Publications

Forthcoming
Emily K. Meineke, Charles C. Davis, and Jonathan Davies. Forthcoming. “The unrealized potential of herbaria for global change biology.” Ecological Monographs, Pp. 1-21.Abstract

 

Plant and fungal specimens in herbaria are becoming primary resources for investigat-

ing 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 inva-

sive 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 speci-

mens are under-explored relative to vascular plants. To facilitate broader application of plant and fun-

gal 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.

Key words: climate change; extinction; global change; habitat conversion; herbarium; historical data; invasive

species; museum specimens.

 

2019
Lucas Marinho, Liming Cai, Xiaoshan Duan, Brad R. Ruhfel, Pedro Fiaschi, André M. Amorim, Cássio van den Berg, and Charles C. Davis. 5/1/2019. “Plastomes resolve generic limits within tribe Clusieae (Clusiaceae) and reveal the new genus Arawakia.” Molecular Phylogenetics and Evolution, 134, Pp. 142-151. Publisher's VersionAbstract
Clusieae is an exclusively Neotropical tribe in the family Clusiaceae sensu stricto. Although tribes within Clusiaceae are morphologically and phylogenetically well-delimited, resolution among genera within these tribes remains elusive. The tribe Clusieae includes an estimated ∼500 species distributed among five genera: ChrysochlamysClusiaDystovomitaTovomita, and Tovomitopsis. In this study, we used nearly complete plastid genomes from 30 exemplar Clusieae species representing all genera recognized, plus two outgroups to infer the phylogeny of the tribe using Maximum Likelihood and Bayesian Inference. For comparison, we also inferred a phylogeny from the nuclear Internal Transcribed Spacer (ITS) region using the same methods. Our study corroborates earlier findings that Clusia is monophyletic while Tovomita is not. It also provides additional support to the hypothesis that Chrysochlamys and Tovomitopsis are not closely related despite gross morphological similarity. Tovomita is divided into three distantly related clades: (i) core Tovomita (including the type T. guianensis), (ii) T. croatii, and (iii) the T. weddelliana species complex. Members of the T. weddelliana complex are isolated from the core Tovomita, and placed in a well-supported clade that is sister to a clade composed of Chrysochlamys plus ClusiaTovomita croatii is nested within Chrysochlamys. We propose taxonomic revisions to accommodate our phylogenetic findings, including the description of the new genus Arawakia, which includes the 18 species formerly recognized in the T. weddelliana species complex. Lectotypes are also designated for nine species (i.e., Arawakia angustataA. lanceolataA. lingulataA. longicuneataA. macrocarpaA. oblanceolataA. pithecobiaA. rhizophoroides, and A. weddelliana), and a taxonomic key for the identification of the six genera of Clusieae recognized is presented.
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Charles C. Davis and Sarah Matthews. 4/24/2019. “Evolution of Land Plants.” Oxford Bibliographies. Publisher's Version PDF
William D. Pearse, Charles C. Davis, David W. Inouye, RIchard B. Primack, and T. Jonathan Davis. 3/2019. “[Author Correction] A statistical estimator for determining the limits of contemporary and historic phenology.” Nature Ecology & Evolution, 3, 3, Pp. 499. Publisher's Version PDF
Liming Cai, André M. Amorim, Sugumaran Manickam, Liang Liu, Joshua S. Rest, and Charles C. Davis. 2/28/2019. “Thrive with Additional Sets of Genome: Widespread Paleopolyploidization Buffers plants Through Eocene Climatic Upheaval.” Oxford University Press 59, Pp. E29-E29.
Liming Cai, Zhenziang Xi, André M Amorim, Manickam Sugumaran, Joshua S. Rest, Liang Liu, and Charles C. Davis. 1/1/2019. “Widespread Ancient whole-genome duplications in Malpighiales coincide with Eocene global climatic upheval.” New Phytologist, 221, 1, Pp. 565-576. Publisher's Version PDF
2018
Daniel S. Park, Ian Breckheimer, Alex C. Williams, Edith Law, Aaron M. Ellison, and Charles C. Davis. 11/19/2018. “Herbarium specimens reveal substantial and unexpected variation in phenological sensitivity across the eastern United States.” The Royal Society Publishing, 374, 1763. Publisher's VersionAbstract

