Is the world wormier than it used to be? We'll never know without natural history collections.

Many disease ecologists and conservation biologists believe that the world is wormier than it used to be-that is, that parasites are increasing in abundance through time. This argument is intuitively appealing. Ecologists typically see parasitic infections, through their association with disease, as a negative endpoint, and are accustomed to attributing negative outcomes to human interference in the environment, so it slots neatly into our worldview that habitat destruction, biodiversity loss and climate change should have the collateral consequence of causing outbreaks of parasites. But surprisingly, the hypothesis that parasites are increasing in abundance through time remains entirely untested for the vast majority of wildlife parasite species. Historical data on parasites are nearly impossible to find, which leaves no baseline against which to compare contemporary parasite burdens. If we want to know whether the world is wormier than it used to be, there is only one major research avenue that will lead to an answer: parasitological examination of specimens preserved in natural history collections. Recent advances demonstrate that, for many specimen types, it is possible to extract reliable data on parasite presence and abundance. There are millions of suitable specimens that exist in collections around the world. When paired with contemporaneous environmental data, these parasitological data could even point to potential drivers of change in parasite abundance, including climate, pollution or host density change. We explain how to use preserved specimens to address pressing questions in parasite ecology, give a few key examples of how collections-based parasite ecology can resolve these questions, identify some pitfalls and workarounds, and suggest promising areas for research. Natural history specimens are 'parasite time capsules' that give ecologists the opportunity to test whether infectious disease is on the rise and to identify what forces might be driving these changes over time. This approach will facilitate major advances in a new sub-discipline: the historical ecology of parasitism.

Wildlife collection for scientific purposes.

Illegal transfer of wildlife has 2 main purposes: trade and scientific research. Trade is the most common, whereas scientific research is much less common and unprofitable, yet still important. Biopiracy in science is often neglected despite that many researchers encounter it during their careers. The use of illegally acquired specimens is detected in different research fields, from scientists bioprospecting for new pharmacological substances, to taxonomists working on natural history collections, to researchers working in zoos, aquariums, and botanical gardens. The practice can be due to a lack of knowledge about the permit requirements in different countries or, probably most often, to the generally high level of bureaucracy associated with rule compliance. Significant regulatory filters to avoid biopiracy can be provided by different stakeholders. Natural history collection hosts should adopt strict codes of conduct; editors of scientific publications should require authors to declare that all studied specimens were acquired legally and to cite museum catalog numbers as guarantee of best practices. Scientific societies should actively encourage publication in peer-reviewed journals of work in which specimens collected from the wild were used. The International Commission on Zoological Nomenclature could require newly designated types based on recently collected specimens to be accompanied by statements of deposition in recognized scientific or educational institutions. We also propose the creation of an online platform that gathers information about environmental regulations and permits required for scientific activities in different countries and respective responsible governmental agencies and the simplification of the bureaucracy related to regulating scientific activities. This would make regulations more agile and easier to comply with. The global biodiversity crisis means data need to be collected ever faster, but biopiracy is not the answer and undermines the credibility of science and researchers. It is critical to find a modus vivendi that promotes compliance with regulations and scientific progress.

