Abstract
Saline and hypersaline wetlands account for almost half of the volume of inland water globally. They provide pivotal habitat for a vast range of species, including crucial ecosystem services for humans such as carbon sink storage and extractive resource reservoirs. Despite their importance, effective ecological assessment is in its infancy compared to current conventional surveys carried out in freshwater ecosystems. The integration of environmental DNA (eDNA) analysis and traditional techniques has the potential to transform biomonitoring processes, particularly in remote and understudied saline environments. In this context, this preliminary study aims to explore the potential of eDNA coupled with conventional approaches by targeting five hypersaline lakes at Rottnest Island (Wadjemup) in Western Australia. We focused on the invertebrate community, a widely accepted key ecological indicator to assess the conservational status in rivers and lakes. The combination of metabarcoding with morphology-based taxonomic analysis described 16 taxa belonging to the orders Anostraca, Diptera, Isopoda, and Coleoptera. DNA-based diversity assessment revealed more taxa at higher taxonomic resolution than the morphology-based taxonomic analysis. However, certain taxa (i.e., Ephydridae, Stratyiomidae, Ceratopogonidae) were only identified via net surveying. Overall, our results indicate that great potential resides in combining conventional net-based surveys with novel eDNA approaches in saline and hypersaline lakes. Indeed, urgent and effective conservational frameworks are required to contrast the enormous pressure that these ecosystems are increasingly facing. Further investigations at larger spatial-temporal scales will allow consolidation of robust, reliable, and affordable biomonitoring frameworks in the underexplored world of saline wetlands.
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Taxonomy data can be found at github.com/MACampbell91/Nets-meet-eDNA-in-salt-lakes.
References
Adler P H, Courtney G W. 2019. Ecological and societal services of aquatic Diptera. Insects, 10(3): 70, https://doi.org/10.3390/insects10030070.
Altschul S F, Gish W, Miller W et al. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215(3): 403–410, https://doi.org/10.1016/S0022-2836(05)80360-2.
Asem A, Eimanifar A, Rastegar-Pouyani N et al. 2020. An overview on the nomenclatural and phylogenetic problems of native Asian brine shrimps of the genus Artemia Leach, 1819 (Crustacea, Anostraca). ZooKeys, 902: 1–15, https://doi.org/10.3897/zookeys.902.34593.
Asem A, Rastegar-Pouyani N, De Los Ríos-Escalante P. 2010. The genus Artemia leach, 1819 (Crustacea: Branchiopoda). I. True and false taxonomical descriptions. Latin American Journal of Aquatic Research, 38(3): 501–506, https://doi.org/10.3856/vol38-issue3-fulltext-14.
Barnes M A, Turner C R, Jerde C L et al. 2014. Environmental conditions influence eDNA persistence in aquatic systems. Environmental Science & Technology, 48(3): 1819–1827, https://doi.org/10.1021/es404734p.
Blackman R C, Brantschen J, Walser J C et al. 2022. Monitoring invasive alien macroinvertebrate species with environmental DNA. River Research and Applications, 38(8): 1400–1412, https://doi.org/10.1002/rra.3947.
Blanchette M L, Allcock R, Gonzalez J et al. 2020. Macroinvertebrates and microbes (archaea, bacteria) offer complementary insights into mine-pit lake ecology. Mine Water and the Environment, 39(3): 589–602, https://doi.org/10.1007/s10230-019-00647-9.
Brantschen J, Blackman R C, Walser J C et al. 2021. Environmental DNA gives comparable results to morphology-based indices of macroinvertebrates in a large-scale ecological assessment. PLoS One, 16(9): e0257510, https://doi.org/10.1371/journal.pone.0257510.
Chessman B C, Trayler K M, Davis J A. 2002. Family- and species-level biotic indices for macroinvertebrates of wetlands on the Swan Coastal Plain, Western Australia. Marine and Freshwater Research, 53(5): 919–930, https://doi.org/10.1071/MF00079.
Davis J A, Christidis F. 1997. A Guide to Wetland Invertebrates of Southwestern Australia. Western Australian Museum for Urban Water Research Association of Australia, Water and Rivers Commission, Land and Water Resources Research and Development Corporation.
De Deckker P, Geddes M C. 1980. Seasonal fauna of ephemeral saline lakes near the Coorong Lagoon, South Australia. Marine and Freshwater Research, 31(5): 677–699, https://doi.org/10.1071/mf9800677.
