Biodiversity Data JournalBiodiversity Data JournalBiodiversity Data JournalBDJ1314-28361314-2828Pensoft PublishersBiodiversity Data Journal10.3897/BDJ.3.e63134292Taxonomic paperAnimaliaPlantaeFungiFaunistics & DistributionFloristics & DistributionTaxonomyCatalogues and ChecklistsSystematicsMolecular systematicsUSA and CanadaBiodiversity inventories in high gear: DNA barcoding facilitates a rapid biotic survey of a temperate nature reserveTelferAngela Catelfer@uoguelph.ca‡YoungMonica R‡QuinnJenna§PerezKate‡SobelCrystal N‡SonesJayme E‡Levesque-BeaudinValerie‡DerbyshireRachael‡Fernandez-TrianaJose|RougerieRodolphe¶ThevanayagamAbinah‡BoskovicAdrian‡BorisenkoAlex V‡CadelAlex#BrownAllison‡PagesAnais¤CastilloAnibal H‡NicolaiAnnegret«Glenn MockfordBarb Mockford»BukowskiBelén˄WilsonBill»TrojahnBrock§LacroixCarole Ann˅BrimblecombeChris¦HayChristoperˀHoChristmas‡SteinkeClaudia‡WarneConnor P‡Garrido CortesCristinaˁEngelkingDaniel‡WrightDanielle‡LijtmaerDario A˄GascoigneDavid»Hernandez MartichDavid₵MorningstarDerekℓNeumannDirk₰SteinkeDirk‡Marco DeBruinDonna DeBruin»DobiasDylanˁSearsElizabeth‡RichardEllenˁDamstraEmily»ZakharovEvgeny V‡LabergeFredericˁCollinsGemma E¦BlagoevGergin A‡GraingeGerrie»AnsellGraham‡MeredithGreg₱HoggIan¦McKeownJaclyn‡TopanJanet‡BraceyJason»GuentherJerry»Sills-GilliganJesse‡AddesiJoseph‡PersiJoshua‡LaytonKara K S₳D'SouzaKareina‡DorjiKencho₴GrundyKevin»NghidinwaKirsti₣RonnenbergKylee‡LeeKyung Min₮XieLinxi₦LuLiuqiong‡PenevLyubomir₭GonzalezMailyn₲RosatiMargaret E‽KekkonenMari‡KuzminaMaria‡IskandarMarianne‡MutanenMarko₮FatahiMaryam‡PentinsaariMikko₮BaumanMiriam»NikolovaNadya‡IvanovaNatalia V‡JonesNathaniel‡WeerasuriyaNimalka₦MonkhouseNorman‡LaviniaPablo D˄JannettaPaul‡HanischPriscila E˄McMullinR. Troy˅Ojeda FloresRafael₩MouttetRaphaëlle₸VenderReid‡LabbeeRenee N‡ForsythRobert‡‡LauderRob§§DicksonRoss»KroftRuth»MillerScott E‽MacDonaldShannon‡PanthiSishir||PedersenStephanie‡Sobek-SwantStephanie§NaikSuresh‡LipinskayaTatsiana¶¶EagalleThanushi‡DecaënsThibaud##KosuthThibault¤BraukmannThomas‡WoodcockTom§RoslinTomas¤¤««ZammitTony»»CampbellVictoria‡DincaVlad‡PenevaVlada˄˄HebertPaul D N‡deWaardJeremy Rdewaardj@uoguelph.ca‡Biodiversity Institute of Ontario, Guelph, Canadarare Charitable Research Reserve, Cambridge, CanadaCNC, Ottawa, CanadaMuséum national d'Histoire Naturelle, Paris, FranceUniversity of Waterloo, Waterloo, CanadaUniversité de Montpellier, Montpellier, FranceEcoBio, Université of Rennes, Rennes, Francerare Charitable Research Reserve (Affiliate of), Cambridge, CanadaMuseo Argentino de Ciencias Naturales "Bernardino Rivadavia" (MACN-CONICET), Buenos Aires, ArgentinaBiodiversity Institute of Ontario Herbarium, Guelph, CanadaUniversity of Waikato, Hamilton, New ZealandUniversity of Western Ontario, London, CanadaUniversity of Guelph, Guelph, CanadaUniversidad Autonoma de Santo Domingo DR, Santo Domingo, Dominican RepublicMyotistar, Cambridge, CanadaSNSB, Zoologische Staatssammlung Muenchen, Munich, GermanyGrand River Conservation Authority, Guelph, CanadaThe University of Western Australia, Perth, AustraliaNational Biodiversity Centre, Thimphu, BhutanMinistry of Environment and Tourism in Namibia, Windhoek, NamibiaUniversity of Oulu, Oulu, FinlandThe University of Western Ontario, London, CanadaPensoft, Sofia, BulgariaInstituto de Investigación de Recursos Biológicos Alexander von Humboldt, Bogotá, ColombiaSmithsonian National Museum of Natural History, Washington, United States of AmericaUniversidad Nacional Autónoma de México, Mexico City, MexicoANSES, Laboratoire de la Santé des Végétaux, Montferrier sur Lez, FranceNew Brunswick Museum, Saint John, CanadaLondon Homeopathy, London, CanadaMinistry of Forests and Soil Conservation, Kathmandu, NepalScientific and Practical Center for Bioresources, National Academy of Sciences of Belarus, Minsk, BelarusUniversité de Montpellier Centre d'Ecologie Fonctionnelle et Evolutive, Montpellier, FranceUniversity of Helsinki, Helsinki, FinlandSwedish University of Agricultural Sciences, Uppsala, SwedenGrand River Conservation Authority, Cambridge, CanadaBulgarian Academy of Sciences, Sofia, Bulgaria
Corresponding authors: Angela C Telfer (atelfer@uoguelph.ca), Jeremy R deWaard (dewaardj@uoguelph.ca).
Academic editor: Pavel Stoev
2015300820153e63132408201524082015Angela C Telfer, Monica R Young, Jenna Quinn, Kate Perez, Crystal N Sobel, Jayme E Sones, Valerie Levesque-Beaudin, Rachael Derbyshire, Jose Fernandez-Triana, Rodolphe Rougerie, Abinah Thevanayagam, Adrian Boskovic, Alex V Borisenko, Alex Cadel, Allison Brown, Anais Pages, Anibal H Castillo, Annegret Nicolai, Barb Mockford Glenn Mockford, Belén Bukowski, Bill Wilson, Brock Trojahn, Carole Ann Lacroix, Chris Brimblecombe, Christoper Hay, Christmas Ho, Claudia Steinke, Connor P Warne, Cristina Garrido Cortes, Daniel Engelking, Danielle Wright, Dario A Lijtmaer, David Gascoigne, David Hernandez Martich, Derek Morningstar, Dirk Neumann, Dirk Steinke, Donna DeBruin Marco DeBruin, Dylan Dobias, Elizabeth Sears, Ellen Richard, Emily Damstra, Evgeny V Zakharov, Frederic Laberge, Gemma E Collins, Gergin A Blagoev, Gerrie Grainge, Graham Ansell, Greg Meredith, Ian Hogg, Jaclyn McKeown, Janet Topan, Jason Bracey, Jerry Guenther, Jesse Sills-Gilligan, Joseph Addesi, Joshua Persi, Kara K S Layton, Kareina D'Souza, Kencho Dorji, Kevin Grundy, Kirsti Nghidinwa, Kylee Ronnenberg, Kyung Min Lee, Linxi Xie, Liuqiong Lu, Lyubomir Penev, Mailyn Gonzalez, Margaret E Rosati, Mari Kekkonen, Maria Kuzmina, Marianne Iskandar, Marko Mutanen, Maryam Fatahi, Mikko Pentinsaari, Miriam Bauman, Nadya Nikolova, Natalia V Ivanova, Nathaniel Jones, Nimalka Weerasuriya, Norman Monkhouse, Pablo D Lavinia, Paul Jannetta, Priscila E Hanisch, R. Troy McMullin, Rafael Ojeda Flores, Raphaëlle Mouttet, Reid Vender, Renee N Labbee, Robert Forsyth, Rob Lauder, Ross Dickson, Ruth Kroft, Scott E Miller, Shannon MacDonald, Sishir Panthi, Stephanie Pedersen, Stephanie Sobek-Swant, Suresh Naik, Tatsiana Lipinskaya, Thanushi Eagalle, Thibaud Decaëns, Thibault Kosuth, Thomas Braukmann, Tom Woodcock, Tomas Roslin, Tony Zammit, Victoria Campbell, Vlad Dinca, Vlada Peneva, Paul D N Hebert, Jeremy R deWaardThis is an open access article distributed under the terms of the Creative Commons Attribution License 4.0 (CC-BY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.Background
Comprehensive biotic surveys, or ‘all taxon biodiversity inventories’ (ATBI), have traditionally been limited in scale or scope due to the complications surrounding specimen sorting and species identification. To circumvent these issues, several ATBI projects have successfully integrated DNA barcoding into their identification procedures and witnessed acceleration in their surveys and subsequent increase in project scope and scale. The Biodiversity Institute of Ontario partnered with the rare Charitable Research Reserve and delegates of the 6th International Barcode of Life Conference to complete its own rapid, barcode-assisted ATBI of an established land trust in Cambridge, Ontario, Canada.
New information
The existing species inventory for the rare Charitable Research Reserve was rapidly expanded by integrating a DNA barcoding workflow with two surveying strategies – a comprehensive sampling scheme over four months, followed by a one-day bioblitz involving international taxonomic experts. The two surveys resulted in 25,287 and 3,502 specimens barcoded, respectively, as well as 127 human observations. This barcoded material, all vouchered at the Biodiversity Institute of Ontario collection, covers 14 phyla, 29 classes, 117 orders, and 531 families of animals, plants, fungi, and lichens. Overall, the ATBI documented 1,102 new species records for the nature reserve, expanding the existing long-term inventory by 49%. In addition, 2,793 distinct Barcode Index Numbers (BINs) were assigned to genus or higher level taxonomy, and represent additional species that will be added once their taxonomy is resolved. For the 3,502 specimens, the collection, sequence analysis, taxonomic assignment, data release and manuscript submission by 100+ co-authors all occurred in less than one week. This demonstrates the speed at which barcode-assisted inventories can be completed and the utility that barcoding provides in minimizing and guiding valuable taxonomic specialist time. The final product is more than a comprehensive biotic inventory – it is also a rich dataset of fine-scale occurrence and sequence data, all archived and cross-linked in the major biodiversity data repositories. This model of rapid generation and dissemination of essential biodiversity data could be followed to conduct regional assessments of biodiversity status and change, and potentially be employed for evaluating progress towards the Aichi Targets of the Strategic Plan for Biodiversity 2011–2020.
DNA barcodingspecies identificationbiodiversity assessmentbiotic inventoryBarcode Index NumbersOperational Taxonomic Unitsrare Charitable Research ReserveIntroduction
It is now universally accepted that we have entered a period of unprecedented global biodiversity loss (Simberloff 1996, Pimm et al. 1995, Pimm et al. 2014), and quantifying this diversity rapidly and on a massive scale is required to begin the challenging process of halting this trend. The completion of biodiversity inventories at various geographic and time scales can contribute to national and international assessments of biodiversity knowledge, deemed necessary by the newly established Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (Díaz et al. 2015). These assessments are fundamental for evaluating progress towards – and potentially reaching – the Convention on Biological Diversity’s Aichi Targets of the Strategic Plan for Biodiversity 2011–2020 (https://www.cbd.int/sp/targets/). Specifically, biodiversity inventories address a component of Aichi target 19, to improve and disseminate biodiversity knowledge, particularly its status and trends.
