Biological Collections For Understanding Biodiversity Research Articles

Biological collections for understanding biodiversity in the Anthropocene

Global change has become a central focus of modern biology. Yet, our knowledge of how anthropogenic drivers affect biodiversity and natural resources is limited by a lack of biological data spanning the Anthropocene. We propose that the hundreds of millions of plant, fungal and animal specimens deposited in natural history museums have the potential to transform the field of global change biology. We suggest that museum specimens are underused, particularly in ecological studies, given their capacity to reveal patterns that are not observable from other data sources. Increasingly, museum specimens are becoming mobilized online, providing unparalleled access to physiological, ecological and evolutionary data spanning decades and sometimes centuries. Here, we describe the diversity of collections data archived in museums and provide an overview of the diverse uses and applications of these data as discussed in the accompanying collection of papers within this theme issue. As these unparalleled resources are under threat owing to budget cuts and other institutional pressures, we aim to shed light on the unique discoveries that are possible in museums and, thus, the singular value of natural history collections in a period of rapid change.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

A novel proof of concept for capturing the diversity of endophytic fungi preserved in herbarium specimens.

Herbarium specimens represent important records of morphological and genetic diversity of plants that inform questions relevant to global change, including species distributions, phenology and functional traits. It is increasingly appreciated that plant microbiomes can influence these aspects of plant biology, but little is known regarding the historic distribution of microbes associated with plants collected in the pre-molecular age. If microbiomes can be observed reliably in herbarium specimens, researchers will gain a new lens with which to examine microbial ecology, evolution, species interactions. Here, we describe a method for accessing historical plant microbiomes from preserved herbarium specimens, providing a proof of concept using two plant taxa from the imperiled boreal biome (Andromeda polifolia and Ledum palustre subsp. groenlandicum, Ericaceae). We focus on fungal endophytes, which occur within symptomless plant tissues such as leaves. Through a three-part approach (i.e. culturing, cloning and next-generation amplicon sequencing via the Illumina MiSeq platform, with extensive controls), we examined endophyte communities in dried, pressed leaves that had been processed as regular herbarium specimens and stored at room temperature in a herbarium for four years. We retrieved only one endophyte in culture, but cloning and especially the MiSeq analysis revealed a rich community of foliar endophytes. The phylogenetic distribution and diversity of endophyte assemblages, especially among the Ascomycota, resemble endophyte communities from fresh plants collected in the boreal biome. We could distinguish communities of endophytes in each plant species and differentiate likely endophytes from fungi that could be surface contaminants. Taxa found by cloning were observed in the larger MiSeq dataset, but species richness was greater when subsets of the same tissues were evaluated with the MiSeq approach. Our findings provide a proof of concept for capturing endophyte DNA from herbarium specimens, supporting the importance of herbarium records as roadmaps for understanding the dynamics of plant-associated microbial biodiversity in the Anthropocene.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

Bookkeeping of insect herbivory trends in herbarium specimens of purple loosestrife (Lythrum salicaria).

The potential use of herbarium specimens to detect herbivory trends is enormous but largely untapped. The objective of this study was to reconstruct the long-term herbivory pressure on the Eurasian invasive plant, purple loosestrife (Lythrum salicaria), by evaluating leaf damage over 1323 specimens from southern Québec (Canada). The hypothesis tested is that that the prevalence of herbivory damage on purple loosestrife is low during the invasion phase and increases throughout the saturation phase. Historical trends suggest a gradual increase in hole feeding and margin feeding damage from 1883 to around 1940, followed by a period of relative stability. The percentage of specimens with window feeding damage did not begin to increase until the end of the twentieth century, from 3% (2-6%) in 1990 to 45% (14-81%) in 2015. Temporal changes in the frequency of window feeding damage support the hypothesis of an increasing herbivory pressure by recently introduced insects. This study shows that leaf damage made by insects introduced for the biocontrol of purple loosestrife, such as coleopterans of the Neogalerucella genus, can be assessed from voucher specimens. Herbaria are a rich source in information that can be used to answer questions related to plant-insect interactions in the context of biological invasions and biodiversity changes.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

Specimen-based analysis of morphology and the environment in ecologically dominant grasses: the power of the herbarium.