Diaz R J, Solan M, Valente R M. 2004. A review of approaches for classifying benthic habitats and evaluating habitat quality. Journal of Environmental Management, 73(3): 165–181, https://doi.org/10.1016/j.jenvman.2004.06.004.
Edgar R C. 2016. UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing, https://doi.org/10.1101/081257.
Edward D H D. 1983. Inland waters of Rottnest Island in Pen L J, Grecn J W. Research on Rottnest Island. Journal of the Royal Society of Western Australia, 66: 1.
Elbourne, L D H, Sutcliffe B., Humphreys W, et al. 2022. Unravelling stratified microbial assemblages in Australia’s only deep anchialine system, the Bundera Sinkhole. Frontiers in Marine Science, 9: 872082, https://doi.org/10.3389/fmars.2022.872082.
Elbrecht V, Leese F. 2015. Can DNA-based ecosystem assessments quantify species abundance? Testing primer bias and biomass-sequence relationships with an innovative metabarcoding protocol. PLoS One, 10(7): e0130324, https://doi.org/10.1371/journal.pone.0130324.
Griffith M B. 2017. Toxicological perspective on the osmoregulation and ionoregulation physiology of major ions by freshwater animals: teleost fish, Crustacea, aquatic insects, and Mollusca. Environmental Toxicology and Chemistry, 36(3): 576–600, https://doi.org/10.1002/etc.3676.
Halse S A. 1981. Faunal assemblages of some saline lakes near Marchagee, Western Australia. Marine and Freshwater Research, 32(1): 133–142, https://doi.org/10.1071/MF9810133.
How R A, Dell J. 1994. The zoogeographic significance of urban bushland remnants to reptiles in the Perth region, Western Australia. Pacific Conservation Biology, 1(2): 132–140.
Jackson D A. 1995. PROTEST: a PROcrustean randomization TEST of community environment concordance. Écoscience, 2(3): 297–303, https://doi.org/10.1080/11956860.1995.11682297.
Jackson R. 2008. Playing lotto with rotto? Tourism, the environment and gambling with the ethos of a Western Australian island. Australian Geographer, 39(4): 495–519, https://doi.org/10.1080/00049180802419211.
Kelly R P, Closek C J, O’Donnell J L et al. 2017. Genetic and manual survey methods yield different and complementary views of an ecosystem. Frontiers in Marine Science, 3: 283, https://doi.org/10.3389/fmars.2016.00283.
Laini A, Beermann A J, Bolpagni R et al. 2020. Exploring the potential of metabarcoding to disentangle macroinvertebrate community dynamics in intermittent streams. Metabarcoding and Metagenomics, 4: e51433, https://doi.org/10.3897/mbmg.4.51433.
Laini A, Stubbington R, Beerman A et al. 2023. Dissecting biodiversity: assessing the taxonomic, functional and phylogenetic structure of an insect metacommunity in a river network using morphological and metabarcoding data. European Zoological Journal, 90(1): 320–332, https://doi.org/10.1080/24750263.2023.2197924.
Lerman A. 2009. Saline Lakes’ response to global change. Aquatic Geochemistry, 15(1–2): 1–5, https://doi.org/10.1007/s10498-008-9058-8.
Macher J N, Salis R K, Blakemore K S et al. 2016. Multiple-stressor effects on stream invertebrates: DNA barcoding reveals contrasting responses of cryptic mayfly species. Ecological Indicators, 61: 159–169, https://doi.org/10.1016/j.ecolind.2015.08.024.
McClenaghan B, Fahner N, Cote D et al. 2020. Harnessing the power of eDNA metabarcoding for the detection of deep-sea fishes. PLoS One, 15(11): e0236540, https://doi.org/10.1371/journal.pone.0236540.
McMaster K, Savage A, Finston T et al. 2007. The recent spread of Artemia parthenogenetica in Western Australia. Hydrobiologia, 576(1): 39–48, https://doi.org/10.1007/s10750-006-0291-0.
Mieczan T, Tarkowska-Kukuryk M, Ârva D et al. 2018. The effect of epiphytic macroinvertebrates on microbial communities in different types of macrophyte-dominated shallow lakes. Knowledge & Management of Aquatic Ecosystems, 419: 13, https://doi.org/10.1051/kmae/2017060.
