The tiny mayfly in the room: implications of size-dependent invertebrate taxonomic identification for biomonitoring data properties

Abstract The appropriate level of taxonomic identification, taxonomic sufficiency, for biomonitoring purposes continues to be controversial. Taxonomic sufficiency, however, fails to address the bias created by size-dependent taxonomic identification, which can result in coarse-resolution identification for immature specimens lacking distinguishing characteristics. Our study provides a direct test for this potential systematic bias in biomonitoring data by examining two morphological traits: body size and shape of key organisms (Ephemeroptera, Plecoptera, Trichoptera and Odonata) collected from standard aquatic biomonitoring samples. Direct measurement of body size and a geometric morphometric description of body shape provide consistent, quantitative variables to describe the composition of specimens identified at different levels of taxonomic resolution (genus or family). Corroborating our expectations, we observed evidence of systematic size bias in family-level identifications. Specimens that could only reliably be identified to the family level were significantly smaller than specimens identified to the genus level. Qualitative comparisons of shape variation between specimens demonstrated a high degree of variation in specimens identified only at the family level and support the conclusion that specimens identified at the family level possess multiple constituent taxa (genera or species). Thus, size-dependent taxonomy can have negative consequences for the accurate determination of biodiversity and may invalidate common biomonitoring metrics. Improvements to biomonitoring protocols through technological advances, including DNA-based taxonomy to augment specimen identification, should effectively remove the size-bias problem in the long term. In the short-term, recognizing instances of size bias, the degree to which it may impact bioassessment and exploring methods for remediation, including traits-based assessments, can enhance data quality and inferences derived from biomonitoring studies.

[1]  T. Cuffney,et al.  Ambiguous taxa: effects on the characterization and interpretation of invertebrate assemblages , 2007, Journal of the North American Benthological Society.

[2]  B. Statzner,et al.  Taxonomic and biological trait differences of stream macroinvertebrate communities between mediterranean and temperate regions: implications for future climatic scenarios , 2007 .

[3]  Thomas G. Dietterich,et al.  Automated processing and identification of benthic invertebrate samples , 2010, Journal of the North American Benthological Society.

[4]  A. Magurran,et al.  Measuring Biological Diversity , 2004 .

[5]  F. Rohlf,et al.  Ecological character displacement in Plethodon: biomechanical differences found from a geometric morphometric study. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Hanna Tuomisto,et al.  A diversity of beta diversities: straightening up a concept gone awry. Part 2. Quantifying beta diversity and related phenomena , 2010 .

[7]  D. Hannah,et al.  How does macroinvertebrate taxonomic resolution influence ecohydrological relationships in riverine ecosystems , 2012 .

[8]  Donald J. Baird,et al.  Trait patterns of aquatic insects across gradients of flow-related factors: a multivariate analysis of Canadian national data , 2008 .

[9]  S. P. Ferraro,et al.  Taxonomic level sufficient for assessing a moderate impact on macrobenthic communities in Puget Sound, Washington, USA , 1992 .

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

[11]  B. Enquist,et al.  Rebuilding community ecology from functional traits. , 2006, Trends in ecology & evolution.

[12]  J. Flannagan Larvae of the North American Caddisfly Genera (Trichoptera). , 1978 .

[13]  J. Fiasson Introduction à l'étude des Macroinvertébrés des eaux douces (Systématique élémentaire et aperçu écologique). H. Tachet, M. Bournaud et Ph. Richoux, avec la collaboration de L. Caillère, M. Coulet, J. Fontaine, J. Juget et E. Pattée , 1981 .

[14]  V. Resh,et al.  After site selection and before data analysis: sampling, sorting, and laboratory procedures used in stream benthic macroinvertebrate monitoring programs by USA state agencies , 2001, Journal of the North American Benthological Society.

[15]  Rick Gunn,et al.  Assessing the impact of errors in sorting and identifying macroinvertebrate samples , 2006 .

[16]  W. Hilsenhoff An Introduction to the Aquatic Insects of North America , 1997 .

[17]  S. Pauls,et al.  Taxonomy and systematics: contributions to benthology and J-NABS , 2010, Journal of the North American Benthological Society.

[18]  N LeRoy Poff,et al.  Incorporating traits in aquatic biomonitoring to enhance causal diagnosis and prediction , 2011, Integrated environmental assessment and management.