Even prior to the concept’s introduction (Janzen and Hallwachs 1994), several ‘all taxon biodiversity inventories’ (ATBI) and similar initiatives emerged to document large blocks of life in a circumscribed region or protected area. These comprehensive biotic surveys, particularly those in tropical locales, have traditionally been mired at the stage of specimen sorting and species identification. The taxonomic impediment – the shortage of taxonomic information and the gaps in our taxonomic knowledge – have severely limited and slowed the sorting and naming of collected material (Janzen 1993, Lawton et al. 1998, Janzen 2004). The integration of DNA barcoding however, has simplified, accelerated, and democratized this task (Hebert et al. 2003, Packer et al. 2009, Cristescu 2014, Joly et al. 2014). Several ATBI projects have now successfully integrated DNA barcoding into their identification procedures, observed this acceleration, and in many cases, even increased the scope or scale of their project as a result. A few notable ATBIs that have incorporated DNA barcoding for species identification include projects in the Área de Conservación Guanacaste, Costa Rica (Janzen et al. 2009), Churchill, Canada (Zhou et al. 2009), Great Smoky Mountains, United States (Zhou et al. 2011), Madang, Papua New Guinea (Novotny et al. 2007), Moorea, French Polynesia (Check 2006), Zackenberg, Greenland (Wirta et al. 2015), and Mount Kinabalu, Malaysia (Merckx et al. 2015).
Following this model, the present study introduces DNA barcoding to a long-term biotic inventorying effort being conducted in a temperate nature reserve. The objective is to gauge the effect of adding this tool, in terms of both acceleration and increase of taxonomic scope, while concurrently constructing a reference DNA barcode library to facilitate future research and monitoring at this site. The existing inventory is expanded by employing two surveying strategies – a longer and comprehensive invertebrate trapping scheme, followed by a concentrated effort involving taxonomic experts in the form of a bioblitz (Lundmark 2003). In both cases, DNA barcoding is employed to sort the material rapidly into operational taxonomic units (OTUs), provide taxonomic assignment at varying levels of resolution depending on the taxon group, and organize the OTUs and linked specimen vouchers for examination by experts. The results demonstrate the speed at which barcode-assisted surveys can be completed, the role that barcoding plays in limiting and optimizing valuable taxonomic specialist time, and ultimately, a scalable model for rapid biotic surveys and dissemination of the rich biodiversity data captured. The product is not merely a comprehensive biotic inventory, but also a rich dataset of fine-scale occurrence and sequence data, all stored and cross-linked in several public biodiversity data repositories.
Materials and methodsStudy Site and Existing Species Inventory
The rare Charitable Research Reserve is a 365+ hectare land reserve which was set aside in 2001 to preserve the cultural history and ecological integrity of the area, while providing opportunities for scientific research and public education within the context of an urbanized region. It is located at the confluence of the Speed and Grand Rivers in Cambridge, Ontario, Canada (43.381128, -80.357807), where the Carolinian and Northern Hardwood forests also meet. The reserve contains a diversity of habitats including existing and reclaimed agricultural lands, wetlands, floodplains, shrub thickets, limestone cliffs and alvars, cold-water creeks, and old growth forest. Due to these diverse habitats, as well as the organization’s mandate to facilitate scientific research, rare has been the site of a variety of innovative research studies, including studies on fern genetics (Henry et al. 2014), prairie community establishment (Harvey and MacDougall 2014), and pollination services (Woodcock et al. 2014). For the present study, we chose sampling sites to encompass a wide range of habitats within the area. In advance of the bioblitz, sampling was conducted within an alvar, reclaimed agricultural fields, forest edges, and a wetland (Fig. 1). Six additional sites were sampled for the bioblitz: terrestrial and aquatic sampling was performed at the Grand River, Blair Flats Wetland, and Cruickston Creek; terrestrial sampling was conducted at an alvar, a cedar stand, and a silver maple wetland (Fig. 1). The wetlands on the reserve are part of the Barrie's Lake Bauman Creek Wetland Complex, which has been classified as a Provincially Significant Wetland by the Ontario Ministry of Natural Resources. Much of the property is also considered locally significant by the Regional Municipality of Waterloo.
Prior to this study, 2,246 species had been recorded at rare, including birds (231), mammals (37), insects (832), plants (836), mosses (63) and lichens (21) (Suppl. material 1; note that 218 species still require confirmation, denoted by parentheses). These observations have come from a variety of sources including rare staff and advisors, citizen scientists, and academic researchers, some of whom have made notable contributions to this inventory, such as Woodcock et al. 2014 who added 150 species of pollinators. Others have provided observations of rarely encountered species, such as the rove beetles Xantholinuselegans (Olivier, 1795) (first record for North America) and Xantholinuslinearis (Olivier, 1794) (previously known from the east coast of Canada, now present in Ontario) (Brunke and Majka 2010). The rare reserve also hosts several species that fall on the provincial or national lists of conservation concern: 1% of the total have a status ranging from special concern, threatened or endangered (15, 6 and 7 species, respectively), while 1.5% have an undefined status of rare or uncommon (15 and 19 species, respectively). Several of these species, such as the barn swallow [Hirundorustica (Linnaeus, 1758)], which has been nationally listed as threatened since 2011, are the subjects of active recovery projects at rare. Similar to many species inventories, rare's list is evidently more complete for charismatic and well-studied taxa, such as birds, butterflies and vascular plants. The observations for these groups would be enabled by excellent field guides and the disproportionate interest of citizen scientists; the opposite would be the case for most invertebrate taxa, and rare's inventory reflects this. If it is assumed that the proportions of major taxonomic groups inhabiting this reserve resemble those for similar temperate sites (e.g., Great Smoky Mountains: Sharkey 2001) or the Canadian terrestrial and freshwater biota in general (Mosquin et al. 1995), this inventory is deficient in several major groups such as insects, arachnids, nematodes, fungi and lichens. The supporting data for most species entries are also lacking, such as specific locality, date or identifier of each observation. In addition, the bioblitz has highlighted errors in the inventory which may have been present due to the compilation of observations from a variety of sources including non-experts. Furthermore, nearly all observations are not supported by voucher specimens or images to permit verification (Bortolus 2008).
Survey Strategies and Specimen Collection
Two strategies were employed in an effort to maximize the diversity of organisms inventoried. The first was a comprehensive collecting scheme executed over a period of approximately four months (May to August 2015). It involved a variety of targeted taxa and techniques, but heavily favoured the collection of terrestrial arthropods by passive trapping. Four Malaise traps were set up in various habitats around the rare property (Fig. 1) and were serviced weekly. Three pitfall traps were set up in close proximity to each Malaise trap and serviced in parallel. From May 25-31 and July 6-12, 2015, 'standardized sampling' procedures developed by the Biodiversity Institute of Ontario were employed at three different sites at rare (Fig. 1). Standardized sampling includes 20 pitfall traps, 10 pan traps, three litter and/or soil samples for Berlese funnels, one flight intercept trap and one Malaise trap – all deployed for a total of seven days. Standardized sampling also includes 60 total minutes of sweep netting, which is performed in three sessions with four collectors sweep netting for five consecutive minutes simultaneously. Each session is pooled into one sample and preserved in 95% ethanol. Passive traps (pitfall, pan, intercept) were deployed with soapy water and serviced every two days, while the Malaise trap used 95% ethanol and ran for the duration of the collecting period. All specimens collected through this standardized sampling routine were consolidated into individual jars for each technique. From July 23 to Aug 13, 2015, at least two ultraviolet light traps were deployed for one night per week; each trap was left overnight using ethyl acetate as a killing agent. On August 5, 2015, several aquatic samples were collected using stable dip nets for surber sampling, deploying hand nets along the stream banks and selective turning of stones to recover macroinvertebrates hiding below. Then the sample was passed through a 50 µm mesh net to capture the smaller invertebrates. All specimens collected from these samples were preserved in 95% ethanol. This first strategy of comprehensive sampling over several months was conducted by technical staff, including undergraduate students, and completed on Aug 15, 2015.
The second strategy for surveying the reserve was a more concentrated effort and involved taxonomic experts – the execution of a bioblitz (Lundmark 2003). Termed the 'rare BioBlitz', the event involved 113 participants from 31 institutions and coincided with the 6th International Barcode of Life Conference (Adamowicz 2015). Collection efforts at the bioblitz were focused on six sites selected based on habitat diversity, proximity, and potential species diversity (Fig. 1). Sampling efforts were concentrated between 1-3 pm and 9-11 pm and targeted taxa that fell within the expertise of the participants and in groups underrepresented in the rare inventory (e.g., spiders, parasitic wasps, mites, nematodes, fungi, and lichens). Various methods for collecting both terrestrial and aquatic arthropods were employed, including dip nets, seine nets, sweep netting, and plankton netting. Small teams surveyed the property and adjacent rivers for taxonomic groups not collected in the four previous months, including fungi, lichens, and vascular plants. Since the inventory is fairly complete for vascular plants (836 species), an effort was made to barcode all species of Blair Flats, a tall grass prairie site that is an active research site (e.g., Harvey and MacDougall 2014). For these taxa, specimens were collected in the field into bags and processed afterward (e.g., pressed and dried onto herbarium sheets). Fungal specimens were collected and processed in a similar manner. Several taxa were targeted for sightings only, where no voucher specimens were collected; these groups included fish, birds, bats, herptiles and odonates (for bat sightings protocol, see Suppl. material 2). All collected specimens were sorted and identified to the lowest taxonomic level possible by the appropriate expert, both on site and following the event from August 16-20, 2015. Vertebrates, plants, fungi and lichens were almost all identified to species, while most invertebrate specimens were assigned to order or family prior to analysis. Invertebrate specimens were either stored in 95% ethanol or pinned after collection. For all invertebrate, plant, and fungal taxa, voucher specimens were collected where possible and deposited in the Biodiversity Institute of Ontario's natural history collection (BIOUG) or herbarium (BIO-OAC) for permanent storage (Schilthuizen et al. 2015).
DNA Barcode Analysis
Both surveying strategies provided a large number of specimens that were sorted and prepared for subsequent DNA barcode analyses at the Canadian Centre for DNA barcoding (CCDB; www.ccdb.ca). A total of 25,287 specimens were sequenced from collection efforts from May to August 2015, followed by 3,502 specimens directly following the rare BioBlitz on Aug 16, 2015. Tissue samples were prepared in 96-well plate format and when necessary, the whole specimen proceeded through lysis and was recovered as voucher from the filter plate (Porco et al. 2010). Tissue lysis and DNA extraction varied slightly for different taxa (Suppl. material 3), but followed standard CCDB procedures (Ivanova et al. 2006, deWaard et al. 2008, Ivanova et al. 2008, Ivanova et al. 2011, Fazekas et al. 2012).
One or more standard DNA barcode markers were targeted for each major group of organisms: for animals, the mitochondrial gene cytochrome oxidase subunit 1 (COI) (Hebert et al. 2003); for plants, the plastid marker rbcL (Hollingsworth et al. 2009) and the nuclear ribosomal internal transcribed spacer 2 (ITS2) marker (Hollingsworth 2011, Schoch et al. 2012); and for fungi and lichens (where only the fungal component was targeted), the internal transcribed spacer (ITS) marker (Schoch et al. 2012). PCR amplification, cycle sequencing and sequence analysis followed typical CCDB protocols (Ivanova and Grainger 2006, Kuzmina and Ivanova 2011). The primer cocktails used for PCR and sequencing are detailed in Suppl. material 3. The sequences were manually assembled and edited before upload to in the Barcode of Life Data Systems (BOLD, www.boldsystems.org) (Ratnasingham and Hebert 2007). The DNA extracts for all specimens are stored in the DNA Archive of the CCDB where they are available for additional study.