Mohebbi F. 2010. The brine shrimp Artemia and hypersaline environments microalgal composition: a mutual interaction. International Journal of Aquatic Science, 1: 19–27.
Mousavi-Derazmahalleh M, Stott A, Lines R et al. 2021. eDNAFlow, an automated, reproducible and scalable workflow for analysis of environmental DNA sequences exploiting Nextflow and Singularity. Molecular Ecology Resources, 21(5): 1697–1704, https://doi.org/10.1111/1755-0998.13356.
Muha T P, Robinson C V, de Leaniz C G et al. 2019. An optimised eDNA protocol for detecting fish in lentic and lotic freshwaters using a small water volume. PLoS One, 14(7): e0219218, https://doi.org/10.1371/journal.pone.0219218.
Nicholls D G. 1971. Daily and seasonal movements of the quokka, Setinux brachyurus (Marsupialia), on Rottnest Island. Australian Journal of Zoology, 19(3): 215–226, https://doi.org/10.1071/ZO9710215.
Oksanen J, Blanchet F G, Friendly M et al. 2020. Vegan: Community Ecology Package. R package version 2.6–4. https://CRAN.R-project.org/package=vegan.
Pallarés S, Botella-Cruz M, Arribas P et al. 2017. Aquatic insects in a multistress environment: cross-tolerance to salinity and desiccation. Journal of Experimental Biology, 220(7): 1277–1286, https://doi.org/10.1242/jeb.152108.
Pawlowski J, Kelly-Quinn M, Altermatt F et al. 2018. The future of biotic indices in the ecogenomic era: integrating (e) DNA metabarcoding in biological assessment of aquatic ecosystems. Science of the Total Environment, 637–638: 1295–1310, https://doi.org/10.1016/j.scitotenv.2018.05.002.
Perina G, Camacho A I, Cooper S J B et al. 2022. An integrated approach to explore the monophyletic status of the cosmopolitan genus Hexabathynella (Crustacea, Bathynellacea, Parabathynellidae): two new species from Rottnest Island (Wadjemup), Western Australia. Systematics and Biodiversity, 21(1): 2151662.
Perkins P D. 2007. A review of the coastal marsh water beetle Ochthebius queenslandicus Hansen (Coleoptera: Hydraenidae). Zootaxa, 1625(1): 35–42, https://doi.org/10.11646/zootaxa.1625.1.2.
R Core Team. 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.
Saccò M, Gómez V G, Sevilla J R et al. 2020. Exploratory study on the optimisation of sampling effort in a non-vegetated lagoon within a Mediterranean wetland (Albufera Natural Park, Valencia, Spain). Ecological Indicators, 117(3): 106538, https://doi.org/10.1016/j.ecolind.2020.106538.
Saccò M, Guzik M T, van der Heyde M et al. 2022. eDNA in subterranean ecosystems: applications, technical aspects, and future prospects. Science of the Total Environment, 820: 153223, https://doi.org/10.1016/j.scitotenv.2022.153223.
Saccò M, White N E, Campbell M et al. 2021b. Metabarcoding under brine: microbial ecology of five hypersaline lakes at Rottnest Island (WA, Australia). Water, 13(14): 1899, https://doi.org/10.3390/w13141899.
Saccò M, White N E, Harrod C et al. 2021a. Salt to conserve: a review on the ecology and preservation of hypersaline ecosystems. Biological Reviews, 96(6): 2828–2850, https://doi.org/10.1111/brv.12780.
Sainz-Escudero L, López-Estrada E K, Rodríguez-Flores P C et al. 2021. Settling taxonomic and nomenclatural problems in brine shrimps, Artemia (Crustacea: Branchiopoda: Anostraca), by integrating mitogenomics, marker discordances and nomenclature rules. Peer J, 9: e10865, https://doi.org/10.7717/peerj.10865.
Sánchez M I, Paredes I, Lebouvier M et al. 2016. Functional role of native and invasive filter-feeders, and the effect of parasites: learning from hypersaline ecosystems. PLoS One, 11(8): e0161478, https://doi.org/10.1371/journal.pone.0161478.
Saunders D A, De Rebeira P. 2009. A case study of the conservation value of a small tourist resort island: birds of Rottnest Island, Western Australia 1905–2007. Pacific Conservation Biology, 15(1): 11–31, https://doi.org/10.1071/PC090011.
