Cyberdiversity: Improving the Informatic Value of Diverse Tropical Arthropod Inventories

In an era of biodiversity crisis, arthropods have great potential to inform conservation assessment and test hypotheses about community assembly. This is because their relatively narrow geographic distributions and high diversity offer high-resolution data on landscape-scale patterns of biodiversity. However, a major impediment to the more widespread application of arthropod data to a range of scientific and policy questions is the poor state of modern arthropod taxonomy, especially in the tropics. Inventories of spiders and other megadiverse arthropods from tropical forests are dominated by undescribed species. Such studies typically organize their data using morphospecies codes, which make it difficult for data from independent inventories to be compared and combined. To combat this shortcoming, we offer cyberdiversity, an online community-based approach for reconciling results of independent inventory studies where current taxonomic knowledge is incomplete. Participating scientists can upload images and DNA barcode sequences to dedicated databases and submit occurrence data and links to a web site (www.digitalSpiders.org). Taxonomic determinations can be shared with a crowdsourcing comments feature, and researchers can discover specimens of interest available for loan and request aliquots of genomic DNA extract. To demonstrate the value of the cyberdiversity framework, we reconcile data from three rapid structured inventories of spiders conducted in Vietnam with an independent inventory (Doi Inthanon, Thailand) using online image libraries. Species richness and inventory completeness were assessed using non-parametric estimators. Community similarity was evaluated using a novel index based on the Jaccard replacing observed with estimated values to correct for unobserved species. We use a distance-decay framework to demonstrate a rudimentary model of landscape-scale changes in community composition that will become increasingly informative as additional inventories participate. With broader adoption of the cyberdiversity approach, networks of information-sharing taxonomists can more efficiently and effectively address taxonomic impediments while elucidating landscape scale patterns of biodiversity.

[1]  I. Agnarsson The phylogenetic placement and circumscription of the genus Synotaxus (Araneae:Synotaxidae), a new species from Guyana, and notes on theridioid phylogeny , 2003 .

[2]  D. Janzen,et al.  Wolbachia and DNA Barcoding Insects: Patterns, Potential, and Problems , 2012, PloS one.

[3]  L. Frézal,et al.  Four years of DNA barcoding: current advances and prospects. , 2008, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[4]  S. Miller,et al.  Low beta diversity of herbivorous insects in tropical forests , 2007, Nature.

[5]  Stephen P. Hubbell,et al.  Beta-Diversity in Tropical Forest Trees , 2002, Science.

[6]  B. Fontaine,et al.  21 years of shelf life between discovery and description of new species , 2012, Current Biology.

[7]  P. Hebert,et al.  Identification of Birds through DNA Barcodes , 2004, PLoS biology.

[8]  B. Dayrat,et al.  Towards integrative taxonomy , 2005 .

[9]  Jonathan A Coddington,et al.  Undersampling bias: the null hypothesis for singleton species in tropical arthropod surveys. , 2009, The Journal of animal ecology.

[10]  D. Rubinoff Utility of Mitochondrial DNA Barcodes in Species Conservation , 2006, Conservation biology : the journal of the Society for Conservation Biology.

[11]  M. Hedin,et al.  The power and perils of ‘molecular taxonomy’: a case study of eyeless and endangered Cicurina (Araneae: Dictynidae) from Texas caves , 2004, Molecular ecology.

[12]  A. Chao,et al.  ESTIMATING THE NUMBER OF SHARED SPECIES IN TWO COMMUNITIES , 2000 .

[13]  V. S. Smith,et al.  Descriptive Taxonomy: E-publishing descriptive taxonomy: the convergence of taxonomic journals and databases , 2015 .

[14]  Robert K. Colwell,et al.  Density compensation, species composition, and richness of ants on a neotropical elevational gradient , 2011 .

[15]  S. Collins,et al.  Relative contributions of neutral and niche-based processes to the structure of a desert grassland grasshopper community , 2009, Oecologia.

[16]  K. Will,et al.  Myth of the molecule: DNA barcodes for species cannot replace morphology for identification and classification , 2004, Cladistics : the international journal of the Willi Hennig Society.

[17]  A. Gove,et al.  Environmental and historical imprints on beta diversity: insights from variation in rates of species turnover along gradients , 2013, Proceedings of the Royal Society B: Biological Sciences.

[18]  Michael R Chernick,et al.  Bootstrap Methods: A Guide for Practitioners and Researchers , 2007 .