Phenology is a key biological trait that can determine an organism's survival and provides one of the clearest indicators of the effects of recent climatic change. Long time-series observations of plant phenology collected at continental scales could clarify latitudinal and regional patterns of plant responses and illuminate drivers of that variation, but few such datasets exist. Here, we use the web tool CrowdCurio to crowdsource phenological data from over 7000 herbarium specimens representing 30 diverse flowering plant species distributed across the eastern United States. Our results, spanning 120 years and generated from over 2000 crowdsourcers, illustrate numerous aspects of continental-scale plant reproductive phenology. First, they support prior studies that found plant reproductive phenology significantly advances in response to warming, especially for early-flowering species. Second, they reveal that fruiting in populations from warmer, lower latitudes is significantly more phenologically sensitive to temperature than that for populations from colder, higher-latitude regions. Last, we found that variation in phenological sensitivities to climate within species between regions was of similar magnitude to variation between species. Overall, our results suggest that phenological responses to anthropogenic climate change will be heterogeneous within communities and across regions, with large amounts of regional variability driven by local adaptation, phenotypic plasticity and differences in species assemblages. As millions of imaged herbarium specimens become available online, they will play an increasingly critical role in revealing large-scale patterns within assemblages and across continents that ultimately can improve forecasts of the impacts of climatic change on the structure and function of ecosystems.

This article is part of the theme issue ‘Biological collections for understanding biodiversity in the Anthropocene’.