Barcode Index Numbers and Taxonomic Assignment
For the sequences derived from animal specimens, the records were assigned operational taxonomic units (OTUs) called Barcode Index Numbers (BINs) by the Refined Single Linkage (RESL) algorithm implemented on BOLD (Ratnasingham and Hebert 2013). For the sequences that have at least 500 bp coverage of the barcode region, < 1% ambiguous bases, and no stop codon or contamination flags, the RESL algorithm calculates the number of clusters and their membership (see Ratnasingham and Hebert 2013). The RESL algorithm runs weekly on all qualifying barcode sequences in BOLD, which as of August 2015, includes 5M specimens and 420K BINs. The BIN system is accessible through public, individual ‘BIN pages’ and permits rapid diversity assessments, even in the absence of taxonomic information. BINs show a high concordance with traditional taxonomic species names and can be used as a reliable proxy for species.
For each specimen that was assigned an existing BIN, the record received the existing identification of the BIN to the lowest level that did not have taxonomic conflict. For each specimen assigned a new BIN for BOLD, the sequence was queried through the BOLD Identification Engine (BOLD-ID Engine; http://www.boldsystems.org/index.php/IDS_OpenIdEngine). Identifications were applied based on sequence similarity (<15% for family, <5% for genus) if the query sequence fell within a monophyletic cluster of BINs assigned to this family or genus. For animal records that did not receive BINs (<500bp), the sequence was similarly queried through the BOLD-ID Engine, but used a <2% similarity cutoff for assignment to species, in addition to the genus and family thresholds. Following this, a neighbour-joining tree was constructed and examined for unexpected placements which might indicate overlooked contamination events or analytical error. Finally, specimens and images were inspected morphologically to check for errors and refine the assigned taxonomy where possible.
Data resources
Collection data, taxonomic assignment, sequence, electropherograms and primer details for each specimen record, and often a high resolution image, are available on BOLD in the public dataset, "rare BioBlitz 2015 [DS-RBB15]" (http://dx.doi.org/10.5883/DS-RBB15 or http://boldsystems.org/index.php/MAS_Management_OpenDataSet?datasetcode=DS-RBB15). The sequence data for each successfully barcoded specimen were deposited to GenBank by using the 'Submit to GenBank' function in the BOLD workbench (see Suppl. material 4 for accession numbers).
With the 'Data Spreadsheets' function in the BOLD workbench, the complete dataset was downloaded and reformatted into a Darwin Core Archive (Suppl. material 5) for upload to the Canadensys repository (http://www.canadensys.net), Canada's national node for the Global Biodiversity Information Facility (http://www.gbif.org). The online resource (http://doi.org/10.5886/hh6td9jn) contains all records of the 2015 inventory, including human observations. The citation for the resource is as follows:
Telfer A, Young MR, Quinn J, Perez K, Sobel CN, Sones JE, Levesque-Beaudin V, Derbyshire R, Fernandez-Triana J, Rougerie R, Hebert PDN, deWaard JR and contributors* (2015+). Inventory and BioBlitz Records from rare Charitable Research Reserve. 28,916 records. Online at http://data.canadensys.net/ipt/resource.do?r=rare_inventory, http://doi.org/10.5886/hh6td9jn, and http://www.gbif.org/dataset/09e90dfb-5b1b-4dd9-a796-e2fba53d26f0, released on 2015-08-20, version 1. GBIF key: 09e90dfb-5b1b-4dd9-a796-e2fba53d26f0.
* See Suppl. material 6 for complete list of contributors, institutions and email addresses
ChecklistsChecklist of species observed or collected at the <italic>rare</italic> Charitable Research Reserve in Cambridge, Ontario, Canada. The first of five checklists for Kingdom <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="kingdom">Animalia</tp:taxon-name-part></tp:taxon-name>, this checklist contains members of Phylum <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Annelida</tp:taxon-name-part></tp:taxon-name> and Phylum <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Arthopoda</tp:taxon-name-part></tp:taxon-name> (Class <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="class">Arachnida</tp:taxon-name-part></tp:taxon-name> and Class <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="class">Insecta</tp:taxon-name-part></tp:taxon-name> up to Order <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="order">Dermaptera</tp:taxon-name-part></tp:taxon-name>).AnimaliaAnnelidaClitellataArhynchobdellidaErpobdellidaeErpobdellapunctataLeidy, 1870HaplotaxidaLumbricidaeLumbricusterrestrisLinnaeus, 1758ArthropodaArachnidaAraneaeAgelenidaeAgelenopsispotteriBlackwall, 1846AmaurobiidaeCallobiusbennettiBlackwall, 1846Notes
Checklist of species observed or collected at the <italic>rare</italic> Charitable Research Reserve in Cambridge, Ontario, Canada. The second of five checklists for Kingdom <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="kingdom">Animalia</tp:taxon-name-part></tp:taxon-name>, this checklist contains members of Phylum <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Arthopoda</tp:taxon-name-part></tp:taxon-name>, Class <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="class">Insecta</tp:taxon-name-part></tp:taxon-name> (Orders <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="order">Diptera</tp:taxon-name-part></tp:taxon-name>, <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="order">Ephemeroptera</tp:taxon-name-part></tp:taxon-name>, and <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="order">Hemiptera</tp:taxon-name-part></tp:taxon-name>).ArthropodaAnimaliaInsectaDipteraAgromyzidaeAgromyzafrontellaRondani, 1874Notes
Checklist of species observed or collected at the <italic>rare</italic> Charitable Research Reserve in Cambridge, Ontario, Canada. The third of five checklists for Kingdom <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="kingdom">Animalia</tp:taxon-name-part></tp:taxon-name>, this checklist contains members of Phylum <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Arthopoda</tp:taxon-name-part></tp:taxon-name>, Class <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="class">Insecta</tp:taxon-name-part></tp:taxon-name> (Orders <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="order">Hemiptera</tp:taxon-name-part></tp:taxon-name>, <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="order">Hymenoptera</tp:taxon-name-part></tp:taxon-name> and <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="order">Lepidoptera</tp:taxon-name-part></tp:taxon-name>).InsectaHemipteraCicadellidaeErythroneurarubrellaMcAtee, 1920Notes
ElophilagyralisHulst, 1886ElophilaicciusalisWalker, 1859ElophilatinealisMunroe, 1972Checklist of species observed or collected at the <italic>rare</italic> Charitable Research Reserve in Cambridge, Ontario, Canada. The fourth of five checklists for Kingdom <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="kingdom">Animalia</tp:taxon-name-part></tp:taxon-name>, this checklist contains members of Phylum <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Arthopoda</tp:taxon-name-part></tp:taxon-name>, Class <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="class">Insecta</tp:taxon-name-part></tp:taxon-name> (Orders <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="order">Lepidoptera</tp:taxon-name-part></tp:taxon-name> to <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="order">Trichoptera</tp:taxon-name-part></tp:taxon-name>), and Class <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="class">Malacostraca</tp:taxon-name-part></tp:taxon-name>. From Phylum <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Chordata</tp:taxon-name-part></tp:taxon-name>, it contains Classes <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="subclass">Actinopterygii</tp:taxon-name-part></tp:taxon-name>, <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="class">Amphibia</tp:taxon-name-part></tp:taxon-name>, and <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="class">Aves</tp:taxon-name-part></tp:taxon-name> (Orders <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="order">Anseriformes</tp:taxon-name-part></tp:taxon-name> to <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="order">Passeriformes</tp:taxon-name-part></tp:taxon-name>).AnimaliaArthropodaInsectaLepidopteraCrambidaeLoxostegesticticalisLinnaeus, 1761MicrocrambuselegansClemens, 1860NomophilanearcticaMunroe, 1973PerispastacaeculalisZell., 1875PetrophilabifascialisRobinson, 1869SitochroapalealisDenis & Schiffermüller, 1775UdearubigalisGuenée, 1854UrolanivalisDrury, 1773DepressariidaeAgonopterixarenellaDenis & Schiffermüller, 1775Notes
