Monitoring mosquito richness in an understudied area: can environmental DNA metabarcoding be a complementary approach to adult trapping?

Mosquito surveillance programmes are essential to assess the risks of local vector-borne disease outbreaks as well as for early detection of mosquito invasion events. Surveys are usually performed with traditional sampling tools (i.e., ovitraps and dipping method for immature stages or light or decoy traps for adults). Over the past decade, numerous studies have highlighted that environmental DNA (eDNA) sampling can enhance invertebrate species detection and provide community composition metrics. However, the usefulness of eDNA for detection of mosquito species has, to date, been largely neglected. Here, we sampled water from potential larval breeding sites along a gradient of anthropogenic perturbations, from the core of an oil palm plantation to the rainforest on São Tomé Island (Gulf of Guinea, Africa). We showed that (i) species of mosquitoes could be detected via metabarcoding mostly when larvae were visible, (ii) larvae species richness was greater using eDNA than visual identification and (iii) new mosquito species were also detected by the eDNA approach. We provide a critical discussion of the pros and cons of eDNA metabarcoding for monitoring mosquito species diversity and recommendations for future research directions that could facilitate the adoption of eDNA as a tool for assessing insect vector communities.

[1]  Benjamin D. Kaehler,et al.  RESCRIPt: Reproducible sequence taxonomy reference database management , 2021, PLoS Comput. Biol..

[2]  C. Antonio-Nkondjio,et al.  An update on the mosquito fauna and mosquito-borne diseases distribution in Cameroon , 2021, Parasites & vectors.

[3]  K. Hanley,et al.  Shifts in mosquito diversity and abundance along a gradient from oil palm plantations to conterminous forests in Borneo. , 2021, Ecosphere.

[4]  David L. Smith,et al.  Modelling distributions of Aedes aegypti and Aedes albopictus using climate, host density and interspecies competition , 2021, PLoS neglected tropical diseases.

[5]  P. Dambach The use of aquatic predators for larval control of mosquito disease vectors: Opportunities and limitations , 2020 .

[6]  P. Beja,et al.  Species detection from aquatic eDNA: Assessing the importance of capture methods , 2020, Environmental DNA.

[7]  T. Iwamura,et al.  Accelerating invasion potential of disease vector Aedes aegypti under climate change , 2020, Nature Communications.

[8]  K. Balasingham,et al.  Using environmental DNA metabarcoding to map invasive and native invertebrates in two Great Lakes tributaries , 2020 .

[9]  Durrell D. Kapan,et al.  Patterns, Drivers, and Challenges of Vector-Borne Disease Emergence. , 2019, Vector borne and zoonotic diseases.

[10]  Wan-Yu Lin,et al.  Effects of indoor residual spraying and outdoor larval control on Anopheles coluzzii from São Tomé and Príncipe, two islands with pre-eliminated malaria , 2019, Malaria Journal.

[11]  H. Hillebrand,et al.  Rapid reorganization of global biodiversity , 2019, Science.

[12]  A. Escudero,et al.  Estimating belowground plant abundance with DNA metabarcoding , 2019, Molecular ecology resources.

[13]  P. Bodegom,et al.  How Does eDNA Compare to Traditional Trapping? Detecting Mosquito Communities in South-African Freshwater Ponds , 2019, Front. Ecol. Evol..

[14]  M. Schrama,et al.  Field Evaluation of DNA Based Biodiversity Monitoring of Caribbean Mosquitoes , 2019, Front. Ecol. Evol..

[15]  C. Wondji,et al.  Update on the geographical distribution and prevalence of Aedes aegypti and Aedes albopictus (Diptera: Culicidae), two major arbovirus vectors in Cameroon , 2019, PLoS neglected tropical diseases.

[16]  Kristine M. Smith,et al.  Infectious disease and economics: The case for considering multi-sectoral impacts , 2019, One Health.

[17]  Md Saydur Rahman,et al.  Past, present, and future perspectives of environmental DNA (eDNA) metabarcoding: A systematic review in methods, monitoring, and applications of global eDNA , 2019, Global Ecology and Conservation.

[18]  Anne E Jones,et al.  Impact of recent and future climate change on vector‐borne diseases , 2018, Annals of the New York Academy of Sciences.

[19]  D. Sims,et al.  Persistence of environmental DNA in marine systems , 2018, Communications Biology.

[20]  J. C. Brito,et al.  Challenges for assessing vertebrate diversity in turbid Saharan water-bodies using environmental DNA. , 2018, Genome.