Recolección de Fauna con Motivos Científicos Resumen El traslado ilegal de fauna tiene dos objetivos principales: el mercado y la investigación científica. El mercado es el más común, a la vez que la investigación científica es mucho menos común y poco rentable, pero de igual manera importante. La biopiratería en la ciencia comúnmente se ignora a pesar de que muchos investigadores se encuentran con ella a lo largo de sus carreras. El uso de especímenes adquiridos ilegalmente está detectado en diferentes campos de investigación, desde los científicos que realizan bio-exploraciones en búsqueda de nuevas sustancias farmacológicas, pasando por los taxónomos que trabajan en las colecciones de historia natural, hasta los investigadores que trabajan en zoológicos, acuarios y jardines botánicos. Esta práctica puede deberse a la falta de conocimiento sobre los requerimientos de los permisos en diferentes países o, probablemente con mayor frecuencia, a la alta cantidad de burocracia asociada con el seguimiento de las reglas. Los diferentes actores pueden proporcionar filtros regulatorios importantes para evitar la biopiratería. Los dueños de las colecciones de historia natural deberían adoptar códigos estrictos de conducta; los editores de las publicaciones científicas deberían exigirle a los autores que declaren que todos los especímenes estudiados fueron adquiridos legalmente y también que citen el número de catálogo del espécimen como garantías de mejores prácticas. Las sociedades científicas deberían promover activamente la publicación en revistas revisadas por pares de los trabajos en los que se usaron especímenes recolectados en su hábitat natural. La Comisión Internacional sobre la Nomenclatura Zoológica podría requerir que la designación reciente de tipos basada en especímenes recolectados recientemente esté acompañada por declaraciones de deposición en instituciones científicas o educativas reconocidas. También proponemos la creación de una plataforma en línea que recopile la información sobre las regulaciones ambientales y los permisos requeridos para la actividad científica en diferentes países, así como las agencias gubernamentales responsables y la simplificación de la burocracia relacionada con la regulación de las actividades científicas. Ésto haría que las regulaciones sean más ágiles y su cumplimiento más fácil. La crisis mundial de biodiversidad implica que los datos necesitan ser recolectados con mayor velocidad que nunca, pero la biopiratería no es la respuesta, además de que desvirtúa la credibilidad de la ciencia y de los investigadores. Es muy importante que encontremos un modus vivendi que promueva un acuerdo entre las reglas y el progreso científico.

Small herbaria contribute unique biogeographic records to county, locality, and temporal scales.

PREMISE: With digitization and data sharing initiatives underway over the last 15 years, an important need has been prioritizing specimens to digitize. Because duplicate specimens are shared among herbaria in exchange and gift programs, we investigated the extent to which unique biogeographic data are held in small herbaria vs. these data being redundant with those held by larger institutions. We evaluated the unique specimen contributions that small herbaria make to biogeographic understanding at county, locality, and temporal scales. METHODS: We sampled herbarium specimens of 40 plant taxa from each of eight states of the United States of America in four broad status categories: extremely rare, very rare, common native, and introduced. We gathered geographic information from specimens held by large (≥100,000 specimens) and small (<100,000 specimens) herbaria. We built generalized linear mixed models to assess which features of the collections may best predict unique contributions of herbaria and used an Akaike information criterion-based information-theoretic approach for our model selection to choose the best model for each scale. RESULTS: Small herbaria contributed unique specimens at all scales in proportion with their contribution of specimens to our data set. The best models for all scales were the full models that included the factors of species status and herbarium size when accounting for state as a random variable. CONCLUSIONS: We demonstrated that small herbaria contribute unique information for research. It is clear that unique contributions cannot be predicted based on herbarium size alone. We must prioritize digitization and data sharing from herbaria of all sizes.

Disseminating "hidden" scientific collections: the medium and large-sized terrestrial mammals at the Museo di Anatomia Comparata "Giovanni Battista Grassi", Roma, Italy.

The dissemination of specimen data in scientific collections is a crucial step in making them available to the scientific community. However, even today, especially in some countries, little or nothing is known about the contents of the naturalistic collections of some museums. This is regrettable, especially in cases where the collections include historic specimens and endangered species. The Museum of Comparative Anatomy "Giovanni Battista Grassi", situated in Rome, Italy, houses historical anatomical and didactic collections, with specimens gathered from 1600s and almost worldwide. The collection holds 444 specimens of medium and large-sized terrestrial mammals, comprising 25 fossils, 40 skins, 186 skulls, 70 skeletons and 123 anatomical pieces, representing 63% of recent mammal orders, mainly from localities of Africa and Europe. A list of this material, indexed by the orders and families, is provided, as well as comments on the conservation status of the species. Remarkable data are summarised, including new data on a hippopotamus specimen from an extinct population and the record of three rhinoceros species from 1600s. Besides comparative anatomical studies, the Museum of Comparative Anatomy of Sapienza University emerges as a source of important material for biodiversity genomics.