BesmaquercivorariaGuenée in Boisduval and Guenée, 1858BistonbetulariaLinnaeus, 1758CampaeaperlataGuenée in Boisduval and Guenée, 1858CoryphistameadiiPackard, 1874CostaconvexacentrostrigariaWollaston, 1858Ecliptoperasilaceata[Denis and Schiffermüller], 1775EnnomosmagnariaGuenée in Boisduval and Guenée, 1858EpirrhoealternataMüller, 1764EuchlaenaserrataDrury, 1773IdaeadimidiataHufnagel, 1767OperophterabruceataHulst, 1886Notes
PlagodisphlogosariaGuenée in Boisduval and Guenée, 1858Notes
BOLD:AAA3984
PleuropruchainsulsariaGuenée in Boisduval and Guenée, 1858ScopulainductataGuenée in Boisduval and Guenée, 1858SperanzapustulariaGuenée in Boisduval and Guenée, 1858Notes
BOLD:AAA4456
SynchlorafrondariaGuenée in Boisduval and Guenée, 1858TrichodeziaalbovittataGuenée in Boisduval and Guenée, 1858Notes
BOLD:AAA6926
XanthorhoeferrugataClerck, 1759Notes
BOLD:AAA3817
XanthorhoelacustrataGuenée in Boisduval and Guenée, 1858Notes
ErynnisluciliusScudder and Burgess, 1870EuphyesconspicuaW. H. Edwards, 1863EuphyesdionW. H. Edwards, 1879EuphyesvestrisBoisduval, 1852PholisoracatullusFabricius, 1793PoaneshobomokT. Harris, 1862PoanesmassasoitScudder, 1863PoanesviatorW. H. Edwards, 1865PolitesmysticW. H. Edwards, 1863PolitesorigenesFabricius, 1793PolitespeckiusW. Kirby, 1837PolitesthemistoclesLatreille, 1824PompeiusvernaW. H. Edwards, 1862ThymelicuslineolaOchsenheimer, 1808WallengreniaegeremetScudder, 1863LasiocampidaeMalacosomadisstriaHubnerNotes
BOLD:AAA4130
TolypevelledaStoll, 1791LycaenidaeCelastrinaladonCramer, 1780CelastrinaneglectaW. H. Edwards, 1862CupidocomyntasGodart, 1824FenisecatarquiniusFabricius, 1793LycaenahyllusCramer, 1775SatyirumtitusFabricius, 1793SatyriumacadicumW. H. Edwards, 1862SatyriumcalanusHübner, 1809SatyriumcaryaevorusMcDunnough, 1942SatyriumliparopsLeConte, 1833LymantriidaeDasychirabasiflavaPackard, 1864OrgyiadefinitaPackard, 1864OrgyialeucostigmaJ. E. Smith, 1797MomphidaeMomphaterminellaHumphreys & Westwood, 1845Notes
SuccineidaeSuccineaputrisLinnaeus, 1758VitrinidaeVitrinaangelicaeBeck, 1837Checklist of species observed or collected at the <italic>rare</italic> Charitable Research Reserve in Cambridge, Ontario, Canada. This checklist contains members of Kingdom <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Amoebozoa</tp:taxon-name-part></tp:taxon-name>, Phylum <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Mycetozoa</tp:taxon-name-part></tp:taxon-name>.MyxogastriaLicealesTubiferaceaeLycogalaepidendrumLinnaeus, 1829Notes
/ flavofuscum
LiceidaReticulariaceaeTubiferaferruginosa(Batsch) J.F. Gmel.StemonitidaStemonitidaeStemonitisaxiferaBull, 1791Checklist of species observed or collected at the <italic>rare</italic> Charitable Research Reserve in Cambridge, Ontario, Canada. This checklist contains records from Kingdom <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="kingdom">Fungi</tp:taxon-name-part></tp:taxon-name>, including Phyla <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Ascomycota</tp:taxon-name-part></tp:taxon-name>, <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Basidiomycota</tp:taxon-name-part></tp:taxon-name>, and <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Zygomycota</tp:taxon-name-part></tp:taxon-name>.AscomycotaDictyocatenulataalbaFinley & E. F. Morris 1967AscomycotaArthoniomycetesArthonialesArthoniaceaeArthoniacaesiaKoerber, 1861ArthoniacaudataWilley, 1892ArthoniaradiataVetensk-Akad, 1808DothideomycetesPleosporalesVenturiaceaeApiosporinamorbosaArx, 1954PolyporalesFomitopsidaceaeIschnodermaresinosumSchrader, 1794PiptoporusbetulinusBulliard, 1780PostiacaesiaSchrad, 1881Notes
Exidiaglandulosa(Bulliard) Fries (1822)TremellaceaeTremellafoliaceaPersoon (1800)Tremellareticulate(Berkeley) Farl. (1908)UstilaginomycetesUstilaginalesUstilaginaceaeUstilagomaydis(DC.) CordaZygomycotaZygomycetesMortierellalesMortierellaceaeMortierellahyalina(Harz) W. GamsChecklist of species observed or collected at the <italic>rare</italic> Charitable Research Reserve in Cambridge, Ontario, Canada. The first of two checklists for Kingdom <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="kingdom">Plantae</tp:taxon-name-part></tp:taxon-name>, this checklist contains records from Phyla <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Bryophyta</tp:taxon-name-part></tp:taxon-name>, <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Equisetophyta</tp:taxon-name-part></tp:taxon-name>, <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Lycopodiophyta</tp:taxon-name-part></tp:taxon-name> and <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Magnoliophyta</tp:taxon-name-part></tp:taxon-name> (Class <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="class">Liliopsida</tp:taxon-name-part></tp:taxon-name> and <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="class">Magnoliopsida</tp:taxon-name-part></tp:taxon-name>).PlantaeBryophytaBryopsidaBryalesBryaceaeBryumcaespiticiumHedw.BryumargenteumHedw.MniaceaeMniummarginatum(With.) Brid. ex P. Beauv.PlagiomniaceaePlagiomniumcuspidatum(Hedw.) T. Kop.DicranalesDicranaceaeDicranumflagellareHedw.DicranummontanumHedw.DitrichaceaeCeratodonpurpureus(Hedw.) Brid.Ditrichumspp.FissidentaceaeFissidensadianthoidesHedw.FissidenstaxifoliusHedw.Fissidensspp.LeucobryaceaeLeucobryumglaucum(Hedw.) Ångstr. in FriesEncalyptalesEncalyptaceaeEncalyptaproceraBruchGrimmialesGrimmiaceaeSchistidiumapocarpa(Hedw.) BsgSchistidiumrivulare(Brid.) Podp.HedwigialesHedwigiaceaeHedwigiaciliata(Hedw.) P. Beauv.HypnalesAmblystegiaceaeAmblystegiumserpens(Hedw.) Schimp. in B.S.G.Amblystegiumvarium(Hedw.) Lindb.Campyliumchrysophyllum(Brid.) J. LangeCampyliumhispidulum(Brid.) Mitt.Campyliumspp.Hygroamblystegiumfluviatile(Hedw.) LoeskeHygroamblystegiumtenax(Hedw.) Jenn.Leptodictyumriparium(Hedw.) Warnst.Drepanocladusaduncus(Hedw.) Warnst.AnomodontaceaeAnomodonattenuatus(Hedw.) Hüb.Anomodonrostratus(Hedw.) Schimp.BrachytheciaceaeBrachytheciumspp.Cirriphyllumpiliferum(Hedw.) GroutEurhynchiumhians(Hedw.) Sande Lac.Eurhynchiumpulchellum(Hedw.) Jenn.ClimaciaceaeClimaciumamericanumBrid.Climaciumdendroides(Hedw.) Web. & MohrEntodontaceaeEntodonseductrix(Hedw.) C. Müll.FontinalaceaeFontinalishypnoidesHartm.HylocomiaceaeRhytidiadelphustriquetrus(Hedw.) Warnst.HypnaceaeCallicladiumhaldanianum(Grev.) CrumHomomalliumadnatum(Hedw.) Broth.HypnumcurvifoliumHedw.HypnumimponensHedw.HypnumlindbergiiMitt.Hypnumspp.Platydictyasubtilis(Hedw.) CrumTaxiphyllumdeplanatum(Bruch & Schimp. ex Sull.) Fleisch.LeskeaceaeLeskeapolycarpaHedw.Leskeellanervosa(Brid.) LoeskePlagiotheciaceaeIsopterygiopsismuelleriana(Schimp.) Iwats.ThuidiaceaeThuidiumrecognitum(Hedw.) Lindb.Thuidiumdelicatulum(Hedw.) Schimp. in B.S.G.OrthotrichalesOrthotrichaceaeOrthotrichumanomalumHedw.PottialesPottiaceaeBarbulaconvolutaHedw.Desmatodonobtusifolius(Schwaegr.) Schimp.Hymenostyliumrecurvirostre(Hedw.) Dix.Tortellatortuosa(Hedw.) Limpr.BarbulaunguiculataHedw.Tortularuralis(Hedw.) Gaertn. et al.Weissiaspp.SplachnalesMeesiaceaeLeptobryumpyriforme(Hedw.) Wils.PolytrichopsidaPolytrichalesPolytrichaceaeAtrichumangustatum(Brid.) Bruch & Schimp. in B.S.G.Atrichumundulatum(Hedw.) P. Beauv.Polytrichumspp.SphagnopsidaSphagnalesSphagnaceaeSphagnumspp.TetraphidopsidaTetraphidalesTetraphidaceaeTetraphispellucidaHedw.EquisetophytaEquisetopsidaEquisetalesEquisetaceaeEquisetumarvenseLinnaeusEquisetumhyemaleaffine(Engelm.) Calder & Roy L. TaylorEquisetumpalustreLinnaeusEquisetumpratenseEhrh.EquisetumscirpoidesMichx.EquisetumsylvaticumLinnaeusEquisetumvariegatumvariegatumSchleich. ex F. Weber & D. MohrLycopodiophytaLycopodiopsidaHuperziaceaeHuperziaceaeHuperzialucidula(Michx.) Trevis.LycopodialesLycopodiaceaeLycopodiellainundata(Linnaeus) HolubLycopodiumannotinumLinnaeusLycopodiumobscurumLinnaeusLycopodiumssp.SelaginellalesSelaginellalesSelaginellaceaeSelaginellaeclipesW.R. BuckMagnoliophytaLiliopsidaAlismatalesAlismataceaeSagittarialatifoliaWilld.SagittariarigidaPurshAraceaeArisaematriphyllum(Linnaeus) SchottSymplocarpusfoetidus(Linnaeus) Salisb. ex Nutt.ButomaceaeButomusumbellatusLinnaeusPotamogetonaceaePotamogetoncrispusLinnaeusStuckeniapectinata(Linnaeus) BörnerTofieldiaceaeTrianthaglutinosa(Michx.) BakerAralesAraceaeCallapalustrisLinnaeusLemnaminorLinnaeusWolffiaborealis(Engelm. ex Hegelm.) LandoltWolffiacolumbianaH. Karst.AsparagalesAmarylilidaceaeAlliumtricoccumAitonAsparagaceaeAsparagusofficinalisLinnaeusConvallariamajalisLinnaeusMaianthemumcanadenseDesf.Maianthemumracemosumracemosum(Linnaeus) LinkMaianthemumstellatum(Linnaeus) LinkIridaceaeIrispseudacorusLinnaeusOrchidaceaeCypripediumacauleAitonCypripediumarietinumR. Br.Cypripediumparviflorumvar.pubescens(Willd.) O.W. KnightCypripediumreginaeWalterCyperalesCyperaceaeCarexalbursinaE. Sheld.CarexaquatilisWahlenb.CarexarctataBoott ex Hook.CarexatherodesSpreng.CarexbackiiBoottCarexbebbiiOlney ex FernaldCarexblandaDeweyCarexbromoidesSchkuhr ex Willd.CarexchordorrhizaEhrh. ex L. f.CarexcomosaBoottCarexcrinitaLam.CarexcristatellaBrittonCarexdeweyanaSchwein.CarexdiandraSchrankCarexdispermaDeweyCarexeburneaBoottCarexfoeneaWilld.CarexformosaDeweyCarexglaucodeaTuck. ex