Schaffner F, Medlock J M, Van Bortel W. 2013. Public health significance of invasive mosquitoes in Europe. Clinical Microbiology and Infection, 19(8): 685–692, https://doi.org/10.1111/1469-0691.12189.
Schmidt M, Gonda R, Transiskus S. 2021. Environmental degradation at Lake Urmia (Iran): exploring the causes and their impacts on rural livelihoods. GeoJournal, 86(5): 2149–2163.
Takahashi M, Saccò M, Kestel J H et al. 2023. Aquatic environmental DNA: A review of the macro-organismal biomonitoring revolution. Science of The Total Environment, 162322, https://doi.org/10.1016/j.scitotenv.2023.162322.
Thomsen P F, Willerslev E. 2015. Environmental DNA—an emerging tool in conservation for monitoring past and present biodiversity. Biological Conservation, 183: 4–18, https://doi.org/10.1016/j.biocon.2014.11.019.
Timms B V. 2022. Aquatic invertebrate community structure and phenology of the intermittent treed swamps of the semi-arid Paroo lowlands in Australia. Wetlands Ecology and Management, 30(4): 771–784, https://doi.org/10.1007/s11273-021-09846-0.
Vamos E E, Elbrecht V, Leese F. 2017. Short COI markers for freshwater macroinvertebrate metabarcoding. Metabarcoding and Metagenomics, 1: e14625, https://doi.org/10.3897/mbmg.1.14625.
Varó I, Redón S, Garcia-Roger E M et al. 2015. Aquatic pollution may favor the success of the invasive species A. franciscana. Aquatic Toxicology, 161: 208–220, https://doi.org/10.1016/j.aquatox.2015.02.008.
Velasco J, Millán A, Hernández J et al. 2006. Response of biotic communities to salinity changes in a Mediterranean hypersaline stream. Saline Systems, 2: 12, https://doi.org/10.1186/1746-1448-2-12.
Wallace J B, Webster J R. 1996. The role of macroinvertebrates in stream ecosystem function. Annual Review of Entomology, 41: 115–139, https://doi.org/10.1146/annurev.en.41.010196.000555.
West K M, Stat M, Harvey E S et al. 2020. eDNA metabarcoding survey reveals fine-scale coral reef community variation across a remote, tropical island ecosystem. Molecular Ecology, 29(6): 1069–1086, https://doi.org/10.1111/mec.15382.
Williams W D. 1983. On the ecology of Haloniscus searlei (Isopoda, Oniscoidea), an inhabitant of Australian salt lakes. Hydrobiologia, 105(1): 137–142, https://doi.org/10.1007/BF00025183.
Wurtsbaugh W A, Miller C, Null S E et al. 2017. Decline of the world’s saline lakes. Nature Geoscience, 10(11): 816–821, https://doi.org/10.1038/ngeo3052.
Yates M C, Fraser D J, Derry A M. 2019. Meta-analysis supports further refinement of eDNA for monitoring aquatic species-specific abundance in nature. Environmental DNA, 1(1): 5–13, https://doi.org/10.1002/edn3.7.
Zadereev E, Lipka O, Karimov B et al. 2020. Overview of past, current, and future ecosystem and biodiversity trends of inland saline lakes of Europe and Central Asia. Inland Waters, 10(4): 438–452, https://doi.org/10.1080/20442041.2020.1772034.
Acknowledgment
We wish to acknowledge the Traditional Custodians of this Island, the Whadjuk people of the Noongar Nation, their ancestors and their Elders past, present and emerging. We acknowledge and respect their continuing culture and the contribution they make to the life of the Perth and Rottnest Island (Wadjemup) regions. This work was supported by resources provided by the Pawsey Supercomputing Centre with funding from the Australian Government and the Government of Western Australia. M. S. and N. E. W acknowledge support from the BHP-Curtin alliance within the framework of the “eDNA for Global Environment Studies (eDGES)” program.
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Supported by the Curtin-BHP alliance within the framework of the “eDNA for Global Environment Studies (eDGES)” program
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Campbell, M.A., Laini, A., White, N.E. et al. When nets meet environmental DNA metabarcoding: integrative approach to unveil invertebrate community patterns of hypersaline lakes. J. Ocean. Limnol. 41, 1331–1340 (2023). https://doi.org/10.1007/s00343-022-2151-9
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DOI: https://doi.org/10.1007/s00343-022-2151-9