Faster, Higher and Stronger? The Pros and Cons of Molecular Faunal Data for Assessing Ecosystem Condition

Abstract Ecological observation of global change processes is dependent on matching the scale and quality of biological data with associated geophysical and geochemical driver information. Until recently, the scale and quality of biological observation on natural assemblages has often failed to match data generated through physical or chemical platforms due to constraints of cost and taxonomic resolution. With the advent of next-generation DNA sequencing platforms, creating ‘big data’ scale observations of biological assemblages across a wide range of phylogenetic groups are now a reality. Here we draw from a variety of studies to illustrate the potential benefits and drawbacks of this new data source for enhancing our observation of ecological change compared with traditional methods. We focus on a key habitat—estuaries—which are among the most threatened by anthropogenic change processes. When community composition data derived using morphological and molecular approaches were compared, the increased level of taxonomic resolution from the molecular approach allowed for greater discrimination between estuaries. Apart from higher taxonomic resolution, there was also an order of magnitude more taxonomic units recorded in the molecular approach relative to the morphological. While the morphological data set was constrained to traditional macroinvertebrate sampling, the molecular tools could be used to sample a wide range of taxa from the microphytobenthos, e.g., diatoms and dinoflagellates. Furthermore, the information provided by molecular techniques appeared to be more sensitive to a range of well-established drivers of benthic ecology. Our results indicated that molecular approaches are now sufficiently advanced to provide not just equivalent information to that collected using traditional morphological approaches, but rather an order of magnitude bigger, better, and faster data with which to address pressing ecological questions.

[1]  S. Simpson,et al.  A biomarker of contaminant exposure is effective in large scale assessment of ten estuaries. , 2014, Chemosphere.

[2]  Anne Courrat,et al.  Three hundred ways to assess Europe's surface waters: An almost complete overview of biological methods to implement the Water Framework Directive , 2012 .

[3]  Susan M. Huse,et al.  Microbial diversity in the deep sea and the underexplored “rare biosphere” , 2006, Proceedings of the National Academy of Sciences.

[4]  Mehrdad Hajibabaei,et al.  Next‐generation sequencing technologies for environmental DNA research , 2012, Molecular ecology.

[5]  S. T. Buckland,et al.  Long-term datasets in biodiversity research and monitoring: assessing change in ecological communities through time. , 2010, Trends in ecology & evolution.

[6]  Mehrdad Hajibabaei,et al.  Big Data in Ecology , 2013 .

[7]  Stuart L. Simpson,et al.  Handbook for sediment quality assessment , 2005 .

[8]  H. Mooney,et al.  Human Domination of Earth’s Ecosystems , 1997, Renewable Energy.

[9]  S Birk,et al.  Intercalibrating classifications of ecological status: Europe's quest for common management objectives for aquatic ecosystems. , 2013, The Science of the total environment.

[10]  B. Rygg,et al.  Distribution of species along pollution-induced diversity gradients in benthic communities in Norwegian fjords , 1985 .

[11]  A. E. Greenberg,et al.  Standard methods for the examination of water and wastewater : supplement to the sixteenth edition , 1988 .

[12]  Paul J. Somerfield,et al.  Relationships between taxonomic resolution macrobenthic community patterns and disturbance , 1998 .

[13]  A. J. Underwood,et al.  Beyond BACI: Experimental designs for detecting human environmental impacts on temporal variations in natural populations , 1991 .

[14]  A. Louise Heathwaite,et al.  Why is achieving good ecological outcomes in rivers so difficult , 2012 .

[15]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[16]  R. Rosenberg,et al.  Macrobenthic succession in relation to organic enrichment and pollution of the marine environment , 1978 .

[17]  J. Heino.  The importance of metacommunity ecology for environmental assessment research in the freshwater realm , 2013, Biological reviews of the Cambridge Philosophical Society.

[18]  A. Basset,et al.  Biodiversity in transitional waters: steeper ecotone, lower diversity , 2014 .

[19]  T. Stoeck,et al.  Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water , 2010, Molecular ecology.