OlneyCarexgracillimaSchwein.CarexgranularisMuhl. ex Willd.CarexgriseaWahlenb.CarexhirtifoliaMack.CarexhitchcockianaDeweyCarexhystericinaMuhl. ex Willd.CarexintumescensRudgeCarexjamesiiSchwein.CarexlacustrisWilld.Carexlaevivaginata(Kük.) Mack.CarexlasiocarpaEhrh.CarexlaxiculmisSchwein.CarexlaxifloraLam.CarexleptaleaWahlenb.Carexlivida(Wahlenb.) Willd.CarexlupuliformisSartwell ex DeweyCarexlupulinaMuhl. ex Willd.CarexnormalisMack.CarexpeckiiHoweCarexpedunculataMuhl. ex Willd.CarexpensylvanicaLam.CarexplantagineaLam.CarexplatyphyllaJ. CareyCarexprojectaMack.CarexpseudocyperusLinnaeusCarexretrorsaSchwein.CarexroseaSchkuhr ex Willd.CarexscabrataSchwein.CarexschweinitziiDewey ex Schwein.CarexscopariaSchkuhr ex Willd.CarexsparganioidesMuhl. ex Willd.Carexspp.CarexstipataMuhl. ex Willd.CarexstrictaLam.CarextetanicaSchkuhrCarextonsavar.rugosperma(Mack.) CrinsCarextrichocarpaMuhl. ex Willd.CarextrispermaDeweyCarexutriculataBoottCarexvulpinoideaMichx.CarexwoodiiDeweyCyperusbipartitusTorr.CyperusesculentusLinnaeusDulichiumarundinaceum(Linnaeus) BrittonEleocharisacicularis(Linnaeus) Roem. & Schult.EleocharisintermediaSchult.EriophorumvirginicumLinnaeusEriophorumviridicarinatum(Engelm.) FernaldSchoenoplectiellasmithiivar.smithii(A. Gray) HayasakaSchoenoplectustabernaemontani(C.C. Gmel.) PallaScirpusatrovirensWilld.Scirpuscyperinus(Linnaeus) KunthJuncalesJuncaceaeJuniperusvirginianaLinnaeusLuzulaacuminataRaf.Luzulamultifloramultiflora(Ehrh.) Lej.LilialesIridaceaeIrisspp.IrisversicolorLinnaeusSisyrinchiumangustifoliumMill.SisyrinchiummontanumGreeneSisyrinchiummucronatumMichx.LiliaceaeClintoniaborealis(Aiton) Raf.ErythroniumalbidumNutt.ErythroniumamericanumamericanumKer Gawl.Hemerocallisfulva(Linnaeus) L.HemerocallislilioasphodelusLinnaeusLiliumcanadenseLinnaeusLiliummichiganenseFarw.LiliumphiladelphicumLinnaeusLiliumsuperbumLinnaeusMedeolavirginianaLinnaeusPolygonatumbiflorum(Walter) ElliottPolygonatumpubescens(Willd.) PurshStreptopuslanceolatusvar.lanceolatus(Aiton) RevealTrilliumerectumLinnaeusTrilliumgrandiflorum(Michx.) Salisb.Trilliumspp.UvulariagrandifloraSm.MelanthiaceaeAnticleaelegansvar.glaucus(Nutt.) Zomlefer & JuddSmilacaceaeSmilaxherbaceaLinnaeusSmilaxtamnoidesLinnaeusNajadalesNajadaceaeNajasflexilis(Willd.) Rostk. & W.L.E. SchmidtPotamogetonaceaePotamogetonamplifoliusTuck.PotamogetonpusilluspusillusLinnaeusOrchidalesOrchidaceaeAplectrumhyemale(Muhl. ex Willd.) Torr.Epipactishelleborine(Linnaeus) CrantzGalearisspectabilis(Linnaeus) Raf.Liparisloeselii(Linnaeus) Rich.Platantheradilatata(Pursh) Lindl. ex L.C. BeckPlatantherahyperborea(Linnaeus) Lindl.Platantheranivea(Nutt.) LuerSpirantheslucida(H.H. Eaton) AmesPoalesJuncaceaeJuncusacuminatusMichx.JuncusarticulatusLinnaeusJuncusbrachycarpusEngelm.JuncusbufoniusLinnaeusJuncusdudleyiWiegandJuncuseffususLinnaeusJuncusnodosusLinnaeusJuncustenuisWilld.PoaceaeAgrostiscapillarisLinnaeusAgrostisgiganteaRothAgrostisstoloniferaLinnaeusAlopecurusaequalisSobol.AndropogongerardiiVitmanAvenafatuaLinnaeusAvenasativaLinnaeusBrachyelytrumerectum(Schreb.) P. Beauv.BrizamaximaLinnaeusBromusciliatusLinnaeusBromuslatiglumis(Scribn. ex Shear) Hitchc.BromuspubescensMuhl. ex Willd.Calamagrostiscanadensis(Michx.) P. Beauv.CinnaarundinaceaLinnaeusDactylisglomerataLinnaeusDanthoniaspicata(Linnaeus) P. Beauv. ex Roem. & Schult.Dichantheliumdichotomumvar.dichotomum(Linnaeus) GouldDichantheliumlatifolium(Linnaeus) HarvillDichantheliumlinearifolium(Scribn.) GouldDigitariasanguinalis(Linnaeus) Scop.Eleusineindica(Linnaeus) Gaertn.ElymuscanadensisLinnaeusElymushystrixLinnaeusElymuslanceolatuspsammophilus(J.M. Gillett & H. Senn) Á. LöveElymusrepens(Linnaeus) GouldElymusripariusWiegandElymusvirginicusvar.virginicusLinnaeusFestucarubrarubraLinnaeusGlyceriaborealis(Nash) Batch.Glyceriacanadensis(Michx.) Trin.Glyceriamaxima(Hartm.) Holmb.GlyceriaseptentrionalisHitchc.Glyceriastriata(Lam.) Hitchc.Leersiaoryzoides(Linnaeus) Sw.LoliumperenneLinnaeusMiliumeffusumLinnaeusMuhlenbergiaglomerata(Willd.) Trin.Muhlenbergiamexicanavar.mexicana(Linnaeus) Trin.Muhlenbergiatenuiflora(Willd.) Britton, Sterns & Poggenb.OryzopsisasperifoliaMichx.PanicumcapillareLinnaeusPanicumvirgatumLinnaeusPatisracemosa(Smith) Romaschenko, P.M. Peterson & SorengPhalarisarundinaceaLinnaeusPoacompressaLinnaeusPoanemoralisLinnaeusPoapratensispratensisLinnaeusPoassp.Schizachnepurpurascens(Torr.) SwallenSchizachyriumscoparium(Michx.) NashSetariaviridis(Linnaeus) P. Beauv.Sorghastrumnutans(Linnaeus) NashSporobolusvaginiflorus(Torr. ex A. Gray) Alph. WoodBromusinermisLeysserBromuskalmiiA. GrayEchinochloacrus-galli(Linnaeus) P. Beauv.PhleumpratenseLinnaeusPhragmitesaustralis(Cav.) Trin. ex Steud.Setariapumila(Poir.) Roem. & Schult.SpartinapectinataLinkTyphaceaeTyphaangustifoliaLinnaeusTyphalatifoliaLinnaeusTyphalesSparganiaceaeSparganiumamericanumNutt.SparganiumeurycarpumEngelm.MagnoliopsidaApialesApiaceaeAegopodiumpodagrariaLinnaeusAngelicaatropurpureaLinnaeusCicutabulbiferaLinnaeusCicutamaculataLinnaeusConioselinumchinense(Linnaeus) Britton, Sterns & Poggenb.Cryptotaeniacanadensis(Linnaeus) DC.DaucuscarotaLinnaeusErigeniabulbosa(Michx.) Nutt.HeracleummantegazzianumSommier & LevierOsmorhizaclaytonii(Michx.) C.B. ClarkeSaniculacanadensisvar.grandisFernaldSaniculamarilandicaLinnaeusSiumsuaveWalterThaspiumtrifoliatumvar.aureum(Linnaeus) BrittonZiziaaurea(Linnaeus) W.D.J. KochAraliaceaeAraliaelata(Miq.) Seem.AralianudicaulisLinnaeusAraliaracemosaracemosaLinnaeusHydrocotyleamericanaLinnaeusPanaxquinquefoliusLinnaeusPanaxtrifoliusLinnaeusAristolochialesAristolochiaceaeAsarumcanadenseLinnaeusAsteralesAsteraceaeAchilleamillefoliumLinnaeusAgeratinaaltissima(Linnaeus) King & H. Rob.AmbrosiaartemisiifoliaLinnaeusAmbrosiatrifidaLinnaeusAntennarianeglectaGreeneArctiumlappaLinnaeusArctiumminusBernh.Artemisiacampestriscaudata(Michx.) H.M. Hall & Clem.ArtemisiavulgarisLinnaeusAsterspp.BidenscernuaLinnaeusBidensconnataMuhl. ex Willd.BidensfrondosaLinnaeusBidensssp.BidensvulgataGreeneCarduusnutansLinnaeusCentaureajaceaLinnaeusCentaureastoebemicranthos(Gugler) HayekCichoriumintybusLinnaeusCirsiumarvense(Linnaeus) Scop.Cirsiumdiscolor(Muhl. ex Willd.) Spreng.CirsiummuticumMichx.Cirsiumoleraceum(Linnaeus) Scop.Cirsiumpumilumvar.hilii(Canby) B. BoivinCirsiumvulgare(Savi) Ten.Echinaceapurpurea(Linnaeus) MoenchErechtiteshieraciifolius(Linnaeus) Rafinesque ex de CandolleErigeronannuus(Linnaeus) Pers.ErigeroncanadensisLinnaeusErigeronphiladelphicusvar.philadelphicusLinnaeusErigeronpulchellusMichx.ErigeronstrigosusMuhl. ex Willd.EupatoriumhyssopifoliumLinnaeusEupatoriumperfoliatumLinnaeusEurybiamacrophylla(Linnaeus) Cass.Euthamiagraminifolia(Linnaeus) Nutt.Eutrochiummaculatumvar.maculatum(Linnaeus) E.E. LamontEutrochiumpurpureumvar.purpureum(Linnaeus) E.E. LamontHeleniumflexuosumRaf.HelianthusannuusLinnaeusHelianthusdecapetalusLinnaeusHelianthusgiganteusLinnaeusHelianthustuberosusLinnaeusHeliopsishelianthoides(Linnaeus) SweetHieraciumumbellatumLinnaeusHieraciumvulgatumFr.InulaheleniumLinnaeusLactucacanadensisLinnaeusLactucaserriolaLinnaeusLapsanacommunisLinnaeusLeucanthemumvulgareLam.LiatriscylindraceaMichx.MatricariadiscoideaDC.Nabalusalbus(Linnaeus) HookerNabalusaltissimus(Linnaeus) HookerOnopordumacanthiumLinnaeusPackeraaurea(Linnaeus) Á. Löve & D. LövePilosella×floribunda(Wimmer & Grabowski) FriesNotes
X floribundum
Pilosellaaurantiaca(Linnaeus) F.W. Schultz & Schultz BipontinusPilosellacaespitosa(Dumortier) P.D. Sell & C. WestPilosellaofficinarumF.W. Schultz & Schultz BipontinusPilosellapiloselloidespiloselloides(Villars) SojákPilosellapiloselloidespraealta(Gochnat) S. Bräutigam & GreuterPrenanthesspp.Ratibidapinnata(Vent.) BarnhartRudbeckiahirtaLinnaeusRudbeckialaciniataLinnaeusSolidagoaltissimavar.altissimaLinnaeusSolidagocaesiaLinnaeusSolidagocanadensisLinnaeusSolidagoflexicaulisLinnaeusSolidagogiganteaAitonSolidagohispidaMuhl. ex Willd.SolidagojunceaAitonSolidagonemoralisnemoralisAitonSolidagopatulaMuhl. ex Willd.Solidagoptarmicoides(Torr. & A. Gray) B. BoivinSolidagorigidaLinnaeusSolidagorugosarugosaMill.Solidagospp.SolidagoulmifoliaMuhl. ex Willd.SonchusarvensisarvensisLinnaeusSonchusasper(Linnaeus) HillSonchusoleraceusLinnaeusSymphyotrichumcordifolium(Linnaeus) G.L. NesomSymphyotrichumericoidesvar.ericoides(Linnaeus) G.L. NesomSymphyotrichumlaeve(Linnaeus) Á. Löve & D. LöveSymphyotrichumlanceolatum(Willd.) G.L. NesomSymphyotrichumlateriflorumvar.lateriflorum(Linnaeus) Á. Löve & D. LöveSymphyotrichumlateriflorumvar.hirsuticaule(Lindl. ex DC.) G.L. NesomSymphyotrichumnovae-angliae(Linnaeus) G.L. NesomSymphyotrichumnovi-belgii(Linnaeus) G.L. NesomSymphyotrichumoolentangiensevar.oolentangiense(Riddell) G.L. NesomSymphyotrichumoolentangiense(Riddell) G.L. NesomSymphyotrichumpilosumvar.pilosum(Willd.) G.L. NesomSymphyotrichumpuniceum(Linnaeus) Á. Löve & D. LöveSymphyotrichumracemosum(Elliot) G.L. NesomSymphyotrichumspp.Symphyotrichumurophyllum(Lindl.) G.L. NesomTanacetumvulgareLinnaeusTaraxacumofficinaleF.H. Wigg.TragopogondubiusScop.TragopogonpratensisLinnaeusTussilagofarfaraLinnaeusXanthiumstrumariumLinnaeusCampanulaceaeLobeliasiphiliticaLinnaeusBoraginalesBoraginaceaeHackeliavirginiana(Linnaeus) I.M. Johnst.MyosotisscorpioidesLinnaeusBrassicalesBrassicaceaeHesperismatronalisLinnaeusRorippasylvestris(Linnaeus) BesserCampanulalesCampanulaceaeCampanularapunculoidesLinnaeusCampanularotundifoliaLinnaeusLobeliacardinalisLinnaeusLobeliainflataLinnaeusCapparalesBrassicaceaeAlliariapetiolata(M. Bieb.) Cavara & GrandeNotes
