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Title: Modern approaches for leveraging biodiversity collections to understand change in plant-insect interactions
Research on plant-pollinator interactions requires a diversity of perspectives and approaches, and documenting changing pollinator-plant interactions due to declining insect diversity and climate change is especially challenging. Natural history collections are increasingly important for such research and can provide ecological information across broad spatial and temporal scales. Here, we describe novel approaches that integrate museum specimens from insect and plant collections with field observations to quantify pollen networks over large spatial and temporal gradients. We present methodological strategies for evaluating insect-pollen network parameters based on pollen collected from museum insect specimens. These methods provide insight into spatial and temporal variation in pollen-insect interactions and complement other approaches to studying pollination, such as pollinator observation networks and flower enclosure experiments. We present example data from butterfly pollen networks over the past century in the Great Basin Desert and Sierra Nevada Mountains, United States. Complementary to these approaches, we describe rapid pollen identification methods that can increase speed and accuracy of taxonomic determinations, using pollen grains collected from herbarium specimens. As an example, we describe a convolutional neural network (CNN) to automate identification of pollen. We extracted images of pollen grains from 21 common species from herbarium specimens at the University of Nevada Reno (RENO). The CNN model achieved exceptional accuracy of identification, with a correct classification rate of 98.8%. These and similar approaches can transform the way we estimate pollination network parameters and greatly change inferences from existing networks, which have exploded over the past few decades. These techniques also allow us to address critical ecological questions related to mutualistic networks, community ecology, and conservation biology. Museum collections remain a bountiful source of data for biodiversity science and understanding global change.  more » « less
Award ID(s):
2114942 2114793
NSF-PAR ID:
10400156
Author(s) / Creator(s):
; ; ; ; ; ; ;
Date Published:
Journal Name:
Frontiers in Ecology and Evolution
Volume:
10
ISSN:
2296-701X
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
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  1. Abstract

    Pollen is used to investigate a diverse range of ecological problems, from identifying plant–pollinator relationships to tracking flowering phenology. Pollen types are identified according to a set of distinctive morphological characters which are understood to capture taxonomic differences and phylogenetic relationships among taxa. However, categorizing morphological variation among hyperdiverse pollen samples represents a challenge even for an expert analyst.

    We present an automated workflow for pollen analysis, from the automated scanning of pollen sample slides to the automated detection and identification of pollen taxa using convolutional neural networks (CNNs). We analysed aerial pollen samples from lowland Panama and used a microscope slide scanner to capture three‐dimensional representations of 150 sample slides. These pollen sample images were annotated by an expert using a virtual microscope. Metadata were digitally recorded for ~100 pollen grains per slide, including location, identification and the analyst's confidence of the given identification. We used these annotated images to train and test our detection and classification CNN models. Our approach is two‐part. We first compared three methods for training CNN models to detect pollen grains on a palynological slide. We next investigated approaches to training CNN models for pollen identification.

    Because the diversity of pollen taxa in environmental and palaeontological samples follows a long‐tailed distribution, we experimented with methods for addressing imbalanced representation using our most abundant 46 taxa. We found that properly weighting pollen taxa in our training objective functions yielded improved accuracy for individual taxa. Our average accuracy for the 46‐way classification problem was 82.3%. We achieved 89.5% accuracy for our 25 most abundant taxa.

    Pollen represents a challenging visual classification problem that can serve as a model for other areas of biology that rely on visual identification. Our results add to the body of research demonstrating the potential for a fully automated pollen classification system for environmental and palaeontological samples. Slide imaging, pollen detection and specimen identification can be automated to produce a streamlined workflow.

     
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  2. PLEASE CONTACT AUTHORS IF YOU CONTRIBUTE AND WOULD LIKE TO BE LISTED AS A CO-AUTHOR. (this message will be removed some time weeks/months after the first publication)

    Terrestrial Parasite Tracker indexed biotic interactions and review summary.