Shall we promote natural history collection today?-Answered by reviewing Ernest Henry Wilson's plant collection process in China.

Plant diversity exploration needs to be accelerated because many species will go extinct before their discovery and description, and many species-rich regions remain poorly studied. However, most contemporary plant collections prefer to focus on a specific group, which hinders the exploration and conservation of plant diversity. Therefore, we need an alternative approach to the dilemma at hand. The comprehensive Natural History Collection (NHC), which existed throughout the pinnacle of biodiversity exploration in the 20th century could be considered. We explore Ernest Henry Wilson's (one of the most successful naturalists in the 20th) plant collections in China as a case to illustrate the advantages of NHC and discuss whether NHC deserves to be promoted again today. From multiple sources, we gathered 19,218 available specimen records of 11,884 collecting numbers assigned and analyzed the collected species, the collection's nature, and restored four routes of his explorations. Results reveal that Wilson's specimens were collected from 28 prefecture-level cities and 38 county-level regions of 7 provinces or municipalities, they belong to 200 families, 1046 genera, 3794 species, and 342 infraspecific taxa, approximately 41 %, 22 %, 10 %, 5 % of Chinese plant families, genera, species, and infraspecific taxa respectively. The Wilson case study shows that NHC is particularly effective in emphasizing species discovery and conservation, recording ecological information, understanding a region's flora, and developing landscape applications. Therefore, we strongly advocate for the expansion of natural history collections in species-rich regions. Furthermore, we recommend the employment of specialized collectors, the enlistment of international cooperation, and the standardization of guidelines for future NHCs.

Developing the Protocol Infrastructure for DNA Sequencing Natural History Collections.

Intentionally preserved biological material in natural history collections represents a vast repository of biodiversity. Advances in laboratory and sequencing technologies have made these specimens increasingly accessible for genomic analyses, offering a window into the genetic past of species and often permitting access to information that can no longer be sampled in the wild. Due to their age, preparation and storage conditions, DNA retrieved from museum and herbarium specimens is often poor in yield, heavily fragmented and biochemically modified. This not only poses methodological challenges in recovering nucleotide sequences, but also makes such investigations susceptible to environmental and laboratory contamination. In this paper, we review the practical challenges associated with making the recovery of DNA sequence data from museum collections more routine. We first review key operational principles and issues to address, to guide the decision-making process and dialogue between researchers and curators about when and how to sample museum specimens for genomic analyses. We then outline the range of steps that can be taken to reduce the likelihood of contamination including laboratory set-ups, workflows and working practices. We finish by presenting a series of case studies, each focusing on protocol practicalities for the application of different mainstream methodologies to museum specimens including: (i) shotgun sequencing of insect mitogenomes, (ii) whole genome sequencing of insects, (iii) genome skimming to recover plant plastid genomes from herbarium specimens, (iv) target capture of multi-locus nuclear sequences from herbarium specimens, (v) RAD-sequencing of bird specimens and (vi) shotgun sequencing of ancient bovid bone samples.

Enhancing DNA barcode reference libraries by harvesting terrestrial arthropods at the Smithsonian's National Museum of Natural History.

The use of DNA barcoding has revolutionised biodiversity science, but its application depends on the existence of comprehensive and reliable reference libraries. For many poorly known taxa, such reference sequences are missing even at higher-level taxonomic scales. We harvested the collections of the Smithsonian's National Museum of Natural History (USNM) to generate DNA barcoding sequences for genera of terrestrial arthropods previously not recorded in one or more major public sequence databases. Our workflow used a mix of Sanger and Next-Generation Sequencing (NGS) approaches to maximise sequence recovery while ensuring affordable cost. In total, COI sequences were obtained for 5,686 specimens belonging to 3,737 determined species in 3,886 genera and 205 families distributed in 137 countries. Success rates varied widely according to collection data and focal taxon. NGS helped recover sequences of specimens that failed a previous run of Sanger sequencing. Success rates and the optimal balance between Sanger and NGS are the most important drivers to maximise output and minimise cost in future projects. The corresponding sequence and taxonomic data can be accessed through the Barcode of Life Data System, GenBank, the Global Biodiversity Information Facility, the Global Genome Biodiversity Network Data Portal and the NMNH data portal.