park_herbarium_specimens.pdf
Cintia Iha, Christopher J. Grassa, Goia M. de Lyra, Charles C. Davis, Heroen Verbruggen, and Mariana C. Oliveira. 9/12/2018. “Organellar Genomics: A Useful Tool to Study the Evolutionary Relationships and Molecular Evolution in Gracilarilacae (Rhodophyta).” Journal of Phycology, 54, Pp. 775-787. Publisher's VersionAbstract
Gracilariaceae has a worldwide distribution including numerous economically important species. We applied high‐throughput sequencing to obtain organellar genomes (mitochondria and chloroplast) from 10 species of Gracilariaceae and, combined with published genomes, to infer phylogenies and compare genome architecture among species representing main lineages. We obtained similar topologies between chloroplast and mitochondrial genomes phylogenies. However, the chloroplast phylogeny was better resolved with full support. In this phylogeny, Melanthalia intermedia is sister to a monophyletic clade including Gracilaria and Gracilariopsis, which were both resolved as monophyletic genera. Mitochondrial and chloroplast genomes were highly conserved in gene synteny, and variation mainly occurred in regions where insertions of plasmid‐derived sequences (PDS) were found. In mitochondrial genomes, PDS insertions were observed in two regions where the transcription direction changes: between the genes cob and trnL, and trnA and trnN. In chloroplast genomes, PDS insertions were in different positions, but generally found between psdD and rrs genes. Gracilariaceae is a good model system to study the impact of PDS in genome evolution due to the frequent presence of these insertions in organellar genomes. Furthermore, the bacterial leuC/leuD operon was found in chloroplast genomes of Gracilaria tenuistipitata, G. chilensis, and M. intermedia, and in extrachromosomal plasmid of G. vermiculophylla. Phylogenetic trees show two different origins of leuC/leuD: genes found in chloroplast and plasmid were placed with proteobacteria, and genes encoded in the nucleus were close to Viridiplantae and cyanobacteria.
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Liming Cai, Zhenxiang Xi, André M. Amorim, M. Sugumaran, Rest, Joshua S, Liang Liu, and Charles C. Davis. 7/21/2018. “Widespread ancient whole genome duplications in Malpighiales coincide with Eocene global climatic upheaval.” New Phytologist. Publisher's Version PDF
Cintia Iha, Christopher J. Grassa, Goia de M. Lyra, Charles C. Davis, and Heroen Verbruggen. 7/10/2018. “Organellar genomics: a useful tool to study evolutionary relationships and molecular evolution in Gracilariaceae (Rhodophyta).” Journal of Phycology. Publisher's VersionAbstract
Gracilariaceae has a worldwide distribution including numerous economically important species. We applied high‐throughput sequencing to obtain organellar genomes (mitochondria and chloroplast) from ten species of Gracilariaceae and, combined with published genomes, to infer phylogenies and compare genome architecture among species representing main lineages. We obtained similar topologies between chloroplast and mitochondrial genomes phylogenies. However, the chloroplast phylogeny was better resolved with full support. In this phylogeny, Melanthalia intermedia is sister to a monophyletic clade including Gracilaria and Gracilariopsis, which were both resolved as monophyletic genera. Mitochondrial and chloroplast genomes were highly conserved in gene synteny, and variation mainly occurred in regions where insertions of plasmid‐derived sequences (PDS) were found. In mitochondrial genomes, PDS insertions were observed in two regions where the transcription direction changes: between the genes cob and trnL, and trnA and trnN. In chloroplast genomes, PDS insertions were in different positions, but generally found between psdD and rrs genes. Gracilariaceae is a good model system to study the impact of PDS in genome evolution due to the frequent presence of these insertions in organellar genomes. Furthermore, the bacterial leuC/leuD operon was found in chloroplast genomes of Gracilaria tenuistipitata, G. chilensis, and M. intermedia, and in extrachromosomal plasmid of G. vermiculophylla. Phylogenetic trees show two different origins of leuC/leuD: genes found in chloroplast and plasmid were placed with proteobacteria, and genes encoded in the nucleus were close to Viridiplantae and cyanobacteria.
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Daniel S. Park, Aaron M. Ellison, and Charles C. Davis. 7/2018. “Mating system does not predict niche breath.” Global Ecology and Biogeography, 27, 7, Pp. 804-813. Publisher's VersionAbstract
Self‐pollinating plants (‘selfers’) have larger geographical ranges and inhabit higher latitudes than their outcrossing relatives. This finding has led to the hypothesis that selfers also have broader climatic niches (‘niches’) because the increased likelihood of successful colonization into new areas and the initial purging of deleterious mutations could offset the inability of selfers to adapt to new environments owing to low heterozygosity. Here, we examine the niches of hundreds of closely related selfing and outcrossing species to determine whether selfers do indeed have larger niche breadths.
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Joel H. Nitta, Saad Amer, and Charles C. Davis. 6/21/2018. “Microsorum× tohieaense (Polypodiaceae), a New Hybrid Fern from French Polynesia, with Implications for the Taxonomy of Microsorum.” Systematic Botany, 43, 2, Pp. 397-413. Publisher's VersionAbstract
A new hybrid microsoroid fern, Microsorum × tohieaense (Microsorum commutatum × Microsorum membranifolium) from Moorea, French Polynesia is described based on morphology and molecular phylogenetic analysis. Microsorum × tohieaense can be distinguished from other French Polynesian Microsorum by the combination of sori that are distributed more or less in a single line between the costae and margins, apical pinna wider than lateral pinnae, and round rhizome scales with entire margins. Genetic evidence is also presented for the first time supporting the hybrid origin of Microsorum × maximum(Microsorum grossum × Microsorum punctatum), and possibly indicating a hybrid origin for the Hawaiian endemic Microsorum spectrum. The implications of hybridization for the taxonomy of microsoroid ferns are discussed, and a key to the microsoroid ferns of the Society Islands is provided.
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Patrick W. Sweeney, Binil Starly, Paul J. Morris, Yiming Xy, Aimee Jones, Sridhar Radhakrishnan, Christopher J. Grassa, and Charles C. Davis. 6/3/2018. “Large-scale digitization of herbarium specimens: Development and usage of an automated, high-throughput conveyor system.” International Association for Plant Taxonomy, 67, 1, Pp. 165-178. Publisher's VersionAbstract
The billions of specimens housed in natural science collections provide a tremendous source of under-utilized data that are useful for scientific research, conservation, commerce, and education. Digitization and mobilization of specimen data and images promises to greatly accelerate their utilization. While digitization of natural science collection specimens has been occurring for decades, the vast majority of specimens remain un-digitized. If the digitization task is to be completed in the near future, innovative, high-throughput approaches are needed. To create a dataset for the study of global change in New England, we designed and implemented an industrial-scale, conveyor-based digitization workflow for herbarium specimen sheets. The workflow is a variation of an object-to-image-to-data workflow that prioritizes imaging and the capture of storage container-level data. The workflow utilizes a novel conveyor system developed specifically for the task of imaging flattened herbarium specimens. Using our workflow, we imaged and transcribed specimen-level data for almost 350,000 specimens over a 131-week period; an additional 56 weeks was required for storage container-level data capture. Our project has demonstrated that it is possible to capture both an image of a specimen and a core database record in 35 seconds per herbarium sheet (for intervals between images of 30 minutes or less) plus some additional overhead for container-level data capture. This rate was in line with the pre-project expectations for our approach. Our throughput rates are comparable with some other similar, high-throughput approaches focused on digitizing herbarium sheets and is as much as three times faster than rates achieved with more conventional non-automated approaches used during the project. We report on challenges encountered during development and use of our system and discuss ways in which our workflow could be improved. The conveyor apparatus software, database schema, configuration files, hardware list, and conveyor schematics are available for download on GitHub.
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Andrea S. Meseguer, Jorge M. Lobo, Josselin Cornualt, Davis Beerling, Brad R. Ruhfel, Charles C. Davis, Emmanuelle Jousellin, and Isabel Sanmartin. 5/2018. “Reconstructing deep‐time palaeoclimate legacies in the clusioid Malpighiales unveils their role in the evolution and extinction of the boreotropical flora.” Global Ecology and Biogeography, 27, 5, Pp. 616-628. Publisher's VersionAbstract