[19]  Leandro C. S. Assis,et al.  Individuals, kinds, phylogeny and taxonomy , 2011, Cladistics : the international journal of the Willi Hennig Society.

[20]  Robert K. Colwell,et al.  Abundance‐Based Similarity Indices and Their Estimation When There Are Unseen Species in Samples , 2006, Biometrics.

[21]  Robert K. Colwell,et al.  Estimating terrestrial biodiversity through extrapolation. , 1994, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[22]  R. Whittaker Evolution and measurement of species diversity , 1972 .

[23]  T Reid,et al.  The Other 99%. The Conservation and Biodiversity of Invertebrates , 2000 .

[24]  Michael R. Gray,et al.  Spatial turnover in species composition of ground-dwelling arthropods, vertebrates and vascular plants in north-east New South Wales: implications for selection of forest reserves , 1999 .

[25]  A. Albernaz,et al.  A contribution to the knowledge of the spider fauna (Arachnida: Araneae) of the floodplain forests of the main Amazon River channel. , 2009 .

[26]  C. Meyer,et al.  DNA Barcoding: Error Rates Based on Comprehensive Sampling , 2005, PLoS biology.

[27]  Donat Agosti,et al.  Ants : standard methods for measuring and monitoring biodiversity , 2000 .

[28]  David E. Schindel,et al.  Provisional Nomenclature: The On-Ramp to Taxonomic Names , 2010 .

[29]  A. Solow,et al.  Measuring biological diversity , 2006, Environmental and Ecological Statistics.

[30]  P. Hebert,et al.  bold: The Barcode of Life Data System (http://www.barcodinglife.org) , 2007, Molecular ecology notes.

[31]  Marti J. Anderson,et al.  Much ado about nothings: using zero similarity points in distance-decay curves. , 2011, Ecology.

[32]  Jonathan A. Coddington,et al.  Designing and Testing Sampling Protocols to Estimate Biodiversity in Tropical Ecosystems , 1991 .

[33]  Charles E. Griswold,et al.  The symphytognathoid spiders of the Gaoligongshan, Yunnan, China (Araneae: Araneoidea): Systematics and diversity of micro-orbweavers , 2009 .

[34]  J. B. Schmidt,et al.  Rapid biodiversity assessment of spiders (Araneae) using semi‐quantitative sampling: a case study in a Mediterranean forest , 2008 .

[35]  R. Ricklefs,et al.  Beta diversity of angiosperms in temperate floras of eastern Asia and eastern North America , 2004 .

[36]  René Tänzler,et al.  Integrative taxonomy on the fast track - towards more sustainability in biodiversity research , 2013, Frontiers in Zoology.

[37]  K. Gaston Spatial patterns of species description: How is our knowledge of the global insect fauna growing? , 1994 .

[38]  Laurel H. Young,et al.  Estimating Spider Species Richness in a Southern Appalachian Cove Hardwood Forest , 1996 .

[39]  M. Kimura A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences , 1980, Journal of Molecular Evolution.

[40]  K. Crandall,et al.  Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified , 2008, Proceedings of the National Academy of Sciences.

[41]  A. Chao Nonparametric estimation of the number of classes in a population , 1984 .

[42]  Robert K. Colwell,et al.  A new statistical approach for assessing similarity of species composition with incidence and abundance data , 2004 .

[43]  N. Baeshen,et al.  Biological Identifications Through DNA Barcodes , 2012 .

[44]  J. B. Schmidt,et al.  Species richness and composition assessment of spiders in a Mediterranean scrubland , 2009, Journal of Insect Conservation.

[45]  Q. Wheeler The New Taxonomy , 2008 .

[46]  Jeremy A. Miller,et al.  A STRUCTURED INVENTORY OF APPALACHIAN GRASS BALD AND HEATH BALD SPIDER ASSEMBLAGES AND A TEST OF SPECIES RICHNESS ESTIMATOR PERFORMANCE , 2000 .

[47]  J. Coddington,et al.  Inventorying and Estimating Subcanopy Spider Diversity Using Semiquantitative Sampling Methods in an Afromontane Forest , 2002 .

[48]  J. Coddington,et al.  Spiders of Pakitza (Madre de Dios, Perú): species richness and notes on community structure , 1996 .

[49]  D. Rubinoff,et al.  Between two extremes: mitochondrial DNA is neither the panacea nor the nemesis of phylogenetic and taxonomic inference. , 2005, Systematic biology.