Herbaria contain a cumulative sample of the world's flora, assembled by thousands of people over centuries. To capitalize on this resource, we conducted a specimen-based analysis of a major clade in the grass tribe Andropogoneae, including the dominant species of the world's grasslands in the genera Andropogon, Schizachyrium, Hyparrhenia and several others. We imaged 186 of the 250 named species of the clade, georeferenced the specimens and extracted climatic variables for each. Using semi- and fully automated image analysis techniques, we extracted spikelet morphological characters and correlated these with environmental variables. We generated chloroplast genome sequences to correct for phylogenetic covariance and here present a new phylogeny for 81 of the species. We confirm and extend earlier studies to show that Andropogon and Schizachyrium are not monophyletic. In addition, we find all morphological and ecological characters are homoplasious but variable among clades. For example, sessile spikelet length is positively correlated with awn length when all accessions are considered, but when separated by clade, the relationship is positive for three sub-clades and negative for three others. Climate variables showed no correlation with morphological variation in the spikelet pair; only very weak effects of temperature and precipitation were detected on macrohair density.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

Historical collections as a tool for assessing the global pollination crisis.

There is increasing concern about the decline of pollinators worldwide. However, despite reports that pollinator declines are widespread, data are scarce and often geographically and taxonomically biased. These biases limit robust inference about any potential pollinator crisis. Non-structured and opportunistic historical specimen collection data provide the only source of historical information which can serve as a baseline for identifying pollinator declines. Specimens historically collected and preserved in museums not only provide information on where and when species were collected, but also contain other ecological information such as species interactions and morphological traits. Here, we provide a synthesis of how researchers have used historical data to identify long-term changes in biodiversity, species abundances, morphology and pollination services. Despite recent advances, we show that information on the status and trends of most pollinators is absent. We highlight opportunities and limitations to progress the assessment of pollinator declines globally. Finally, we demonstrate different approaches to analysing museum collection data using two contrasting case studies from distinct geographical regions (New Zealand and Spain) for which long-term pollinator declines have never been assessed. There is immense potential for museum specimens to play a central role in assessing the extent of the global pollination crisis.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

Fungarium specimens: a largely untapped source in global change biology and beyond.

For several hundred years, millions of fungal sporocarps have been collected and deposited in worldwide collections (fungaria) to support fungal taxonomy. Owing to large-scale digitization programs, metadata associated with the records are now becoming publicly available, including information on taxonomy, sampling location, collection date and habitat/substrate information. This metadata, as well as data extracted from the physical fungarium specimens themselves, such as DNA sequences and biochemical characteristics, provide a rich source of information not only for taxonomy but also for other lines of biological inquiry. Here, we highlight and discuss how this information can be used to investigate emerging topics in fungal global change biology and beyond. Fungarium data are a prime source of knowledge on fungal distributions and richness patterns, and for assessing red-listed and invasive species. Information on collection dates has been used to investigate shifts in fungal distributions as well as phenology of sporocarp emergence in response to climate change. In addition to providing material for taxonomy and systematics, DNA sequences derived from the physical specimens provide information about fungal demography, dispersal patterns, and are emerging as a source of genomic data. As DNA analysis technologies develop further, the importance of fungarium specimens as easily accessible sources of information will likely continue to grow.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

Fossil Atmospheres: a case study of citizen science in question-driven palaeontological research.

Palaeontologists increasingly use large datasets of observations collected from museum specimens to address broad-scale questions about evolution and ecology on geological timescales. One such question is whether information from fossil organisms can be used as a robust proxy for atmospheric carbon dioxide through time. Here, we present the citizen science branch of 'Fossil Atmospheres', a project designed to refine stomatal index of Ginkgo leaves as a palaeo-CO2 proxy by involving citizen scientists in data collection through the Zooniverse website. Citizen science helped to overcome a barrier presented by the time taken to count cells in Ginkgo samples; however, a new set of challenges arose as a result. A beta-testing phase with Zooniverse volunteers provided an opportunity to improve instructions to ensure high fidelity data. Exploration of citizen scientists' estimates shows that volunteer counts of stomata are accurate with respect to counts made by the project's lead scientist. However, counts of epidermal cells have a wide range, and mean values tend to underestimate expert counts. We demonstrate a variety of approaches to reducing the inaccuracy in the calculated stomatal index that this variation causes. Zooniverse serves as an ideal tool for collection of palaeontological data where the distribution of fossils would be impossible, but where specimens can be easily imaged. Such an approach facilitates the collection of a large palaeontological dataset, as well as providing an opportunity for citizens to engage with climate research.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

The history and impact of digitization and digital data mobilization on biodiversity research.

