing the uses for plant specimens, you can’t do better than refer to Vicki Funk’s classic 2004 article “100 Uses for an Herbarium (Well at Least 72).” It is thorough and succinct. So why am I bothering to write on the same topic, if Funk has covered it so brilliantly? Well, that would deprive me of the fun of exploring some of those uses in a little more detail and perhaps even unearthing one or two new ones. While service to botany may seem the obvious place to begin, I’m going to start with medicine, the field that prompted the creation of the first documented herbarium, that of the Italian botanist and professor of medical botany, Luca Ghini (1490-1556), founded the first botanical garden at Pisa. The garden was designed to introduce students to the plants that were used by apothecaries, so they would be able to recognize them. This was obviously the function of the herbarium as well, and several of Ghini’s students, including Andrea Cesalpino (1519-1603) and Ulisse Aldrovandi (1522-1605) created specimen collections that exist to this day. Apothecaries also took up the practice, with Hieronymus Harder (1523-1607) creating a dozen bound herbaria, eleven of which are still extant.

The link between herbaria and medicine continues to this day. Those doing research on herbal medicines are often required to create voucher specimens of the plants they are studying so others can verify the identification in the future (Eisenman et al., 2012). One problem in past research was the difficulty of getting consistent results from one batch of plant material to the next. Having some of the material itself preserved in a voucher makes it easier to check whether or not the same species, subspecies, or variety was used in both cases. Not only can the plants be visually examined, but chemical tests can be done on the material if necessary. Rainer Bussmann has a chapter on “Taxonomy—An Irreplaceable Tool for Validation of Herbal Medicine” if you would like to learn more on this topic.

Voucher herbarium specimens are required in almost all botanical research, because the plant itself is the best evidence for answering questions about what species was actually growing where at a particular time. The most valuable kind of voucher is the type specimen, the record of the plant that was used in describing the species for the first time. Since modern taxonomy dates back to the publication of names by Carl Linnaeus in Species Plantarum in 1753, it is no wonder that the material he studied is itself still being tracked down to give as full a record as possible of the plant specimens, and in some cases plant images, upon which he based his descriptions (Jarvis, 2007). To this day, journals such as Taxon require authors to list specimen numbers and the herbaria where they are located for all material studied in revising taxa.

With the advent of DNA sequencing, herbarium vouchers can now be used in an entirely new way. A small piece of a specimen may yield enough intact DNA for researchers to identify a species with DNA sequencing. There are a number of factors limiting success including age, method of preparation, and species, but there are now many papers documenting the reliability of the results. The rich information the studies can yield include improvement in the fungal phylogenetic tree (Dentinger et al., 2015), tentatively identifying plants on Linnaeus’s Hamerby’s estate as related to his type specimens (Andreasen et al., 2014), and employing herbarium specimens in large-scale genomics research.

There are also more conventional uses of specimens that are nonetheless critical to botany. The development of floras—lists of plants in a particular locale—are impossible without using herbaria for collecting information. And when botanists are looking for living specimens of a species, the logical place to begin is in the herbarium where they can discover the location of past collections for the plant in question. The Royal Botanic Gardens, Kew (Kew) produces seed collecting guides for botanists going to areas such as Mozambique. The guides include descriptions of each species with a photo of the herbarium sheet as well as of the live plant. Specimens also can be used to hunt for other things besides plants, like diamonds and gold. The palm-like plant, Pandanus candelabrum is rare because it only grows in soils containing kimberlite which is rich in magnesium, potassium, and phosphorus. Kimberlite is also the volcanic rock where diamonds are found. So P. candelabrum, which grows in Liberia, may make it a little easier to discover these gems. As for gold, particles of the metal in Eucalyptus specimens may indicate gold deposits in the area where the trees grew. Using this link to direct prospecting is still experimental. It is definitely a long way from panning for gold, but worth a try (Lintern et al., 2013). These are very specific examples of botanical biogeography, but this is a much broader topic that I’ll discuss in my next post.

References

Andreasen, K., Manktelow, M., Sehic, J., & Garkava-Gustavsson, L. (2014). Genetic identity of putative Linnaean plants: Successful DNA amplification of Linnaeus’s crab apple Malus baccata. Taxon, 63(2), 408–416.

Dentinger, B. T. M., Gaya, E., O’Brien, H., Suz, L. M., Lachlan, R., Díaz-Valderrama, J. R., … Aime, M. C. (2015). Tales from the crypt: genome mining from fungarium specimens improves resolution of the mushroom tree of life. Biological Journal of the Linnean Society, 117(1), 11-32.

Eisenman, S., Tucker, A., & Struwe, L. (2012). Voucher specimens are essential for documenting source material used in medicinal plant investigations. Journal of Medicinally Active Plants, 1(1), 30–43.

Jarvis, C. (2007). Order Out of Chaos: Linnaean Plant Names and Their Types. London, UK: Linnaean Society.

Lintern, M., Anand, R., Ryan, C., & Paterson, D. (2013). Natural gold particles in Eucalyptus leaves and their relevance to exploration for buried gold deposits. Nature Communications, 4, 2274.