[21]  Kristian Meissner,et al.  Implementation options for DNA-based identification into ecological status assessment under the European Water Framework Directive. , 2018, Water research.

[22]  D. Weetman,et al.  Detection and quantification of Anopheles gambiae sensu lato mosquito larvae in experimental aquatic habitats using environmental DNA (eDNA). , 2018, Wellcome open research.

[23]  Benjamin D. Kaehler,et al.  Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin , 2018, Microbiome.

[24]  Holly M. Bik,et al.  Acidity promotes degradation of multi-species environmental DNA in lotic mesocosms , 2018, Communications Biology.

[25]  E. Garcia-Vazquez,et al.  eDNA for detection of five highly invasive molluscs. A case study in urban rivers from the Iberian Peninsula , 2017, PloS one.

[26]  Kristy Deiner,et al.  Environmental DNA metabarcoding: Transforming how we survey animal and plant communities , 2017, Molecular ecology.

[27]  C. Haddad,et al.  eDNA metabarcoding: a promising method for anuran surveys in highly diverse tropical forests , 2017, Molecular ecology resources.

[28]  Andrew S. Buxton,et al.  Is the detection of aquatic environmental DNA influenced by substrate type? , 2017, PloS one.

[29]  A. Cornel,et al.  First record of Aedes albopictus (Skuse 1894) on São tomé island. , 2017, Acta tropica.

[30]  P. Somboon,et al.  Culex (Culiciomyia) sasai (Diptera: Culicidae), senior synonym of Cx. spiculothorax and a new country record for Bhutan. , 2017, Acta tropica.

[31]  Carol A. Stepien,et al.  Environmental DNA (eDNA) metabarcoding assays to detect invasive invertebrate species in the Great Lakes , 2017, PloS one.

[32]  J. Amberg,et al.  Comparing Efficiency of American Fisheries Society Standard Snorkeling Techniques to Environmental DNA Sampling Techniques , 2017 .

[33]  M. Úriz,et al.  Spatio-temporal monitoring of deep-sea communities using metabarcoding of sediment DNA and RNA , 2016, PeerJ.

[34]  L. Waits,et al.  Critical considerations for the application of environmental DNA methods to detect aquatic species , 2016 .

[35]  Ben Nichols,et al.  VSEARCH: a versatile open source tool for metagenomics , 2016, PeerJ.

[36]  Pierre Taberlet,et al.  Detection of Invasive Mosquito Vectors Using Environmental DNA (eDNA) from Water Samples , 2016, PloS one.

[37]  Tony Brooks,et al.  Accurate Sample Assignment in a Multiplexed, Ultrasensitive, High-Throughput Sequencing Assay for Minimal Residual Disease. , 2016, The Journal of molecular diagnostics : JMD.

[38]  P. Taberlet,et al.  Spatial Representativeness of Environmental DNA Metabarcoding Signal for Fish Biodiversity Assessment in a Natural Freshwater System , 2016, PloS one.

[39]  Måns Magnusson,et al.  MultiQC: summarize analysis results for multiple tools and samples in a single report , 2016, Bioinform..

[40]  A. Piaggio,et al.  No filters, no fridges: a method for preservation of water samples for eDNA analysis , 2016, BMC Research Notes.

[41]  B. Azhar,et al.  Effects of monoculture and polyculture farming in oil palm smallholdings on terrestrial arthropod diversity , 2016 .

[42]  B. Deagle,et al.  Quantitative DNA metabarcoding: improved estimates of species proportional biomass using correction factors derived from control material , 2016, Molecular ecology resources.

[43]  K. McKelvey,et al.  Sampling large geographic areas for rare species using environmental DNA: a study of bull trout Salvelinus confluentus occupancy in western Montana. , 2016, Journal of fish biology.

[44]  P. Taberlet,et al.  Next‐generation monitoring of aquatic biodiversity using environmental DNA metabarcoding , 2016, Molecular ecology.

[45]  D. Segan,et al.  A global assessment of current and future biodiversity vulnerability to habitat loss–climate change interactions , 2016 .

[46]  M. Bonkowski,et al.  Not all are free‐living: high‐throughput DNA metabarcoding reveals a diverse community of protists parasitizing soil metazoa , 2015, Molecular ecology.

[47]  Rafael Gutiérrez-López,et al.  Comparison of Manual and Semi-Automatic DNA Extraction Protocols for the Barcoding Characterization of Hematophagous Louse Flies (Diptera: Hippoboscidae) , 2015, Journal of vector ecology : journal of the Society for Vector Ecology.