or petiolata
BarbareavulgarisW.T. AitonBerteroaincana(Linnaeus) DC.Brassicajuncea(Linnaeus) Czern.BrassicarapaLinnaeusCapsellabursa-pastoris(Linnaeus) Medik.Cardaminebulbosa(Schreb. ex Muhl.) Britton, Sterns & Poggenb.Cardamineconcatenata(Michx.) Sw.Cardaminediphylla(Michx.) Alph. WoodCardaminemaxima(Nutt.) Alph. WoodCardaminepensylvanicaMuhl. ex Willd.ErysimumcheiranthoidesLinnaeusNasturtiumofficinaleW.T. AitonRorippapalustrispalustrisLinnaeusSinapisalbaLinnaeusSinapisarvensisLinnaeusSisymbriumaltissimumLinnaeusThlaspiarvenseLinnaeusTurritisglabraLinnaeusCaryophyllalesAmaranthaceaeAmaranthusalbusLinnaeusAmaranthusretroflexusLinnaeusAmaranthustuberculatus(Moq.) J.D. SauerCaryophyllaceaeArenariaserpyllifoliaLinnaeusCerastiumarvensearvenseLinnaeusCerastiumfontanumvulgare(Hartm.) Greuter & BurdetDianthusarmeriaLinnaeusDianthusbarbatusLinnaeusSaponariaofficinalisLinnaeusSilenelatifolia(Mill.) Britten & RendleSilenevulgaris(Moench) GarckeStellariagramineaLinnaeusChenopodiaceaeChenopodiumalbumLinnaeusPhytolaccaceaePhytolaccaamericanavar.americanaLinnaeusPolygonaceaePersicariahydropiper(Linnaeus) OpizPersicariapensylvanica(Linnaeus) M. GómezRumexbritannicaLinnaeusRumexcrispusLinnaeusRumexobtusifoliusLinnaeusRumexverticillatusLinnaeusPortulacaceaeClaytoniavirginicaLinnaeusCelastralesAquifoliaceaeIlexverticillata(Linnaeus) A. GrayCelastraceaeCelastrusscandensLinnaeusEuonymusalatus(Thunb.) SieboldEuonymusatropurpureusJacq.EuonymusobovatusNutt.CornalesCornaceaeCornusalternifoliaL. f.CornuscanadensisLinnaeusCornusobliquaRaf.CornusracemosaLam.CornusrugosaLam.CornusstoloniferaMichx.CucurbitalesCucurbitaceaeEchinocystislobata(Michx.) Torr. & A. GrayDipsacalesAdoxaceaeViburnumacerifoliumLinnaeusViburnumlantanaLinnaeusViburnumlentagoLinnaeusViburnumopulusLinnaeusViburnumopulustrilobumvar.americanumAitonViburnumrafinesquianumSchult.CaprifoliaceaeCaprifoliaceaespp.DiervillaloniceraMill.Dipsacussativus(Linnaeus) Honck.Linnaeaborealislongiflora(Torr.) HulténLoniceracanadensisBartram & W. Bartram ex MarshallLoniceradioicaLinnaeusLoniceramorrowiiA. GrayLoniceratataricaLinnaeusSambucuscanadensisLinnaeusSambucusnigraLinnaeusSambucusracemosapubens(Michx.) HouseSymphoricarposalbus(Linnaeus) S.F. BlakeSymphoricarposoccidentalisHook.TriosteumaurantiacumE.P. BicknellDipsacaceaeDipsacusfullonumLinnaeusValerianaceaeValerianaeduliscilata(Torrey & A. Gray) F.G. MeyerEricalesBalsaminaceaeImpatienscapensisMeerb.EricaceaeEpigaearepensLinnaeusGaultheriahispidula(Linnaeus) Muhl. ex BigelowGaultheriaprocumbensLinnaeusVacciniumangustifoliumAitonVacciniummyrtilloidesMichx.PrimulaceaeLysimachiaarvensis(Linnaeus) U. Manns & AnderbergPyrolaceaePyrolaellipticaNutt.Pyrolaspp.EuphorbialesEuphorbiaceaeEuphorbiacyparissiasLinnaeusEuphorbiaesulaLinnaeusChecklist of species observed or collected at the <italic>rare</italic> Charitable Research Reserve in Cambridge, Ontario, Canada. The second of two checklists for Kingdom <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="kingdom">Plantae</tp:taxon-name-part></tp:taxon-name>, this checklist contains records from Phyla <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Magnoliophyta</tp:taxon-name-part></tp:taxon-name> (Class <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="class">Magnoliopsida</tp:taxon-name-part></tp:taxon-name>), <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Marchantiophyta</tp:taxon-name-part></tp:taxon-name>, <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Pinophyta</tp:taxon-name-part></tp:taxon-name>, and <tp:taxon-name><tp:taxon-name-part taxon-name-part-type="phylum">Pteridophyta</tp:taxon-name-part></tp:taxon-name>.MagnoliophytaPlantaeMagnoliopsidaFabalesFabaceaeAmorphacanescensPurshAmphicarpaeabracteata(Linnaeus) FernaldApiosamericanaMedik.Desmodiumcanadense(Linnaeus) DC.GlycyrrhizalepidotaPurshLespedezacapitataMichx.LotuscorniculatusLinnaeusMedicagolupulinaLinnaeusMedicagosativasativaLinnaeusMelilotusalbusMedik.RobiniapseudoacaciaLinnaeusTrifoliumaureumPollichTrifoliumcampestreSchreb.TrifoliumhybridumLinnaeusTrifoliumpratenseLinnaeusTrifoliumrepensLinnaeusViciaamericanaMuhl. ex Willd.ViciacraccaLinnaeusFagalesBetulaceaeAlnusglutinosa(Linnaeus) Gaertn.Alnusincanarugosa(Du Roi) R.T. ClausenBetulaalleghaniensisBrittonBetulapapyriferaMarshallBetulapendulaRothBetulapopulifoliaMarshallBetulapumilaLinnaeusCarpinuscarolinianavirginiana(Marshall) FurlowCorylusamericanaWalterCoryluscornutacornutaMarshallOstryavirginiana(Mill.) K. KochFagaceaeFagusgrandifoliaEhrh.QuercusalbaLinnaeusQuercusbicolorWilld.QuercusellipsoidalisE.J. HillQuercusmacrocarpaMichx.QuercuspalustrisMünchh.QuercusrubraLinnaeusQuercusvelutinaLam.JuglandaceaeJuglansnigraLinnaeusGentianalesApocynaceaeApocynumandrosaemifoliumLinnaeusApocynumcannabinumLinnaeusApocynumsp.Notes
RubiaceaeGaliumaparineLinnaeusGaliumasprellumMichx.GeranialesBalsaminaceaeImpatiensglanduliferaRoyleImpatienspallidaNutt.GeraniaceaeGeraniummaculatumLinnaeusGeraniumrobertianumLinnaeusOxalidaceaeOxaliscorniculataLinnaeusOxalismontanaRaf.OxalisstrictaLinnaeusHaloragalesHaloragaceaeMyriophyllumheterophyllumMichx.MyriophyllumverticillatumLinnaeusHamamelidalesPlatanaceaePlatanusoccidentalisLinnaeusJuglandalesJuglandaceaeCaryacordiformis(Wangenh.) K. KochCaryaglabra(Mill.) SweetCaryaovatavar.ovata(Mill.) K. KochJuglanscinereaLinnaeusLamialesBoraginaceaeAnchusaarvensis(Linnaeus) M. Bieb.CynoglossumofficinaleLinnaeusEchiumvulgareLinnaeusLithospermumparviflorumWeakley, Witsell & D. EstesMyosotislaxaLehm.MyosotisvernaNutt.SymphytumofficinaleLinnaeusLamiaceaeAgastachenepetoides(Linnaeus) KuntzeAjugareptansLinnaeusBlephiliahirsuta(Pursh) Benth.ClinopodiumvulgareLinnaeusCollinsoniacanadensisLinnaeusGaleopsistetrahitLinnaeusGlechomahederaceaLinnaeusLamiumamplexicauleLinnaeusLeonuruscardiacaLinnaeusLycopusamericanusMuhl. ex W.P.C. BartramLycopusasperGreeneLycopusuniflorusMichx.MelissaofficinalisLinnaeusMenthaarvensisauct. non L.MenthacanadensisLinnaeusMenthasp.Notes
DigitalispurpureaLinnaeusPolygalalesPolygalaceaePolygalasppPolygalaverticillatavar.verticillataLinnaeusPolygaloidespaucifolia(Willdenow) J.R. AbbottPolygonalesPolygonaceaeFallopiaconvolvulus(Linnaeus) Á. LöveFallopiascandens(Linnaeus) HolubPersicariahydropiperoides(Michx.) SmallPersicariamaculosaGrayPersicariapunctata(Elliott) SmallPersicariasagittata(Linnaeus) H. GrossPolygonumaviculareLinnaeusPrimulalesPrimulaceaeLysimachiaborealis(Rafinesque) U. Manns & AnderbergLysimachiaciliataLinnaeusLysimachianummulariaLinnaeusLysimachiathyrsifloraLinnaeusPrimulamistassinicaMichx.RanunculalesBerberidaceaeBerberiscanadensisMill.BerberisthunbergiiDC.BerberisvulgarisLinnaeusCaulophyllumthalictroides(Linnaeus) Michx.PodophyllumpeltatumLinnaeusMenispermaceaeMenispermumcanadenseLinnaeusRanunculaceaeActaeapachypodaElliottActaearubra(Aiton) Willd.Actaeaspp.Anemoneacutiloba(DC.) G. LawsonAnemoneamericana(DC.) H. HaraAnemonecanadensisLinnaeusAnemonecylindricaA. GrayAnemonequinquefoliaLinnaeusAnemonevirginianavar.virginianaLinnaeusAnemonevirginianavar.alba(Oakes) Alph. WoodAquilegiacanadensisLinnaeusCalthapalustrisLinnaeusClematisvirginianaLinnaeusCoptistrifolia(Linnaeus) Salisb.RanunculusabortivusLinnaeusRanunculusacrisLinnaeusRanunculushispidusvar.caricetorum(Greene) T. DuncanRanunculusrecurvatusvar.recurvatusPoir.RanunculusrepensLinnaeusRanunculussceleratusvar.sceleratusLinnaeusThalictrumdasycarpumFisch. & Avé-Lall.ThalictrumdioicumLinnaeusThalictrumpubescensPurshThalictrumthalictroides(Linnaeus) Eames & B. BoivinRhamnalesElaeagnaceaeElaeagnusangustifoliaLinnaeusElaeagnusumbellataThunb.Shepherdiacanadensis(Linnaeus) Nutt.RhamnaceaeFrangulaalnusMill.RhamnusalnifoliaL'Hér.RosalesCannabaceaeHumuluslupulusLinnaeusCrassulaceaeSedumacreLinnaeusGrossulariaceaeRibesamericanumMill.RibescynosbatiLinnaeusRibesglandulosumGrauerRibeshirtellumMichx.Ribeslacustre(Pers.) Poir.Ribesoxyacanthoidesvar.oxycanthoidesLinnaeusRibesrubrumLinnaeusRibesssp.RibestristePall.HydrangeaceaePhiladelphuscoronariusLinnaeusRhamnaceaeRhamnuscatharticaLinnaeusRosaceaeAgrimoniagryposepalaWallr.Amelanchierarborea(F. Michx.) FernaldAmelanchierlaevisWiegandAmelanchierspicata(Lam.) K. KochAruncusdioicus(Walter) FernaldCrataeguschrysocarpaAsheCrataeguscrus-galliLinnaeusCrataegusdissonaSarg.CrataeguspunctataJacq.Crataegusspp.Dasiphorafruticosaauct. non (Linnaeus) Rydb.FragariavescaLinnaeusFragariavirginianaDuchesneGeumaleppicumJacq.GeumcanadenseJacq.Geumfragarioides(Michaux) SmedmarkGeumlaciniatumMurrayGeumrivaleLinnaeusGeumurbanumLinnaeusMaluscoronaria(Linnaeus) Mill.MaluspumilaMill.Physocarpusopulifolius(Linnaeus) Maxim.PotentillaanserinaanserinaLinnaeusPotentillaargenteaLinnaeusPotentillanorvegicaLinnaeusPotentillarectaLinnaeusPotentillasimplexMichx.PrunusamericanaMarshallPrunusavium(Linnaeus) L.PrunusmahalebLinnaeusPrunuspensylvanicaL. f.PrunusserotinaEhrh.PrunusvirginianavirginianaLinnaeusPyruscommunisLinnaeusRosablandaAitonRosacinnamomeaL. sensu 1759, non 1753RosamultifloraThunb.RosapalustrisMarshallRosarugosaThunb.RosavirginianaMill.RubusallegheniensisPorterRubuscanadensisLinnaeusRubusflagellarisWilld.RubushispidusLinnaeusRubusidaeusLinnaeusRubusoccidentalisLinnaeusRubuspubescensRaf.Rubusrepens(Linnaeus) KuntzeSorbusamericanaMarshallSorbusaucupariaLinnaeusSpiraeaalbaDu RoiSaxifragaceaeMicranthesvirginiensis(Michx.) SmallMitelladiphyllaLinnaeusMitellanudaLinnaeusParnassiaglaucaRaf.TiarellacordifoliaLinnaeusRubialesRubiaceaeGaliumcircaezansMichx.GaliummollugoLinnaeusGaliumpalustreLinnaeusGaliumtinctoriumLinnaeusGaliumtrifidumtrifidumLinnaeusGaliumtriflorumMichx.MitchellarepensLinnaeusSalicalesSalicaceaeSalix×fragilisLinnaeusSalixalbaLinnaeusSalixamygdaloidesAnderssonSalixbebbianaSarg.SalixcandidaFlüggé ex Willd.SalixcordataMuhl.SalixdiscolorMuhl.SalixeriocephalaMichx.SalixexiguaNutt.Salixhumilisvar.humilisMarshallSalixlucidaMuhl.SalixnigraMarshallSalixpedicellarisPurshSalixpetiolarisSm.SalixpurpureaLinnaeusSalixserissima(L.H. Bailey) FernaldSalixviminalisLinnaeusSapindalesAceraceaeAcernigrumF. MichauxAcerplatanoidesLinnaeusAcerrubrumLinnaeusAcersaccharinumLinnaeusAcersaccharumMarshallAcerspicatumLam.AnacardiaceaeRhusaromaticaAitonRhustyphinaLinnaeusToxicodendronradicansnegundo(Greene) GillisToxicodendronradicansvar.rydbergii(Small ex Rydb.) ErskineToxicodendronvernix(Linnaeus) KuntzeRutaceaeZanthoxylumamericanumMill.SapindaceaeAcernegundoLinnaeusAesculushippocastanumLinnaeusStaphyleaceaeStaphyleatrifoliaLinnaeusSaxifragalesHaloragaceaeMyriophyllumsibiricumKom.ScrophularialesOleaceaeFraxinusamericanaLinnaeusFraxinusnigraMarsh.FraxinuspennsylvanicaMarshallOrobanchaceaeConopholisamericana(Linnaeus) Wallr.Epifagusvirginiana(Linnaeus) W.P.C. BartonScrophulariaceaeAureolariaflava(Linnaeus) Farw.Aureolariavirginica(Linnaeus) PennellPediculariscanadensisLinnaeusPenstemondigitalisNutt. ex SimsPenstemonhirsutus(Linnaeus) Willd.ScrophularialanceolataPurshScrophulariamarilandicaLinnaeusVerbascumblattariaLinnaeusVeronicaamericanaSchwein. ex Benth.SolanalesConvolvulaceaeCalystegiaspithamaea(Linnaeus) PurshConvolvulusarvensisLinnaeusCuscutagronoviiWilld. ex Schult.HydrophyllaceaeHydrophyllumcanadenseLinnaeusHydrophyllumvirginianumLinnaeusPolemoniaceaePhloxsubulatasubulataLinnaeusSolanaceaePhysalisheterophyllaNeesSolanumdulcamaraLinnaeusSolanumlycopersicumLinnaeusUrticalesMoraceaeMorusalbaLinnaeusUlmaceaeCeltisoccidentalisLinnaeusUlmusamericanaLinnaeusUlmuspumilaLinnaeusUlmusrubraMuhl.UlmusthomasiiSarg.UrticaceaeBoehmeriacylindrica(Linnaeus) Sw.Laporteacanadensis(Linnaeus) Wedd.Pileapumila(Linnaeus) A. GrayUrticadioicagracilis(Aiton) SelanderUrticadioicadioicaLinnaeusViolalesCucurbitaceaeSicyosangulatusLinnaeusViolaceaeViolaaduncavar.aduncaSm.ViolacanadensisLinnaeusViolacucullataAitonViolalabradoricaSchrankViolamacloskeyiF.E. LloydViolanephrophyllaGreeneViolapubescensAitonViolarenifoliaA. GrayViolarostrataPurshViolasororiaWilld.Violasororiavar.affinis(Leconte) L.E. McKinneyViolaspp.VitalesVitaceaeParthenocissusquinquefolia(Linnaeus) Planch.VitisripariaMichx.LamialesPhrymaceaePhrymaleptostachyaLinnaeusSaxifragalesHamamelidaceaeHamamelisvirginianaLinnaeusMarchantiophytaJungermanniopsidaMetzgerialesAneuraceaeAneurapinguis(Linnaeus) Dumort.JungermannialesGeocalycaceaeLophocoleaheterophylla(Schrad.) Dum.PorellaceaePorellaplatyphylla(Linnaeus) Pfeiff.RadulaceaeRadulacomplanata(Linnaeus) Dum.PorellalesFrullaniaceaeFrullaniaeboracensisGottscheMarchantiopsidaMarchantialesAytoniaceaeRebouliahemisphaerica(Linnaeus) RaddiConocephalaceaeConocephalumconicum(Linnaeus) Lindb.MarchantiaceaeMarchantiapolymorphaLinnaeusPinophytaPinopsidaCupressalesCupressaceaeJuniperuscommunisLinnaeusJuniperuscommunisvar.depressaPurshPinalesCupressaceaeThujaoccidentalisLinnaeusPinaceaeLarixdeciduaMill.Larixlaricina(Du Roi) K. KochPiceaabies(Linnaeus) Karst.Piceaglauca(Moench) VossPiceapungensEngelm.PinusbanksianaLamb.PinusresinosaAitonPinusstrobusLinnaeusPinussylvestrisLinnaeusTsugacanadensis(Linnaeus) CarrièrePteridophytaFilicopsidaOphioglossalesOphioglossaceaeBotrypusvirginianus(Linnaeus) MichauxPolypodialesAspleniaceaeAspleniumplatyneuron(Linnaeus) Britton, Sterns & Poggenb.AspleniumtrichomanestrichomanesLinnaeusAspleniumvirideHuds.DennstaedtiaceaePteridiumaquilinumvar.latiusculum(Desv.) Underw. ex A. HellerDryopteridaceaeAthyriumfilix-feminavar.angustum(Willd.) G. LawsonCystopterisbulbifera(Linnaeus) Bernh.Cystopterisfragilis(Linnaeus) Bernh.Notes
or tenuis
Depariaacrostichoides(Sw.) M. KatoDryopteris×triploideaWherryDryopteriscarthusiana(Vill.) H.P. FuchsNotes
or spinulosa
Dryopterisclintoniana(D.C. Eaton) DowellDryopteriscristata(Linnaeus) A. GrayDryopterisgoldiana(Hook. ex Goldie) A. GrayDryopterisintermedia(Muhl. ex Willd.) A. GrayDryopterismarginalis(Linnaeus) A. GrayGymnocarpiumdryopteris(Linnaeus) NewmanMatteucciastruthiopterisvar.pensylvanica(Willd.) C.V. MortonOnocleasensibilisLinnaeusPolystichumacrostichoides(Michx.) SchottOsmundaceaeOsmundaclaytonianaLinnaeusOsmundaregalisvar.spectabilis(Willd.) A. GrayPolypodiaceaePolypodiumvirginianumLinnaeusNotes
or vulgare
PteridaceaeAdiantumpedatumLinnaeusPellaeaglabellaMett. ex KuhnThelypteridaceaeThelypterisnoveboracensis(Linnaeus) Nieuwl.Thelypterispalustrisvar.pubescens(G. Lawson) FernaldPolypodiopsidaOsmundalesOsmundaceaeOsmundastrumcinnamomea(Linnaeus) C. PreslOsmundastrumcinnamomea(Linnaeus) C. PreslAnalysis
The two surveying strategies – a four-month long terrestrial arthropod survey, followed by a concentrated bioblitz targeting a variety of taxa – resulted in 25,287 and 3,502 specimens barcoded, respectively, out of a total of 32,645 specimens collected. Observations of an additional 125 species and two higher taxa (for which no voucher specimen was kept) were recorded at the bioblitz (Suppl. material 7). Altogether the surveys covered 14 phyla, 29 classes, 117 orders, and 531 families of animals, plants, fungi and lichens. This comprised 3,986 BINs of animals, 1,193 of which are identified to species (Suppl. materials 4, 8, 9).
The most diverse groups were Ichneumonidae, Chironomidae, and Cecidomyiidae with 188, 365, and 584 BINs respectively. In terms of abundance, the three groups Sciaridae, Cecidomyiidae, and Chironomidae had the largest number of specimens with 1,528, 2,477, and 9,636 specimens. The most abundant BINs were BOLD:ACC0651 (Thripidae: Taeniothripsinconsequens), BOLD:AAD5253 (Chironomidae: Thienemanniellaxena), and BOLD:AAP5920 (Chironomidae: Cricotopustriannulatus) with 349, 636, and 1619 specimens collected. For these three BINs, and many similarly abundant BINs, the presence of closely allied and morphologically similar taxa makes oversampling of these exceptionally common species unavoidable.
Combining all existing data results in a final tally of 3,348 species (Table 1), 1,102 of them new records for the reserve (Suppl. material 10). An incidence-based rarefaction analysis (Fig. 2 Suppl. material 11) computed in EstimateS (Colwell and Elsensohn 2014) approximates that 6,744 BINs of invertebrate animals are present at the reserve, indicating that our inventory is at most 30% complete. 1,918 BINs were singletons (i.e. represented by one specimen); the high proportion of singletons (48%) is another indication that the species inventory is far from complete (Magurran 2004). For comparison, the Great Smoky Mountains National Park (North Carolina and Tennessee, United States) established an ATBI effort in 1998 and have tallied 18,545 of the estimated 100,000 species present in the park. In only a few months, our survey found 20% of the Great Smoky Mountains total from 17 years of effort. The Great Smoky Mountains National Park has recognized the contribution DNA barcoding can play in their ATBI effort and have included this method in their survey (e.g., Scholtens and Wagner 2007, Zhou et al. 2011).
Discussion
The present study has conducted an expansive biotic survey, released the data in several public biodiversity data repositories, and published the unique process and findings – all within a relatively modest timeframe. This model for rapid generation and dissemination of critical biodiversity data could be followed to conduct regional assessments of biodiversity status and change, and potentially aid in evaluating progress towards the Aichi Targets of the Strategic Plan for Biodiversity 2011–2020. To fully appreciate this approach, a closer look at four elements is presented: highlights of the biotic inventory, the multiple levels of acceleration, future improvements to the resource, and the utility of the resource going forward.