[19]  Mehrdad Hajibabaei,et al.  Biomonitoring 2.0: a new paradigm in ecosystem assessment made possible by next‐generation DNA sequencing , 2012, Molecular ecology.

[20]  H. Tuomisto A diversity of beta diversities: straightening up a concept gone awry. Part 1. Defining beta diversity as a function of alpha and gamma diversity , 2010 .

[21]  J. Ward Aquatic insect ecology. 1. Ecology and habitat. , 1992 .

[22]  N. LeRoy Poff,et al.  A database of lotic invertebrate traits for North America , 2006 .

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

[24]  A. Huryn,et al.  Life history and production of stream insects. , 2000, Annual review of entomology.

[25]  Vincent H. Resh,et al.  Taxonomy and stream ecology—The benefits of genus- and species-level identifications , 2001, Journal of the North American Benthological Society.

[26]  A. Chao,et al.  Partitioning diversity for conservation analyses , 2010 .

[27]  J. Heino,et al.  Are higher taxa adequate surrogates for species-level assemblage patterns and species richness in stream organisms? , 2007 .

[28]  Eoin J. O’Gorman,et al.  A functional guide to functional diversity measures , 2009 .

[29]  J. Geist,et al.  Taxonomic sufficiency in freshwater ecosystems: effects of taxonomic resolution, functional traits, and data transformation , 2013, Freshwater Science.

[30]  C. Buddle,et al.  Does species‐level resolution matter? Taxonomic sufficiency in terrestrial arthropod biodiversity studies , 2013 .

[31]  Carl Beierkuhnlein,et al.  Inventory, differentiation, and proportional diversity: a consistent terminology for quantifying species diversity , 2009, Oecologia.

[32]  D. Baird,et al.  Environmental Barcoding: A Next-Generation Sequencing Approach for Biomonitoring Applications Using River Benthos , 2011, PloS one.

[33]  J. M. Elliott Life histories and drifting of the Plecoptera and Ephemeroptera in a Dartmoor stream , 1967 .

[34]  M. Zelditch,et al.  Geometric Morphometrics for Biologists , 2012 .

[35]  S. Dolédec,et al.  Invertebrate community responses to land use at a broad spatial scale: trait and taxonomic measures compared in New Zealand rivers , 2011 .

[36]  Robert C. Bailey,et al.  Taxonomic resolution of benthic macroinvertebrate communities in bioassessments , 2001, Journal of the North American Benthological Society.

[37]  D. Ellis Taxonomic sufficiency in pollution assessment , 1985 .

[38]  J. Lawton,et al.  Patterns in the distribution and abundance of insect populations , 1988, Nature.

[39]  K. Cummins,et al.  An Introduction to the Aquatic Insects of North America , 1981 .

[40]  Marti J. Anderson,et al.  Multivariate dispersion as a measure of beta diversity. , 2006, Ecology letters.

[41]  D. Kendall MORPHOMETRIC TOOLS FOR LANDMARK DATA: GEOMETRY AND BIOLOGY , 1994 .

[42]  N. LeRoy Poff,et al.  Functional trait niches of North American lotic insects: traits-based ecological applications in light of phylogenetic relationships , 2006, Journal of the North American Benthological Society.

[43]  F. Chris JonesF.C. Jones,et al.  Taxonomic sufficiency: The influence of taxonomic resolution on freshwater bioassessments using benthic macroinvertebrates , 2008 .

[44]  Michel Loreau,et al.  Biodiversity, Ecosystem Functioning, and Human Wellbeing: An Ecological and Economic Perspective , 2009 .

[45]  Anne E. Magurran,et al.  Biological Diversity: Frontiers in Measurement and Assessment , 2011 .

[46]  N. Poff,et al.  Variability and convergence in benthic communities along the longitudinal gradients of four physically similar Rocky Mountain streams , 2005 .

[47]  H. David Sheets,et al.  Geometric morphometrics for biologists : a primer , 2004 .

[48]  R. Bailey,et al.  Does taxonomic resolution affect the multivariate description of the structure of freshwater benthic macroinvertebrate communities , 1997 .

[49]  Jing Xiong,et al.  Is coarse taxonomy sufficient for detecting macroinvertebrate patterns in floodplain lakes , 2013 .

[50]  Julien Claude,et al.  Morphometrics with R , 2009 .