[20]  Jean-Claude Dauvin,et al.  Paradox of estuarine quality: benthic indicators and indices, consensus or debate for the future. , 2007, Marine pollution bulletin.

[21]  Michael Elliott,et al.  The Estuarine Quality Paradox, Environmental Homeostasis and the difficulty of detecting anthropogenic stress in naturally stressed areas. , 2007, Marine pollution bulletin.

[22]  J. Bunge,et al.  Microbial community structure in the North Pacific ocean , 2009, The ISME Journal.

[23]  Matthew J. Colloff,et al.  Ecological assessment of estuarine sediments by pyrosequencing eukaryotic ribosomal DNA , 2010 .

[24]  Holly M. Bik,et al.  A molecular‐based approach for examining responses of eukaryotes in microcosms to contaminant‐spiked estuarine sediments , 2014, Environmental toxicology and chemistry.

[25]  B. Cole.  Evaluation of an ATP photometer for measuring 14C activity , 1984 .

[26]  Susan M. Huse,et al.  Ironing out the wrinkles in the rare biosphere through improved OTU clustering , 2010, Environmental microbiology.

[27]  Donald J. Baird,et al.  Beyond taxonomy: a review of macroinvertebrate trait‐based community descriptors as tools for freshwater biomonitoring , 2010 .

[28]  Richard K. Johnson,et al.  Detection of ecological change in stream macroinvertebrate assemblages using single metric, multimetric or multivariate approaches , 2009 .

[29]  E. Johnston,et al.  Assessing contaminated sediments in the context of multiple stressors , 2010, Environmental toxicology and chemistry.

[30]  A. Georges,et al.  Global biodiversity assessment and hyper-cryptic species complexes: more than one species of elephant in the room? , 2014, Systematic biology.

[31]  D. Baird,et al.  Rapid and accurate taxonomic classification of insect (class Insecta) cytochrome c oxidase subunit 1 (COI) DNA barcode sequences using a naïve Bayesian classifier , 2014, Molecular Ecology Resources.

[32]  Mark V Brown,et al.  Cob gene pyrosequencing enables characterization of benthic dinoflagellate diversity and biogeography. , 2014, Environmental microbiology.

[33]  R. Giblin-Davis,et al.  Ultrasequencing of the meiofaunal biosphere: practice, pitfalls and promises , 2010, Molecular ecology.

[34]  I. Snape,et al.  Human impacts in Antartic marine soft-sediment assemblages: correlations between multivariate biological patterns and environmental variables at Casey Station , 2003 .

[35]  A. Chariton,et al.  Improved Inference of Taxonomic Richness from Environmental DNA , 2013, PloS one.

[36]  A. Chariton,et al.  Influence of the choice of physical and chemistry variables on interpreting patterns of sediment contaminants and their relationships with estuarine macrobenthic communities. , 2010 .

[37]  M. Kennish.  Environmental threats and environmental future of estuaries , 2002, Environmental Conservation.

[38]  G. Charmantier,et al.  Ecophysiological adaptation to salinity throughout a life cycle: a review in homarid lobsters. , 2001, The Journal of experimental biology.

[39]  H. Rogers.  Occurrence and Retention of Plankton Within the Estuary , 1940 .

[40]  J. Wiens.  Spatial Scaling in Ecology , 1989 .

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

[42]  A. Miskiewicz,et al.  Strong links between metal contamination, habitat modification and estuarine larval fish distributions. , 2011, Environmental Pollution.

[43]  K. Winemiller,et al.  Seasonal and spatial variations in fish and macrocrustacean assemblage structure in Mad Island Marsh estuary, Texas , 2003 .

[44]  L. Zinger,et al.  Two decades of describing the unseen majority of aquatic microbial diversity , 2012, Molecular ecology.

[45]  F. Manes,et al.  Fluid Intelligence and Psychosocial Outcome: From Logical Problem Solving to Social Adaptation , 2011, PloS one.

[46]  S. Green.  How Many Subjects Does It Take To Do A Regression Analysis. , 1991, Multivariate behavioral research.