[50]  Gustavo Hormiga,et al.  WHEN TO QUIT? ESTIMATING SPIDER SPECIES RICHNESS IN A NORTHERN EUROPEAN DECIDUOUS FOREST , 2003 .

[51]  R. Whittaker Vegetation of the Siskiyou Mountains, Oregon and California , 1960 .

[52]  Rudolf Meier,et al.  On the inappropriate use of Kimura‐2‐parameter (K2P) divergences in the DNA‐barcoding literature , 2012, Cladistics : the international journal of the Willi Hennig Society.

[53]  A. Martinoli,et al.  Integrated Operational Taxonomic Units (IOTUs) in Echolocating Bats: A Bridge between Molecular and Traditional Taxonomy , 2012, PloS one.

[54]  C. Marshall,et al.  Has the Earth’s sixth mass extinction already arrived? , 2011, Nature.

[55]  A. Mitchell DNA barcoding demystified , 2008 .

[56]  Xuhua Xia,et al.  Data Analysis in Molecular Biology and Evolution , 2002, Springer US.

[57]  J. Dobyns Effects of sampling intensity on the collection of spider (Araneae) species and the estimation of species richness , 1997 .

[58]  Robert I. McDonald,et al.  The distance decay of similarity in ecological communities , 2007 .

[59]  Benjamin Gilbert,et al.  Neutrality, niches, and dispersal in a temperate forest understory. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[60]  Jimmy Cabra-García,et al.  Additive partitioning of spider diversity in a fragmented tropical dry forest (Valle del Cauca, Colombia) , 2010 .

[61]  Charles E. Griswold,et al.  Taxonomic revision of the spider family Penestomidae (Araneae, Entelegynae) , 2010 .

[62]  A. Chao,et al.  APPLICATION OF LAPLACE'S BOUNDARY‐MODE APPROXIMATIONS TO ESTIMATE SPECIES AND SHARED SPECIES RICHNESS , 2006 .

[63]  X. Xia,et al.  DAMBE: software package for data analysis in molecular biology and evolution. , 2001, The Journal of heredity.

[64]  Robert K. Colwell,et al.  Terrestrial Arthropod Assemblages: Their Use in Conservation Planning , 1993 .

[65]  P. White,et al.  The distance decay of similarity in biogeography and ecology , 1999 .

[66]  M. D’Amen,et al.  Protected areas and insect conservation: questioning the effectiveness of Natura 2000 network for saproxylic beetles in Italy , 2013 .

[67]  R. Vrijenhoek,et al.  DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. , 1994, Molecular marine biology and biotechnology.

[68]  P. Cardoso Standardization and optimization of arthropod inventories—the case of Iberian spiders , 2009, Biodiversity and Conservation.

[69]  Joseph Felsenstein,et al.  DISTANCE METHODS FOR INFERRING PHYLOGENIES: A JUSTIFICATION , 1984, Evolution; international journal of organic evolution.

[70]  Sujeevan Ratnasingham,et al.  A DNA-Based Registry for All Animal Species: The Barcode Index Number (BIN) System , 2013, PloS one.

[71]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[72]  Anne E. Thessen,et al.  Data issues in the life sciences , 2011, ZooKeys.

[73]  S. Sarkar,et al.  Systematic conservation planning , 2000, Nature.

[74]  Rudolf Meier,et al.  Dna Sequences In Taxonomy: Opportunities And Challenges , 2008 .

[75]  Rob DeSalle,et al.  Integrating DNA barcode data and taxonomic practice: Determination, discovery, and description , 2011, BioEssays : news and reviews in molecular, cellular and developmental biology.

[76]  M. Hedin,et al.  The effects of preservatives and temperatures on arachnid DNA , 2005 .

[77]  Systema Naturae 250 - The Linnaean Ark , 2010 .

[78]  Paul D. N. Hebert,et al.  Identifying spiders through DNA barcodes , 2005 .

[79]  R. Busing,et al.  The Unified Neutral Theory of Biodiversity and Biogeography , 2002 .

[80]  A structured inventory of spiders (Arachnida, Araneae) in natural and artificial forest gaps at Porto Urucu, Western Brazilian Amazonia , 2010 .

[81]  Vena Kapoor AN ASSESSMENT OF SPIDER SAMPLING METHODS IN TROPICAL RAINFOREST FRAGMENTS OF THE ANAMALAI HILLS, WESTERN GHATS, INDIA , 2006 .