The first two decades of the twenty-first century have seen a rapid rise in the mobilization of digital biodiversity data. This has thrust natural history museums into the forefront of biodiversity research, underscoring their central role in the modern scientific enterprise. The advent of mobilization initiatives such as the United States National Science Foundation's Advancing Digitization of Biodiversity Collections (ADBC), Australia's Atlas of Living Australia (ALA), Mexico's National Commission for the Knowledge and Use of Biodiversity (CONABIO), Brazil's Centro de Referência em Informação (CRIA) and China's National Specimen Information Infrastructure (NSII) has led to a rapid rise in data aggregators and an exponential increase in digital data for scientific research and arguably provide the best evidence of where species live. The international Global Biodiversity Information Facility (GBIF) now serves about 131 million museum specimen records, and Integrated Digitized Biocollections (iDigBio) in the USA has amassed more than 115 million. These resources expose collections to a wider audience of researchers, provide the best biodiversity data in the modern era outside of nature itself and ensure the primacy of specimen-based research. Here, we provide a brief history of worldwide data mobilization, their impact on biodiversity research, challenges for ensuring data quality, their contribution to scientific publications and evidence of the rising profiles of natural history collections.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

Using insect natural history collections to study global change impacts: challenges and opportunities.

Over the past two decades, natural history collections (NHCs) have played an increasingly prominent role in global change research, but they have still greater potential, especially for the most diverse group of animals on Earth: insects. Here, we review the role of NHCs in advancing our understanding of the ecological and evolutionary responses of insects to recent global changes. Insect NHCs have helped document changes in insects' geographical distributions, phenology, phenotypic and genotypic traits over time periods up to a century. Recent work demonstrates the enormous potential of NHCs data for examining insect responses at multiple temporal, spatial and phylogenetic scales. Moving forward, insect NHCs offer unique opportunities to examine the morphological, chemical and genomic information in each specimen, thus advancing our understanding of the processes underlying species' ecological and evolutionary responses to rapid, widespread global changes.This article is part of the theme issue 'Biological collections for understanding biodiversity in the anthropocene'.

Museum specimens provide novel insights into changing plant-herbivore interactions.

Mounting evidence shows that species interactions may mediate how individual species respond to climate change. However, long-term anthropogenic effects on species interactions are poorly characterized owing to a lack of data. Insect herbivory is a major ecological process that represents the interaction between insect herbivores and their host plants, but historical data on insect damage to plants is particularly sparse. Here, we suggest that museum collections of insects and plants can fill key gaps in our knowledge on changing trophic interactions, including proximate mechanisms and the net outcomes of multiple global change drivers across diverse insect herbivore-plant associations. We outline theory on how global change may affect herbivores and their host plants and highlight the unique data that could be extracted from museum specimens to explore their shifting interactions. We aim to provide a framework for using museum specimens to explore how some of the most diverse co-evolved relationships are responding to climate and land use change.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

Facets of phylodiversity: evolutionary diversification, divergence and survival as conservation targets.

Biodiversity is often described as having multiple facets, including species richness, functional diversity and phylogenetic diversity. In this paper, we argue that phylogenetic diversity itself has three distinct facets-lineage diversification, character divergence and survival time-that can be quantified using distinct branch length metrics on an evolutionary tree. Each dimension is related to different processes of macroevolution, has different spatial patterns and is tied to distinct goals for conserving biodiversity and protecting its future resilience and evolutionary potential. We compared the landscapes identified as top conservation priorities by each of these three metrics in a conservation gap analysis for California, a world biodiversity hotspot, using herbarium data on the biogeography and evolutionary relationships of more than 5000 native plant species. Our analysis incorporated a novel continuous metric of current land protection status, fine-scale data on landscape intactness and an optimization algorithm used to identify complementary priority sites containing concentrations of taxa that are evolutionarily unique, vulnerable due to small range size and/or poorly protected across their ranges. Top conservation priorities included pockets of coastal and northern California that ranked highly for all three phylodiversity dimensions and for species richness, as well as sites uniquely identified by each metric whose value may depend on whether properties such as genetic divergence, high net diversification or independent survival experience are most desirable in an Anthropocene flora.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

The use and misuse of herbarium specimens in evaluating plant extinction risks.