    The Terrestrial Parasite Tracker (TPT) project began in 2019 and is funded by the National Science foundation to mobilize data from vector and ectoparasite collections to data aggregators (e.g., iDigBio, GBIF) to help build a comprehensive picture of arthropod host-association evolution, distributions, and the ecological interactions of disease vectors which will assist scientists, educators, land managers, and policy makers. Arthropod parasites often are important to human and wildlife health and safety as vectors of pathogens, and it is critical to digitize these specimens so that they, and their biotic interaction data, will be available to help understand and predict the spread of human and wildlife disease.

    This data publication contains versioned TPT associated datasets and related data products that were tracked, reviewed and indexed by Global Biotic Interactions (GloBI) and associated tools. GloBI provides open access to finding species interaction data (e.g., predator-prey, pollinator-plant, pathogen-host, parasite-host) by combining existing open datasets using open source software.

    If you have questions or comments about this publication, please open an issue at https://github.com/ParasiteTracker/tpt-reporting or contact the authors by email.

    Funding:
    The creation of this archive was made possible by the National Science Foundation award "Collaborative Research: Digitization TCN: Digitizing collections to trace parasite-host associations and predict the spread of vector-borne disease," Award numbers DBI:1901932 and DBI:1901926

    References:
    Jorrit H. Poelen, James D. Simons and Chris J. Mungall. (2014). Global Biotic Interactions: An open infrastructure to share and analyze species-interaction datasets. Ecological Informatics. https://doi.org/10.1016/j.ecoinf.2014.08.005.