Can Artificial Intelligence Help in the Study of Vegetative Growth Patterns from Herbarium Collections? An Evaluation of the Tropical Flora of the French Guiana Forest.

A better knowledge of tree vegetative growth phenology and its relationship to environmental variables is crucial to understanding forest growth dynamics and how climate change may affect it. Less studied than reproductive structures, vegetative growth phenology focuses primarily on the analysis of growing shoots, from buds to leaf fall. In temperate regions, low winter temperatures impose a cessation of vegetative growth shoots and lead to a well-known annual growth cycle pattern for most species. The humid tropics, on the other hand, have less seasonality and contain many more tree species, leading to a diversity of patterns that is still poorly known and understood. The work in this study aims to advance knowledge in this area, focusing specifically on herbarium scans, as herbariums offer the promise of tracking phenology over long periods of time. However, such a study requires a large number of shoots to be able to draw statistically relevant conclusions. We propose to investigate the extent to which the use of deep learning can help detect and type-classify these relatively rare vegetative structures in herbarium collections. Our results demonstrate the relevance of using herbarium data in vegetative phenology research as well as the potential of deep learning approaches for growing shoot detection.

Illustrated catalogue of type specimens of insects (Hexapoda) at Coleção Entomológica "Prof. J.M.F.Camargo" (RPSP), Universidade de São Paulo, Brazil.

The present catalogue lists the insect types (Hexapoda) deposited at Coleção Entomológica "Prof. J.M.F.Camargo" (RPSP), Universidade de São Paulo, Ribeirão Preto, Brazil. This collection is known as one of the most significant depositories of stingless bees (Hymenoptera: Apidae: Meliponini) for the Brazilian and Neotropical faunas, largely because of the legacy of Professor João Franco Maria de Camargo (in memoriam) and co-workers. The Meliponini constitute the most emblematic portion of the collection, comprising 3,335 type-specimens (66 holotypes, 3,254 paratypes, and 15 paralectotypes), which represent 132 species-names. In addition to stingless bees, 495 type specimens of other Hymenoptera (23 holotypes and 472 paratypes) are deposited at RPSP representing 71 hymenopteran species-names: Agaonidae (16 names), Andrenidae (3 names), non-Meliponini Apidae (21 names), Chrysididae (2 names), Halictidae (16 names), Colletidae (5 names), Megachilidae (5 names), Melittidae (1 name), Pteromalidae (1 name), and Vespidae (1 name); the only other insect order currently represented by types at RPSP is Diptera (Drosophilidae: 2 names). Altogether, there currently are 3,832 type-specimens deposited at RPSP. Label data and additional information from the RPSP registers, literature sources, and taxonomic remarks are given, including photographs of name bearing types and representatives of other type specimens of the species herein considered.

The Odonata of Quebec: Specimen data from seven collections.