Resource Highlights
The biotic inventory of rare Charitable Research Reserve performed between May and August 2015 was noteworthy for a number of reasons. The taxonomic scope of the surveys, which covered fourteen phyla over several kingdoms, was only made possible by the integration of DNA barcoding and by assembling a diverse group of experts. Taxa that appeared under-represented on the prior species inventory were targeted where possible, and in many cases, increased significantly. Spiders (Araneae) for instance were completely absent from the prior inventory. Using the expertise of single specialist, focused collecting efforts, and a comprehensive barcode reference library for Canadian spiders (Blagoev et al. 2015) our survey resulted in the addition of 181 species (12.3% of Canadian fauna), two of which were newly recorded for BOLD (Grammonotainornata, Philodromuspraelustris) and three representing new provincial records (Cicurinapallida, Neoantisteagosiuta, Xysticuswinnipegensis) (Suppl. material 12). Likewise, only 21 lichen species were reported from rare previously, but 53 were collected in a single day at the reserve, increasing the species list to 66. Not all the significant increases were in understudied taxa however: 18 snail and slug species (Mollusca) were added, all new to the reserve; 14 species of fishes were observed, adding three to the previous list of 28; and one mammal (hoary bat, Lasiuruscinereus) of the six observed were added to the list for a total of 37. In terms of BINs, many under-represented taxa did not witness a dramatic increase in named species, but did see large numbers of individual (and unnamed) BINs inventoried; the mites (Acari; 268 BINs) and gall midges (Cecidomyiidae; 584 BINs) are remarkable examples.
Rapid Creation of the Resource
The rapidness of conducting this inventory was due to the acceleration of several steps that comprise the procedure. Firstly, several types of passive traps were employed to acquire large sample sizes for minimal collector effort. For instance, malaise traps often collect 2,000 specimens in a single week with only minutes of servicing time. Secondly, as discussed above, the addition of DNA barcoding streamlines sorting of the material, dividing the specimens into distinct units, minimizing the total number of specimens that require examination. Thirdly, in addition to the initial sorting, barcoding also provides nearly instant taxonomic assignment by querying against reference libraries using BOLD; the resolution of the assignment for queried records depends on the completeness of the reference library. Fourthly, the processing of the bioblitz material and analyses of the DNA barcode data were accelerated at all possible stages to test how quickly a large volume of specimens could proceed through all steps. The generation of data following the bioblitz was impressive: tissue sampling and lysis within 12 hours; DNA extraction and PCR within 24 h; cycle sequencing, cleanup and sequencer loading by 48 h; edited and validated sequences on BOLD by 72 h; taxonomic assignment, data release and manuscript presubmission by 96 h; final manuscript submission to BDJ by 108 h. The laboratory steps are mostly accelerated by automation, while data sharing is greatly facilitated by data release platforms such as BOLD and the Integrated Publishing Toolkit of Canadensys (Robertson et al. 2014), and finally, the manuscript stage is sped up considerably by the online writing tools introduced by Pensoft and other publishers.
Refinement of the Resource
Many BINs are presently identified only to family, subfamily, or at most, genus level. It's important to note that the inventoried taxa that lack species-level determination, including intractable groups such as mites and midges, will be refined over time. Not only does DNA barcoding, empowered by the BIN system, roughly sort the material to direct and minimize the efforts of taxonomic experts (deWaard et al. 2009), but it also facilitates crowd-sourcing of taxonomic refinement. For example, if two specimens are collected in unrelated projects and locations, but assigned to the same BIN, any taxonomic determination on one specimen will be applicable to the other, and the pertinent data (such as identifier and locality) is shared on the public BIN page. For the specimens of this study, their taxonomy could be honed by the efforts of completely unrelated (but now linked) projects.
In addition to this passive approach to refining the taxonomy of these specimens, we will be actively pursuing expert determinations for the unnamed BINs. For many groups, the experts among our coauthors will be able to provide species level resolution in a short period of time (e.g., J.F.-T. specializes in Braconidae, particularly the subfamily Microgastrinae). For other BINs, and over a longer period of time, it will be necessary to solicit determinations from our network of collaborators that specialize on Nearctic taxa. The public release of these data to multiple data repositories should also aid in recruiting active specialists presently outside our network. The vouchered material, all deposited in a single repository (BIOUG), can be quickly assembled and loaned out, along with the associated data and files that may assist in determinations (e.g., tree files and image libraries: Suppl. materials 8, 9). There will however be taxa for which species names will be problematic, due to a lack of active specialists, keys, and/or revisionary work, and where a large proportion of that taxon awaits description. For example, the number of gall midges (Diptera: Cecidomyiidae) inventoried for rare (584) is nearly six times the number of Canadian species described to date (ca. 100, following Gagne and Jaschhof 2014).
When a significant number of species and other taxon categories become available, the refined dataset can be updated in the various data repositories and potentially in a second, updated version of the paper in BDJ. Any subsequent versions – each with a separate Digital Object Identifier (DOI) – would be linked to the original paper, allowing for continuing improvement and additions to the species list for the reserve. It is important to emphasize that the taxa awaiting species-level determination still have persistent identifiers as part of the BIN system; each BIN is assigned a BOLD-generated uniform resource identifier (URI) upon its establishment (e.g. BOLD:AAA0001). Until the species binomial is determined or described, this URI can be used in its place. For example, this URI permits assessing and comparing local diversity (Young et al. 2012) despite uncertainty in taxonomic placement.
Utility of the Resource
While the overarching objective of the study was to develop, assess and demonstrate a model for conducting and disseminating DNA barcode-assisted biotic surveys, a valuable resource was created in the process. The rare Charitable Research Reserve provides a unique urban reserve with the infrastructure necessary to conduct research in its diversity of habitats; a barcode reference library and updated species inventory can now both be added to the infrastructure shared with their researchers and educators. Ecological studies in particular, such as the ongoing prairie community field experiments (e.g., Harvey and MacDougall 2014), could benefit greatly from this resource that allows the investigation of ecological questions previously impossible to address (Joly et al. 2014, Kress et al. 2015). Moreover, these studies and others are increasingly using next generation sequencing (NGS) technologies, where validated reference libraries linked to voucher specimens are of critical importance, since this link is generally lost in NGS studies (Cristescu 2014). This reference library created can also be amalgamated with external barcode records, local inventories, and taxon-specific efforts to create regional and national libraries; this study for instance has enhanced the reference library for animals by providing 468 unique BINs to BOLD. Finally, as mentioned above, it is crucial that we begin to assess biodiversity change and disseminate these data widely -- the resource created here can form the baseline for accessible, repeated assessments, to gauge trends in an important temperate reserve.
Acknowledgements
Financial support was provided by the Ontario Ministry of Research and Innovation and by the government of Canada through Genome Canada and the Ontario Genomics Institute in support of the International Barcode of Life project. Anne McCain Evans and Chris Evans provided support for the BIObus program (www.biobus.ca), whose students conducted much of the field work. A biotic survey and bioblitz of this magnitude could not be completed without the help of many volunteers; we would like to thank the following for their contributions to this study: Reza Zahiri, Carleigh Pope, Cheyanne Richardson, Christine Thompson, Dan Radoslav, Dave Achtymichuk, Erika Kastner, Kim Robichaud, Mike Achtymichuk, Tim Skuse, Lisandra Gal, and Suz Bateson. We would also like to thank our reviewers for their helpful suggestions and contributions to this manuscript: Jeremy Miller, Pavel Stoev, and Torsten Dikow.
Author contributions
Author contributions: P.D.N.H. and J.R.D. designed the study; J.S., C.N.S. and M.R.Y. oversaw specimen and sequence analyses; A.C.T., J.R.D. and V.L.-B. conducted the analyses. J.M. and E.S. provided specimen images. All authors discussed the results and contributed to specimen collection, identifications, and to the manuscript, which was written by J.R.D., R.D., J.F.-T.
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Map indicating habitat types and sampling sites for the 2015 biotic survey conducted at rare Charitable Research Reserve in Cambridge, Ontario, Canada.
Accumulation curves for singleton and total observed BINs for the 2015 survey of rare Charitable Research Reserve.
Summary of species inventory for rare Charitable Research Reserve in Cambridge, Ontario, Canada, following the present study.
Major Group
Common Name
No. on previous inventory
No. on 2015 surveys
New Species
New Total
Annelida
Earthworms
0
2
2
2
Arthropoda:Arachnida
Spiders and others
0
198
198
198
Arthropoda:Crustacea
Crustaceans
0
7
7
7
Arthropoda:Entognatha
Collembola
0
9
9
9
Arthropoda:Insecta
Insects
832
895
778
1,610
Arthropoda:Myriapoda
Millipedes, Centipedes
0
6
6
6
Chordata:Actinopterygii
Fishes
28
14
3
31
Chordata:Amphibia
Amphibians
13
2
0
13
Chordata:Aves
Birds
231
87
0
231
Chordata:Mammalia
Mammals
37
6
1
38
Chordata:Reptilia
Reptiles
10
0
0
10
Fungi
Fungus, Lichens
191
84
60
251
Mollusca
Snails, Clams
0
18
18
18
Plantae
Plants, Mosses, Liverworts
901
103
20
921
Protozoa
Protozoans
3
3
0
3
Total Species
2,246
1,433
1,102
3,348
Species inventory of rare prior to May 2015
Data type: checklist
Brief description: Species inventory for rare Charitable Research Reserve in Cambridge, Canada as of May 2015, prior to the present study.
File: oo_55088.xlsx
Telfer et al.
Bat protocols
Data type: protocols
Brief description: Protocols for the bat component of rare BioBlitz
File: oo_54234.pdf
Telfer et al.
Lysis, primer and marker details
Data type: laboratory
Brief description: Details for laboratory work.
File: oo_54237.xlsx
Telfer et al.
Summary data for 2015 inventory
Data type: summary
Brief description: Summary data for the 28,789 specimens collected for the 2015 inventory, including BIN assignments and locality
File: oo_55064.xlsx
Telfer et al.
Darwin core archive
Data type: occurrences
Brief description: Darwin core archive of 2015 rare species inventory
File: oo_55065.zip
Telfer et al.
Contributors list
Data type: authors
Brief description: A list of all contributors who took part in the collection and identification of specimens collected as part of the 2015 inventory.
File: oo_54646.xls
Telfer et al.
Human observations during rare BioBlitz
Data type: occurrences
Brief description: Human observations during rare BioBlitz, of mostly plants, birds, etc.
File: oo_55066.xlsx
Telfer et al.
BIN representative tree
Data type: tree
Brief description: A neighbour-joining tree constructed from a single representative of each distinct BIN collected in rare, along with a single representative of clusters without BINs.
File: oo_55067.pdf
Telfer et al.
BIN image library
Data type: images
Brief description: A collection of representative images of each BIN collected from the rare Charitable Research Reserve. BINs are listed in the same order as the tree. Specimens without BINs are not included.
File: oo_55068.pdf
Telfer et al.
Final combined inventory for rare Charitable Research Reserve
Data type: checklist
Brief description: The final combined inventory for rare Charitable Research Reserve as of August 2015; including previous checklist and all 2015 species added.
File: oo_55089.xlsx
Telfer et al.
Raw data for accumulation curve
Data type: occurences
Brief description: Lot and BIN data was downloaded for each specimen that received a BIN from BOLD Systems. It was formatted for input into EstimateS (Version 9.1.0) for creation of an accumulation curve.
File: oo_54647.xlsx
Telfer et al.
Sampling and new record images
Data type: images
Brief description: Images of sampling sites, sampling techniques, specimen processing, and three new provincial spider reccords.