Herbarium specimens provide verifiable and citable evidence of the occurrence of particular plants at particular points in space and time, and are vital resources for assessing extinction risk in the tropics, where plant diversity and threats to plants are greatest. We reviewed approaches to assessing extinction risk in response to the Convention on Biological Diversity's Global Strategy for Plant Conservation Target 2: an assessment of the conservation status of all known plant species by 2020. We tested five alternative approaches, using herbarium-derived data for trees, shrubs and herbs in five different plant groups from temperate and tropical regions. All species were previously fully assessed for the IUCN Red List. We found significant variation in the accuracy with which different approaches classified species as threatened or not threatened. Accuracy was highest for the machine learning model (90%) but the least data-intensive approach also performed well (82%). Despite concerns about spatial, temporal and taxonomic biases and uncertainties in herbarium data, when specimens represent the best available evidence for particular species, their use as a basis for extinction risk assessment is appropriate, necessary and urgent. Resourcing herbaria to maintain, increase and disseminate their specimen data is essential to guide and focus conservation action.This article is part of the theme issue ‘Biological collections for understanding biodiversity in the Anthropocene’.

Herbarium specimens reveal substantial and unexpected variation in phenological sensitivity across the eastern United States.

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'.

Botanic gardens are an untapped resource for studying the functional ecology of tropical plants.

Functional traits are increasingly used to understand the ecology of plants and to predict their responses to global changes. Unfortunately, trait data are unavailable for the majority of plant species. The lack of trait data is especially prevalent for hard-to-measure traits and for tropical plant species, potentially owing to the many inherent difficulties of working with species in remote, hyperdiverse rainforest systems. The living collections of botanic gardens provide convenient access to large numbers of tropical plant species and can potentially be used to quickly augment trait databases and advance our understanding of species' responses to climate change. In this review, we quantitatively assess the availability of trait data for tropical versus temperate species, the diversity of species available for sampling in several exemplar tropical botanic gardens and the validity of garden-based leaf and root trait measurements. Our analyses support the contention that the living collections of botanic gardens are a valuable scientific resource that can contribute significantly to research on plant functional ecology and conservation.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

Museum specimens of terrestrial vertebrates are sensitive indicators of environmental change in the Anthropocene.

Natural history museums and the specimen collections they curate are vital scientific infrastructure, a fact as true today as it was when biologists began collecting and preserving specimens over 200 years ago. The importance of museum specimens in studies of taxonomy, systematics, ecology and evolutionary biology is evidenced by a rich and abundant literature, yet creative and novel uses of specimens are constantly broadening the impact of natural history collections on biodiversity science and global sustainability. Excellent examples of the critical importance of specimens come from their use in documenting the consequences of environmental change, which is particularly relevant considering the alarming rate at which we now modify our planet in the Anthropocene. In this review, we highlight the important role of bird, mammal and amphibian specimens in documenting the Anthropocene and provide examples that underscore the need for continued collection of museum specimens.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

Using museum specimens to track morphological shifts through climate change.

Museum specimens offer a largely untapped resource for detecting morphological shifts in response to climate change. However, morphological shifts can be obscured by shifts in phenology or distribution or sampling biases. Additionally, interpreting phenotypic shifts requires distinguishing whether they result from plastic or genetic changes. Previous studies using collections have documented consistent historical size changes, but the limited studies of other morphological traits have often failed to support, or even test, hypotheses. We explore the potential of collections by investigating shifts in the functionally significant coloration of a montane butterfly, Colias meadii, over the past 60 years within three North American geographical regions. We find declines in ventral wing melanism, which correspond to reduced absorption of solar radiation and thus reduced risk of overheating, in two regions. However, contrary to expected responses to climate warming, we find melanism increases in the most thoroughly sampled region. Relationships among temperature, phenology and morphology vary across years and complicate the distinction between plastic and genetic responses. Differences in these relationships may account for the differing morphological shifts among regions. Our findings highlight the promise of using museum specimens to test mechanistic hypotheses for shifts in functional traits, which is essential for deciphering interacting responses to climate change.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.