[48]  Jim Foster,et al.  Using eDNA to develop a national citizen science-based monitoring programme for the great crested newt (Triturus cristatus) , 2015 .

[49]  L. Waits,et al.  Using environmental DNA methods to improve detectability in a hellbender (Cryptobranchus alleganiensis) monitoring program , 2015 .

[50]  Philippe Esling,et al.  Accurate multiplexing and filtering for high-throughput amplicon-sequencing , 2015, Nucleic acids research.

[51]  A. Piaggio,et al.  Detecting an elusive invasive species: a diagnostic PCR to detect Burmese python in Florida waters and an assessment of persistence of environmental DNA , 2014, Molecular ecology resources.

[52]  Robert S. Arkle,et al.  Factors influencing detection of eDNA from a stream‐dwelling amphibian , 2014, Molecular ecology resources.

[53]  W. L. Chadderton,et al.  Environmental conditions influence eDNA persistence in aquatic systems. , 2014, Environmental science & technology.

[54]  A. Manirakiza,et al.  Temporal Patterns of Abundance of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) and Mitochondrial DNA Analysis of Ae. albopictus in the Central African Republic , 2013, PLoS neglected tropical diseases.

[55]  A. James,et al.  The invasive mosquito species Aedes albopictus: current knowledge and future perspectives. , 2013, Trends in parasitology.

[56]  M. Coetzee,et al.  Molecular systematics and insecticide resistance in the major African malaria vector Anopheles funestus. , 2013, Annual review of entomology.

[57]  C. Wiuf,et al.  Monitoring endangered freshwater biodiversity using environmental DNA. , 2012, Molecular ecology.

[58]  Z. Kawabata,et al.  Surveillance of fish species composition using environmental DNA , 2012, Limnology.

[59]  S. Salzberg,et al.  FLASH: fast length adjustment of short reads to improve genome assemblies , 2011, Bioinform..

[60]  François Pompanon,et al.  Persistence of Environmental DNA in Freshwater Ecosystems , 2011, PloS one.

[61]  Robert S. Arkle,et al.  Molecular Detection of Vertebrates in Stream Water: A Demonstration Using Rocky Mountain Tailed Frogs and Idaho Giant Salamanders , 2011, PloS one.

[62]  Rob Knight,et al.  UCHIME improves sensitivity and speed of chimera detection , 2011, Bioinform..

[63]  Marcel Martin Cutadapt removes adapter sequences from high-throughput sequencing reads , 2011 .

[64]  Jake L. Snaddon,et al.  Oil palm expansion into rain forest greatly reduces ant biodiversity in canopy, epiphytes and leaf-litter , 2010 .

[65]  F. Simard,et al.  Comparative role of Aedes albopictus and Aedes aegypti in the emergence of Dengue and Chikungunya in central Africa. , 2010, Vector borne and zoonotic diseases.

[66]  W. Stolk,et al.  The role of monitoring mosquito infection in the Global Programme to Eliminate Lymphatic Filariasis. , 2009, Trends in parasitology.

[67]  S. Juliano Species interactions among larval mosquitoes: context dependence across habitat gradients. , 2009, Annual review of entomology.

[68]  P. Taberlet,et al.  Species detection using environmental DNA from water samples , 2008, Biology Letters.

[69]  L. P. Koh,et al.  Is oil palm agriculture really destroying tropical biodiversity? , 2008 .

[70]  S. Ball,et al.  Rapid, One-Step DNA Extraction for Insect Pest Identification by Using DNA Barcodes , 2008, Journal of economic entomology.

[71]  R. Wilkerson,et al.  Insight into Global Mosquito Biogeography from Country Species Records , 2007, Journal of medical entomology.

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

[73]  P. Hebert,et al.  DNA barcoding: how it complements taxonomy, molecular phylogenetics and population genetics. , 2007, Trends in genetics : TIG.

[74]  M. Ferdig,et al.  DNA barcoding of parasites and invertebrate disease vectors: what you don't know can hurt you. , 2003, Trends in parasitology.

[75]  P. Taberlet,et al.  Urine collected in the field as a source of DNA for species and individual identification , 2000, Molecular ecology.

[76]  W. Reisen,et al.  Effects of sampling design on the estimation of adult mosquito abundance. , 1999, Journal of the American Mosquito Control Association.