During its entire history, the Earth has gone through periods of climate change similar in scale and pace to the warming trend observed today in the Anthropocene. The impact of these ancient climatic events on the evolutionary trajectories of organisms provides clues on the organismal response to climate change, including extinction, migration and persistence. Here, we examine the evolutionary response to climate cooling/warming events of the clusioid families Calophyllaceae, Podostemaceae and Hypericaceae (CPH clade) and the genus Hypericum as test cases.
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Jennifer M. Yost, Patrick W. Sweeney, Ed Gilbert, Gil Nelson, Robert Guralnick, Amanda S. Gallnat, Elizabeth R. Ellwood, Natalie Rossington, Charles G. Willis, Stanley D. Blum, Romona L. Walls, Elspeth M. Haston, Michael W. Denslow, Constantin M. Zohner, Ashley B. Morris, Brian J. Stucky, J. Richard Carter, David G. Baxter, Kjell Bolmgren, Ellen G. Denny, Ellen Dean, Katelin D. Pearson, Charles C. Davis, Brent D. Mishler, Pamela S. Soltis, and Susan J. Mazer. 2/28/2018. “Digitization protocol for scoring reproductive phenology from herbarium specimens of seed plants.” Applications in Plant Sciences, 6, 2, Pp. 1-11. Publisher's VersionAbstract

Premise of the Study
Herbarium specimens provide a robust record of historical plant phenology (the timing of seasonal events such as flowering or fruiting). However, the difficulty of aggregating phenological data from specimens arises from a lack of standardized scoring methods and definitions for phenological states across the collections community.

Methods and Results
To address this problem, we report on a consensus reached by an iDigBio working group of curators, researchers, and data standards experts regarding an efficient scoring protocol and a data-sharing protocol for reproductive traits available from herbarium specimens of seed plants. The phenological data sets generated can be shared via Darwin Core Archives using the Extended MeasurementOrFact extension.

Conclusions
Our hope is that curators and others interested in collecting phenological trait data from specimens will use the recommendations presented here in current and future scoring efforts. New tools for scoring specimens are reviewed.

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Charles C. Davis and Aaron M. Ellison. 2018. “The Brave New World of the Digital Herbarium.” ReVista, Spring/Summer 2018, Pp. 8-11. Publisher's Version PDF
2017
Emily K. Meineke, Charles C. Davis, and Jonathan T. Davies. 11/14/2017. “Running head: Herbaria for understanding global change.” BioRxiv. Publisher's VersionAbstract
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 outline 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, despite potentially large biases. With the goal of positioning herbaria as hubs for global change research, we suggest future research directions and curation priorities.
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William D. Pearse, Charles D. Davis, David W. Inouye, RIchard B. Primack, and T. Jonathan Davies. 11/5/2017. “A statistical estimator for determining the limits of contemporary and historic phenology.” Nature, Ecology & Evolution.Abstract

