Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH FRONT (Open Access)

A muddy time capsule: using sediment environmental DNA for the long-term monitoring of coastal vegetated ecosystems

N. R. Foster A D , B. M. Gillanders A , A. R. Jones A , J. M. Young B and M. Waycott https://orcid.org/0000-0002-0822-0564 A C
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, University of Adelaide, Adelaide, SA 5005, Australia.

B College of Science and Engineering, Flinders University, Bedford Park, SA 5042, Australia.

C State Herbarium of South Australia, Botanic Gardens and State Herbarium, Department of Environment and Water (DEW), Adelaide, SA 5001, Australia.

D Corresponding author. Email: nicole.foster@adelaide.edu.au

Marine and Freshwater Research 71(8) 869-876 https://doi.org/10.1071/MF19175
Submitted: 15 May 2019  Accepted: 23 January 2020   Published: 16 March 2020

Journal Compilation © CSIRO 2020 Open Access CC BY-NC-ND

Abstract

Seagrass, saltmarsh and mangrove habitats are declining around the world as anthropogenic activity and climate change intensify. To be able to effectively restore and maintain healthy coastal-vegetation communities, we must understand how and why they have changed in the past. Identifying shifts in vegetation communities, and the environmental or human drivers of these, can inform successful management and restoration strategies. Unfortunately, long-term data (i.e. decades to hundreds of years) on coastal vegetated ecosystems that can discern community-level changes are mostly non-existent in the scientific record. We propose implementing DNA extracted from coastal sediments to provide an alternative approach to long-term ecological reconstruction for coastal vegetated ecosystems. This type of DNA is called ‘environmental DNA’ and has previously been used to generate long-term datasets for other vegetated systems but has not yet been applied to vegetation change in coastal settings. In this overview, we explore the idea of using sediment eDNA as a long-term monitoring tool for seagrass, saltmarsh and mangrove communities. We see real potential in this approach for reconstructing long-term ecological histories of coastal vegetated ecosystems, and advocate that further research be undertaken to develop appropriate methods for its use.

Additional keywords: climate change, eDNA, mangrove, saltmarsh, seagrass.


References

Adams, C. I. M., Knapp, M., Gemmell, N. J., Jeunen, G. J., Bunce, M., Lamare, M. D., and Taylor, H. R. (2019). Beyond biodiversity: can environmental DNA (eDNA) cut it as a population genetics tool? Genes 10, 192.
Beyond biodiversity: can environmental DNA (eDNA) cut it as a population genetics tool?Crossref | GoogleScholarGoogle Scholar |

Alongi, D. M. (2008). Mangrove forests: resilience, protection from tsunamis, and responses to global climate change. Estuarine, Coastal and Shelf Science 76, 1–13.
Mangrove forests: resilience, protection from tsunamis, and responses to global climate change.Crossref | GoogleScholarGoogle Scholar |

Bálint, M., Pfenninger, M., Grossart, H. P., Taberlet, P., Vellend, M., Leibold, M. A., Englund, G., and Bowler, D. (2018). Environmental DNA time series in ecology. Trends in Ecology & Evolution 33, 945–957.
Environmental DNA time series in ecology.Crossref | GoogleScholarGoogle Scholar |

Barbier, E. B., Hacker, S. D., Kennedy, C., Koch, E. W., Stier, A. C., and Silliman, B. R. (2011). The value of estuarine and coastal ecosystem services. Ecological Monographs 81, 169–193.
The value of estuarine and coastal ecosystem services.Crossref | GoogleScholarGoogle Scholar |

Boero, F., Kraberg, A. C., Krause, G., and Wiltshire, K. H. (2015). Time is an affliction: why ecology cannot be as predictive as physics and why it needs time series. Journal of Sea Research 101, 12–18.
Time is an affliction: why ecology cannot be as predictive as physics and why it needs time series.Crossref | GoogleScholarGoogle Scholar |