[82]  S. Ferrier,et al.  Biogeographical concordance and efficiency of taxon indicators for establishing conservation priority in a tropical rainforest biota , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[83]  V. Novotný,et al.  From communities to continents: beta diversity of herbivorous insects , 2005 .

[84]  René Tänzler,et al.  One hundred and one new species of Trigonopterus weevils from New Guinea , 2013, ZooKeys.

[85]  J. Lamarque,et al.  Global Biodiversity: Indicators of Recent Declines , 2010, Science.

[86]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[87]  Robert K. Colwell,et al.  BIODIVERSITY ASSESSMENT USING STRUCTURED INVENTORY: CAPTURING THE ANT FAUNA OF A TROPICAL RAIN FOREST , 1997 .

[88]  R. Guralnick,et al.  Ramping up biodiversity discovery via online quantum contributions. , 2012, Trends in ecology & evolution.

[89]  A Chao,et al.  Estimating population size via sample coverage for closed capture-recapture models. , 1994, Biometrics.

[90]  D. Posada jModelTest: phylogenetic model averaging. , 2008, Molecular biology and evolution.

[91]  C. Gaspar,et al.  Assessing spider species richness and composition in Mediterranean cork oak forests , 2008 .

[92]  A. Chao,et al.  Estimating the Number of Classes via Sample Coverage , 1992 .

[93]  Kevin J. Gaston,et al.  Taxonomy of taxonomists , 1992, Nature.

[94]  Pedro Cardoso,et al.  The seven impediments in invertebrate conservation and how to overcome them , 2011 .

[95]  R. Ricklefs,et al.  A latitudinal gradient in large-scale beta diversity for vascular plants in North America. , 2007, Ecology letters.

[96]  P. White,et al.  Putting Beta-Diversity on the Map: Broad-Scale Congruence and Coincidence in the Extremes , 2007, PLoS biology.

[97]  Michael Balke,et al.  Determining species boundaries in a world full of rarity: singletons, species delimitation methods. , 2012, Systematic biology.

[98]  Q. Wheeler,et al.  The perils of DNA barcoding and the need for integrative taxonomy. , 2005, Systematic biology.

[99]  C. Cicero,et al.  Open access, freely available online Correspondence DNA Barcoding: Promise and Pitfalls , 2022 .

[100]  J. León-Cortés,et al.  Spider diversity in a tropical habitat gradient in Chiapas, Mexico , 2006 .

[101]  T. Erwin,et al.  Mapping Patterns of P • Diversity for Beetles Across the Western Amazon Basin : A Preliminary Case for Improving Inventory Methods and Conservation Strategies , 2007 .

[102]  J. L. Parra,et al.  Very high resolution interpolated climate surfaces for global land areas , 2005 .

[103]  Jeremy R. deWaard,et al.  DNA barcodes for 1/1000 of the animal kingdom , 2009, Biology Letters.

[104]  W. Ponder,et al.  The Other 99%: The Conservation and Biodiversity of Invertebrates , 1999 .

[105]  Jorge Soberón,et al.  The big questions for biodiversity informatics , 2010 .

[106]  G. Powell,et al.  Mapping More of Terrestrial Biodiversity for Global Conservation Assessment , 2004 .

[107]  A. Chao Estimating the population size for capture-recapture data with unequal catchability. , 1987, Biometrics.

[108]  王丽华,et al.  国际生命条形码计划—DNA Barcoding , 2009 .

[109]  Anne Chao,et al.  Measuring and Estimating Species Richness, Species Diversity, and Biotic Similarity from Sampling Data , 2013 .

[110]  Robert K. Colwell,et al.  THE ANT FAUNA OF A TROPICAL RAIN FOREST: ESTIMATING SPECIES RICHNESS THREE DIFFERENT WAYS , 2002 .

[111]  Cristian J. Grismado Palpimanid spiders from Guyana: new species of the genera Fernandezina and Otiothops (Araneae, Palpimanidae, Otiothopinae) , 2002 .

[112]  Stephen Cameron,et al.  A genomic perspective on the shortcomings of mitochondrial DNA for "barcoding" identification. , 2006, The Journal of heredity.

[113]  S. Hubbell,et al.  The unified neutral theory of biodiversity and biogeography at age ten. , 2011, Trends in ecology & evolution.