[47]  Guy Woodward,et al.  Biomonitoring of Human Impacts in Freshwater Ecosystems: The Good, the Bad and the Ugly , 2011 .

[48]  C. Wong,et al.  The challenge of choosing environmental indicators of anthropogenic impacts in estuaries. , 2012, Environmental pollution.

[49]  S. Bay,et al.  Comparison of methods for evaluating acute and chronic toxicity in marine sediments , 2008, Environmental toxicology and chemistry.

[50]  A. Merenlender,et al.  Faunal indicator taxa selection for monitoring ecosystem health , 2000 .

[51]  B. Statzner,et al.  Developments in aquatic insect biomonitoring: a comparative analysis of recent approaches. , 2006, Annual review of entomology.

[52]  S. Simpson,et al.  Performance and sensitivity of rapid sublethal sediment toxicity tests with the amphipod Melita plumulosa and copepod Nitocra spinipes , 2011, Environmental toxicology and chemistry.

[53]  W. Traunspurger,et al.  Toxicity analysis of freshwater and marine sediments with meio- and macrobenthic organisms: a review , 1996, Hydrobiologia.

[54]  J. Hedges,et al.  Carbon and nitrogen determinations of carbonate‐containing solids1 , 1984 .

[55]  Pat Hutchings,et al.  Overview of integrative tools and methods in assessing ecological integrity in estuarine and coastal systems worldwide. , 2008, Marine pollution bulletin.

[56]  R. O'Neill,et al.  Ecological Risk Assessment at The Regional Scale: Ecological Archives A005-001. , 1991, Ecological applications : a publication of the Ecological Society of America.

[57]  Mark V Brown,et al.  Core sediment bacteria drive community response to anthropogenic contamination over multiple environmental gradients. , 2013, Environmental microbiology.

[58]  R. Oliver,et al.  Carbon source accounting for fish using combined DNA and stable isotope analyses in a regulated lowland river weir pool , 2010, Molecular ecology.

[59]  Eric Coissac,et al.  Bioinformatic challenges for DNA metabarcoding of plants and animals , 2012, Molecular ecology.

[60]  C. Hawkins,et al.  The comparability of bioassessments: a review of conceptual and methodological issues1 , 2011, Journal of the North American Benthological Society.

[61]  J. T. Curtis,et al.  An Ordination of the Upland Forest Communities of Southern Wisconsin , 1957 .

[62]  Brendan P. Kelaher,et al.  Variation in detrital enrichment causes spatio-temporal variation in soft-sediment assemblages , 2003 .

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

[64]  Marti J. Anderson,et al.  A new method for non-parametric multivariate analysis of variance in ecology , 2001 .

[65]  E. Long,et al.  Calculation and uses of mean sediment quality guideline quotients: a critical review. , 2006, Environmental science & technology.

[66]  A. Budden,et al.  Big data and the future of ecology , 2013 .

[67]  P. Chapman,et al.  Assessing sediment contamination in estuaries , 2001, Environmental toxicology and chemistry.

[68]  M. Coleman,et al.  Polychaete Richness and Abundance Enhanced in Anthropogenically Modified Estuaries Despite High Concentrations of Toxic Contaminants , 2013, PloS one.

[69]  G. Quinn,et al.  Experimental Design and Data Analysis for Biologists , 2002 .

[70]  E. Johnston,et al.  Contaminants reduce the richness and evenness of marine communities: a review and meta-analysis. , 2009, Environmental pollution.

[71]  Mark V Brown,et al.  Bacterial communities are sensitive indicators of contaminant stress. , 2012, Marine pollution bulletin.

[72]  Michael Elliott,et al.  A typology of marine and estuarine hazards and risks as vectors of change: A review for vulnerable coasts and their management , 2014 .

[73]  A. Chariton,et al.  DNA Metabarcoding Meets Experimental Ecotoxicology: Advancing Knowledge on the Ecological Effects of Copper in Freshwater Ecosystems , 2014 .