    GloBI Data Review Report

    Datasets under review:
     - University of Michigan Museum of Zoology Insect Division. Full Database Export 2020-11-20 provided by Erika Tucker and Barry Oconner. accessed via https://github.com/EMTuckerLabUMMZ/ummzi/archive/6731357a377e9c2748fc931faa2ff3dc0ce3ea7a.zip on 2022-06-24T14:02:48.801Z
     - Academy of Natural Sciences Entomology Collection for the Parasite Tracker Project accessed via https://github.com/globalbioticinteractions/ansp-para/archive/5e6592ad09ec89ba7958266ad71ec9d5d21d1a44.zip on 2022-06-24T14:04:22.091Z
     - Bernice Pauahi Bishop Museum, J. Linsley Gressitt Center for Research in Entomology accessed via https://github.com/globalbioticinteractions/bpbm-ent/archive/c085398dddd36f8a1169b9cf57de2a572229341b.zip on 2022-06-24T14:04:37.692Z
     - Texas A&M University, Biodiversity Teaching and Research Collections accessed via https://github.com/globalbioticinteractions/brtc-para/archive/f0a718145b05ed484c4d88947ff712d5f6395446.zip on 2022-06-24T14:06:40.154Z
     - Brigham Young University Arthropod Museum accessed via https://github.com/globalbioticinteractions/byu-byuc/archive/4a609ac6a9a03425e2720b6cdebca6438488f029.zip on 2022-06-24T14:06:51.420Z
     - California Academy of Sciences Entomology accessed via https://github.com/globalbioticinteractions/cas-ent/archive/562aea232ec74ab615f771239451e57b057dc7c0.zip on 2022-06-24T14:07:16.371Z
     - Clemson University Arthropod Collection accessed via https://github.com/globalbioticinteractions/cu-cuac/archive/6cdcbbaa4f7cec8e1eac705be3a999bc5259e00f.zip on 2022-06-24T14:07:40.925Z
     - Denver Museum of Nature and Science (DMNS) Parasite specimens (DMNS:Para) accessed via https://github.com/globalbioticinteractions/dmns-para/archive/a037beb816226eb8196533489ee5f98a6dfda452.zip on 2022-06-24T14:08:00.730Z
     - Field Museum of Natural History IPT accessed via https://github.com/globalbioticinteractions/fmnh/archive/6bfc1b7e46140e93f5561c4e837826204adb3c2f.zip on 2022-06-24T14:18:51.995Z
     - Illinois Natural History Survey Insect Collection accessed via https://github.com/globalbioticinteractions/inhs-insects/archive/38692496f590577074c7cecf8ea37f85d0594ae1.zip on 2022-06-24T14:19:37.563Z
     - UMSP / University of Minnesota / University of Minnesota Insect Collection accessed via https://github.com/globalbioticinteractions/min-umsp/archive/3f1b9d32f947dcb80b9aaab50523e097f0e8776e.zip on 2022-06-24T14:20:27.232Z
     - Milwaukee Public Museum Biological Collections Data Portal accessed via https://github.com/globalbioticinteractions/mpm/archive/9f44e99c49ec5aba3f8592cfced07c38d3223dcd.zip on 2022-06-24T14:20:46.185Z
     - Museum for Southern Biology (MSB) Parasite Collection accessed via https://github.com/globalbioticinteractions/msb-para/archive/178a0b7aa0a8e14b3fe953e770703fe331eadacc.zip on 2022-06-24T15:16:07.223Z
     - The Albert J. Cook Arthropod Research Collection accessed via https://github.com/globalbioticinteractions/msu-msuc/archive/38960906380443bd8108c9e44aeff4590d8d0b50.zip on 2022-06-24T16:09:40.702Z
     - Ohio State University Acarology Laboratory accessed via https://github.com/globalbioticinteractions/osal-ar/archive/876269d66a6a94175dbb6b9a604897f8032b93dd.zip on 2022-06-24T16:10:00.281Z
     - Frost Entomological Museum, Pennsylvania State University accessed via https://github.com/globalbioticinteractions/psuc-ento/archive/30b1f96619a6e9f10da18b42fb93ff22cc4f72e2.zip on 2022-06-24T16:10:07.741Z
     - Purdue Entomological Research Collection accessed via https://github.com/globalbioticinteractions/pu-perc/archive/e0909a7ca0a8df5effccb288ba64b28141e388ba.zip on 2022-06-24T16:10:26.654Z
     - Texas A&M University Insect Collection accessed via https://github.com/globalbioticinteractions/tamuic-ent/archive/f261a8c192021408da67c39626a4aac56e3bac41.zip on 2022-06-24T16:10:58.496Z
     - University of California Santa Barbara Invertebrate Zoology Collection accessed via https://github.com/globalbioticinteractions/ucsb-izc/archive/825678ad02df93f6d4469f9d8b7cc30151b9aa45.zip on 2022-06-24T16:12:29.854Z
     - University of Hawaii Insect Museum accessed via https://github.com/globalbioticinteractions/uhim/archive/53fa790309e48f25685e41ded78ce6a51bafde76.zip on 2022-06-24T16:12:41.408Z
     - University of New Hampshire Collection of Insects and other Arthropods UNHC-UNHC accessed via https://github.com/globalbioticinteractions/unhc/archive/f72575a72edda8a4e6126de79b4681b25593d434.zip on 2022-06-24T16:12:59.500Z
     - Scott L. Gardner and Gabor R. Racz (2021). University of Nebraska State Museum - Parasitology. Harold W. Manter Laboratory of Parasitology. University of Nebraska State Museum. accessed via https://github.com/globalbioticinteractions/unl-nsm/archive/6bcd8aec22e4309b7f4e8be1afe8191d391e73c6.zip on 2022-06-24T16:13:06.914Z
     - Data were obtained from specimens belonging to the United States National Museum of Natural History (USNM), Smithsonian Institution, Washington DC and digitized by the Walter Reed Biosystematics Unit (WRBU). accessed via https://github.com/globalbioticinteractions/usnmentflea/archive/ce5cb1ed2bbc13ee10062b6f75a158fd465ce9bb.zip on 2022-06-24T16:13:38.013Z
     - US National Museum of Natural History Ixodes Records accessed via https://github.com/globalbioticinteractions/usnm-ixodes/archive/c5fcd5f34ce412002783544afb628a33db7f47a6.zip on 2022-06-24T16:13:45.666Z
     - Price Institute of Parasite Research, School of Biological Sciences, University of Utah accessed via https://github.com/globalbioticinteractions/utah-piper/archive/43da8db550b5776c1e3d17803831c696fe9b8285.zip on 2022-06-24T16:13:54.724Z
     - University of Wisconsin Stevens Point, Stephen J. Taft Parasitological Collection accessed via https://github.com/globalbioticinteractions/uwsp-para/archive/f9d0d52cd671731c7f002325e84187979bca4a5b.zip on 2022-06-24T16:14:04.745Z
     - Giraldo-Calderón, G. I., Emrich, S. J., MacCallum, R. M., Maslen, G., Dialynas, E., Topalis, P., … Lawson, D. (2015). VectorBase: an updated bioinformatics resource for invertebrate vectors and other organisms related with human diseases. Nucleic acids research, 43(Database issue), D707–D713. doi:10.1093/nar/gku1117. accessed via https://github.com/globalbioticinteractions/vectorbase/archive/00d6285cd4e9f4edd18cb2778624ab31b34b23b8.zip on 2022-06-24T16:14:11.965Z
     - WIRC / University of Wisconsin Madison WIS-IH / Wisconsin Insect Research Collection accessed via https://github.com/globalbioticinteractions/wis-ih-wirc/archive/34162b86c0ade4b493471543231ae017cc84816e.zip on 2022-06-24T16:14:29.743Z
     - Yale University Peabody Museum Collections Data Portal accessed via https://github.com/globalbioticinteractions/yale-peabody/archive/43be869f17749d71d26fc820c8bd931d6149fe8e.zip on 2022-06-24T16:23:29.289Z