BACKGROUND: The Odonata, dragonflies and damselflies, constitute one of the more charismatic and better-studied orders of insects. The approximately 6,000 extant species on Earth can be variously found on all continents, except Antarctica. A relatively stable taxonomy, a relative ease of species identification and an aquatic immature stage has made the Odonata a taxon of interest in documenting the symptoms of global environmental change, especially at higher latitudes. The Odonata fauna of the north-temperate Canadian province of Quebec includes 150 species, many of which are at the northern limits of their geographic distribution. NEW INFORMATION: Quebec hosts multiple entomological specimen depositories, including seven publicly-accessible research collections. One of these, the University of Montreal's Ouellet-Robert Entomological Collection, houses an exceptionally large collection of Odonata. An initial specimen data capture project for this collection gathered 31,595 Quebec Odonata occurrence records, but several Quebec species were missing and geographic coverage was biased towards the Montreal region. To complement this dataset, we undertook to digitise the Odonata records of six other public research collections. They are, in order of Quebec Odonata collection size, the Laval University Entomological Collection, McGill University's Lyman Entomological Museum, the Insectarium of Montreal Research Collection, the Quebec Government's Insect Collection, Bishop's University's Insect Collection and the Laurentian Forestry Centre's René-Martineau Insectarium. Of the 40,447 total specimen occurrence records, 36,951 are identified to the species level, including 137 of the 150 species officially-recorded in Quebec and 2 non-nominotypical subspecies. We here summarise the data and highlight the strengths and weaknesses of the datasets. The complete dataset is available with this publication (Suppl. material 1), whereas the specimen data associated with each collection are available as Darwin Core archives at Canadensys.net and will be updated as appropriate.

Ichthyological collection of the Museu Oceanográfico D. Carlos I.

The collection of the Museu Oceanográfico D. Carlos I is a historical specimen, instrument, and document collection that has been housed at the Aquário Vasco da Gama since 1935. The collection is largely the result of several scientific campaigns conducted by Dom Carlos de Bragança between 1896 and 1907. Specifically, the ichthyological collection consists of 675 surviving catalogue records of specimens caught, acquired or offered to D. Carlos I between 1892 to 1907, and includes the type specimen for Odontaspis nasutus Bragança, 1904 (junior synonym of Mitsukurina owstoni Jordan, 1898), along with several specimens of deep sea species. All specimens were captured in coastal Portuguese waters, and were preserved in alcohol, formalin, or mounted.

Digitizing specimens in a small herbarium: A viable workflow for collections working with limited resources.

PREMISE OF THE STUDY: Small herbaria represent a significant portion of herbaria in the United States, but many are not digitizing their collections. METHODS: At the Arkansas State University Herbarium (STAR), we have created a viable workflow to help small herbaria begin the digitization process, including suggestions for publishing data on the Internet. We calculated hourly rates of each phase of the digitization process. We also mapped accessions at the county level to determine geographic strengths in the collection. RESULTS: All 17,678 accessioned flowering plant specimens at STAR are imaged, databased in Specify, and available electronically on the herbarium's website. Students imaged the specimens at a mean rate of 145/h. We found differences in databasing rates between the graduate student leading the project (47/h) and undergraduate assistants (25/h). The majority of specimens at STAR were collected within the counties neighboring the institution. DISCUSSION: With this workflow, we estimate that one person can digitize a 20,000-specimen collection in less than 2.5 yr by working only 10 h/wk. Because STAR is a small herbarium with limited resources, the application of the workflow described should assist curators of similar-sized collections as they contemplate and undertake the digitization process.

Symbiota - A virtual platform for creating voucher-based biodiversity information communities.

We review the Symbiota software platform for creating voucher-based biodiversity information portals and communities. Symbiota was originally conceived to promote small- to medium-sized, regionally and/or taxonomically themed collaborations of natural history collections. Over the past eight years the taxonomically diverse portals have grown into an important resource in North America and beyond for mobilizing, integrating, and using specimen- and observation-based occurrence records and derivative biodiversity information products. Designed to mirror the conceptual structure of traditional floras and faunas, Symbiota is exclusively web-based and employs a novel data model, information linking, and algorithms to provide highly dynamic customization. The themed portals enable meaningful access to biodiversity data for anyone from specialist to high school student. Symbiota emulates functionality of modern Content Management Systems, providing highly sophisticated yet intuitive user interfaces for data entry, batch processes, and editing. Each kind of content provision may be selectively accessed by authenticated information providers. Occupying a fairly specific niche in the biodiversity informatics arena, Symbiota provides extensive data exchange facilities and collaborates with other development projects to incorporate and not duplicate functionality as appropriate.