Climate change affects not just where species are found, but also when species’ key life-history events occur—their phenol-

ogy. Measuring such changes in timing is often hampered by a reliance on biased survey data: surveys identify that an event

has taken place (for example, the flower is in bloom), but not when that event happened (for example, the flower bloomed

yesterday). Here, we show that this problem can be circumvented using statistical estimators, which can provide accurate and

unbiased estimates from sparsely sampled observations. We demonstrate that such methods can resolve an ongoing debate

about the relative timings of the onset and cessation of flowering, and allow us to place modern observations reliably within the

context of the vast wealth of historical data that reside in herbaria, museum collections, and written records. We also analyse

large-scale citizen science data from the United States National Phenology Network and reveal not just earlier but also poten-

tially more variable flowering in recent years. Evidence for greater variability through time is important because increases in

variation are characteristic of systems approaching a state change.

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Williams. Alex C., Joslin Goh, Charlie G. Willis, Aaron M. Ellison, James H. Brusuelas, Charles C. Davis, and Edith Law. 10/26/2017. “Deja Vu: Characterizing Worker Reliability Using Task Consistency.” In Association for the Advancement of Artificial IntelligenceI Conference on Human Computation and Crowdsourcing . Québec City, Québec, Canada: The AAAI Press, Palo Alto, California. Publisher's VersionAbstract
Consistency is a practical metric that evaluates an instrument’s reliability based on its ability to yield the same output when repeatedly given a particular input. Despite its broad usage, little is understood about the feasibility of using consistency as a measure of worker reliability in crowdwork. In this paper, we explore the viability of measuring a worker’s reliability by their ability to conform to themselves. We introduce and describe Deja Vu, a mechanism for dynamically generating task queues with consistency probes to measure the consistency of workers who repeat the same task twice. We present a study that utilizes Deja Vu to examine how generic characteristics of the duplicate task — such as placement, difficulty, and transformation — affect a workers task consistency in the context of two unique object detection tasks. Our findings provide insight into the design and use of consistency-based reliability metrics.
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Andrea S. Meseguer, George M. Lobo, Josselin Cornuault, David Beerling, Brad R. Ruhfel, Charles C. Davis, Emmanuelle Jousselin, and Isabel Sanmartín. 10/24/2017. “Reconstructing deep-time paleoclimate legacies in the clusioid Malpighiales unveils their role in the evolution and extinction of the boreotropical flora.” Global Ecology and Biogeography, Pp. 1-24. Publisher's VersionAbstract

Aim: Since the Late Cretaceous, the Earth has gone through periods of climate change similar in scale and pace to the warming trend observed today in the Anthropocene. The impact of these ancient climatic events on the evolutionary trajectories of organisms provides clues on the organismal response to climate change, including extinction, migration or persistence. Here, we examine the evolutionary response to climate cooling/warming events of the clusioid families Calophyllaceae, Podostemaceae and Hypericaceae (CPH), and the genus Hypericum as test cases.

Location: Holarctic.

Time period: Late Cretaceous–Cenozoic

Major taxa studied: angiosperms

Methods: We use paleoclimate simulations, species distribution models and phylogenetic comparative approaches calibrated with fossils.

Results: Ancestral CPH lineages could have been distributed in the Holarctic 100 Ma, occupying tropical subhumid assemblages, a finding supported by the fossil record. Expansion to closed-canopy tropical rain forests occurred after 60 Ma, in the Cenozoic, in agreement with earlier ideas of a post-Cretaceous origin of current tropical rain forest. Cooling during this period triggered diversification declines on CPH tropical lineages, and was associated with a climatic shift towards temperate affinities in Hypericum. Hypericum subsequently migrated to tropical mountains where it encountered different temperate conditions than in the Holarctic.

Main Conclusions: We hypothesize that most clusioid CPH lineages failed to adapt to temperate regimes during periods of Cenozoic climate change, and thus went extinct in the Holarctic. In contrast, boreotropical descendants including Hypericum that underwent niche evolution demonstrated selective advantages as climates became colder. Our results points toward macroevolutionary trajectories involving the altering fates of closely related clades that adapt to periods of global climate change versus those that do not. Moreover, they suggest the hypothesis that potentially many clades, particularly inhabitants of boreotropical floras, were likely extirpated from the Holarctic and persist today (if at all) in more southern tropical locations.

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