    Generated on:
    2022-06-24

    by:
    GloBI's Elton 0.12.4 
    (see https://github.com/globalbioticinteractions/elton).

    Note that all files ending with .tsv are files formatted 
    as UTF8 encoded tab-separated values files.

    https://www.iana.org/assignments/media-types/text/tab-separated-values


    Included in this review archive are:

    README:
      This file.

    review_summary.tsv:
      Summary across all reviewed collections of total number of distinct review comments.

    review_summary_by_collection.tsv:
      Summary by reviewed collection of total number of distinct review comments.

    indexed_interactions_by_collection.tsv: 
      Summary of number of indexed interaction records by institutionCode and collectionCode.

    review_comments.tsv.gz:
      All review comments by collection.

    indexed_interactions_full.tsv.gz:
      All indexed interactions for all reviewed collections.

    indexed_interactions_simple.tsv.gz:
      All indexed interactions for all reviewed collections selecting only sourceInstitutionCode, sourceCollectionCode, sourceCatalogNumber, sourceTaxonName, interactionTypeName and targetTaxonName.

    datasets_under_review.tsv:
      Details on the datasets under review.

    elton.jar: 
      Program used to update datasets and generate the review reports and associated indexed interactions.

    datasets.zip:
      Source datasets used by elton.jar in process of executing the generate_report.sh script.

    generate_report.sh:
      Program used to generate the report

    generate_report.log:
      Log file generated as part of running the generate_report.sh script
     

     
    more » « less
  3. Abstract

    The widespread digitization of natural history collections, combined with novel tools and approaches is revolutionizing biodiversity science. The ‘extended specimen’ concept advocates a more holistic approach in which a specimen is framed as a diverse stream of interconnected data. Herbarium specimens that by their very nature capture multispecies relationships, such as certain parasites, fungi and lichens, hold great potential to provide a broader and more integrative view of the ecology and evolution of symbiotic interactions. This particularly applies to parasite–host associations, which owing to their interconnectedness are especially vulnerable to global environmental change.

    Here, we present an overview of how parasitic flowering plants is represented in herbarium collections. We then discuss the variety of data that can be gathered from parasitic plant specimens, and how they can be used to understand global change impacts at multiple scales. Finally, we review best practices for sampling parasitic plants in the field, and subsequently preparing and digitizing these specimens.

    Plant parasitism has evolved 12 times within angiosperms, and similar to other plant taxa, herbarium collections represent the foundation for analysing key aspects of their ecology and evolution. Yet these collections hold far greater potential. Data and metadata obtained from parasitic plant specimens can inform analyses of co‐distribution patterns, changes in eco‐physiology and species plasticity spanning temporal and spatial scales, chemical ecology of tripartite interactions (e.g. host–parasite–herbivore), and molecular data critical for species conservation. Moreover, owing to the historic nature and sheer size of global herbarium collections, these data provide the spatiotemporal breadth essential for investigating organismal response to global change.

    Parasitic plant specimens are primed to serve as ideal examples of extended specimen concept and help motivate the next generation of creative and impactful collection‐based science. Continued digitization efforts and improved curatorial practices will contribute to opening these specimens to a broader audience, allowing integrative research spanning multiple domains and offering novel opportunities for education.

     
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  4. Natalie Cooper (Ed.)
    1. Historical datasets can establish a critical baseline of plant–animal interactions for understanding contemporary interactions in the context of global change. Pollen is often incidentally preserved on animals in natural history collections. Techniques for removing pollen from insects have largely been developed for fresh insect specimens or historical specimens with large amounts of pollen on specialized structures. However, many key pollinating insects do not have these specialized structures and thus, there is a need for a method to extract pollen from these small and fragile insects. 2. Here, we propose a precision glycerine jelly swab tool to allow for the precise removal of pollen from old, small and fragile insect specimens. We use this tool to remove pollen from five families of insects collected in the late 1970s. Additionally, we compare our method with four previously published techniques for removing pollen from pinned contemporary specimens. 3. We show the functionality of the precision glycerine jelly swab for removing small quantities of pollen across insect families. We found that across the five methods, all removed pollen; yet, it was clear that some are better suited for fragile specimens. In particular, the traditional glycerine jelly swab and the precision glycerine jelly swabs both performed well for removing pollen from bee faces. The shaking wash resulted in specimen fracture and residue left behind, the ethanol rinses left setae matted, and the glycerol swabbing left residue on the specimen. Additionally, we present photographs documenting the effects of these methods on pinned honey bee specimens. 4. The precision glycerine jelly swab opens up opportunities to sample pollen from a variety of insects in natural history collections. These pollen samples can be incorporated into downstream analyses for pollen identification either via mi-croscopy or DNA sequencing, and the resulting plant–insect interaction data can establish historical baselines for contemporary comparison. Beyond our ap-plication of this method to pollen on insects, this precision glycerine jelly swab tool could be used to explore pollen placement specialization or to sample bryo-phyte, fungal and tree fern spores dispersing on animals. 
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  5. Abstract

    Determining how pollinators visit plants vs. how they carry and transfer pollen is an ongoing project in pollination ecology. The current tools for identifying the pollens that bees carry have different strengths and weaknesses when used for ecological inference. In this study we use three methods to better understand a system of congeneric, coflowering plants in the genusClarkiaand their bee pollinators: observations of plant–pollinator contact in the field, and two different molecular methods to estimate the relative abundance of eachClarkiapollen in samples collected from pollinators. We use these methods to investigate if observations of plant–pollinator contact in the field correspond to the pollen bees carry; if individual bees carryClarkiapollens in predictable ways, based on previous knowledge of their foraging behaviors; and how the three approaches differ for understanding plant–pollinator interactions. We find that observations of plant–pollinator contact are generally predictive of the pollens that bees carry while foraging, and network topologies using the three different methods are statistically indistinguishable from each other. Results from molecular pollen analysis also show that while bees can carry multiple species ofClarkiaat the same time, they often carry one species of pollen. Our work contributes to the growing body of literature aimed at resolving how pollinators use floral resources. We suggest our novel relative amplicon quantification method as another tool in the developing molecular ecology and pollination biology toolbox.

     
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