Boessenkool, S., McGlynn, G., Epp, L. S., Taylor, D., Pimentel, M., Gizaw, A., Nemomissa, S., Brochmann, C., and Popp, M. (2014). Use of ancient sedimentary DNA as a novel conservation tool for high-altitude tropical biodiversity. Conservation Biology 28, 446–455.
Use of ancient sedimentary DNA as a novel conservation tool for high-altitude tropical biodiversity.Crossref | GoogleScholarGoogle Scholar | 24372820PubMed |

Breed, M. F., Lowe, A. J., and Mortimer, P. E. (2016). Restoration: ‘garden of Eden’ unrealistic. Nature 533, 469.
Restoration: ‘garden of Eden’ unrealistic.Crossref | GoogleScholarGoogle Scholar | 27225110PubMed |

Cohen, M. C. L., Pessenda, L. C. R., Behling, H., de Fátima Rossetti, D., França, M. C., Guimarães, J. T. F., Friaes, Y., and Smith, C. B. (2012). Holocene palaeoenvironmental history of the Amazonian mangrove belt. Quaternary Science Reviews 55, 50–58.
Holocene palaeoenvironmental history of the Amazonian mangrove belt.Crossref | GoogleScholarGoogle Scholar |

Costanza, R., Graumlich, L., Steffen, W., Crumley, C., Dearing, J., Hibbard, K., Leemans, R., Redman, C., and Schimel, D. (2007). Sustainability or collapse: what can we learn from integrating the history of humans and the rest of nature? Ambio 36, 522–527.
Sustainability or collapse: what can we learn from integrating the history of humans and the rest of nature?Crossref | GoogleScholarGoogle Scholar | 18074887PubMed |

Costanza, R., de Groot, R., Sutton, P., van der Ploeg, S., Anderson, S. J., Kubiszewski, I., Farber, S., and Turner, R. K. (2014). Changes in the global value of ecosystem services. Global Environmental Change 26, 152–158.
Changes in the global value of ecosystem services.Crossref | GoogleScholarGoogle Scholar |

Cristescu, M. E., and Hebert, P. D. (2018). Uses and misuses of environmental DNA in biodiversity science and conservation. Annual Review of Ecology, Evolution, and Systematics 49, 209–230.
Uses and misuses of environmental DNA in biodiversity science and conservation.Crossref | GoogleScholarGoogle Scholar |

Danovaro, R., Carugati, L., Berzano, M., Cahill, A. E., Carvalho, S., Chenuil, A., Corinaldesi, C., Cristina, S., David, R., Dell’Anno, A., Dzhembekova, N., Garcés, E., Gasol, J. M., Goela, P., Féral, J.-P., Ferrera, I., Forster, R. M., Kurekin, A. A., Rastelli, E., Marinova, V., Miller, P. I., Moncheva, S., Newton, A., Pearman, J. K., Pitois, S. G., Reñé, A., Rodríguez-Ezpeleta, N., Saggiomo, V., Simis, S. G. H., Stefanova, K., Wilson, C., Lo Martire, M., Greco, S., Cochrane, S. K. J., Mangoni, O., and Borja, A. (2016). Implementing and innovating marine monitoring approaches for assessing marine environmental status. Frontiers in Marine Science 3, 213.
Implementing and innovating marine monitoring approaches for assessing marine environmental status.Crossref | GoogleScholarGoogle Scholar |

Dormontt, E. E., Van Dijk, K.-j., Bell, K. L., Biffin, E., Breed, M. F., Byrne, M., Caddy-Retalic, S., Encinas-Viso, F., Neville, P., and Shapcott, A. (2018). Advancing DNA metabarcoding applications for plants requires systematic analysis of herbarium collections: an Australian perspective. Frontiers in Ecology and Evolution 6, 134.
Advancing DNA metabarcoding applications for plants requires systematic analysis of herbarium collections: an Australian perspective.Crossref | GoogleScholarGoogle Scholar |

Duffy, J. E., Benedetti-Cecchi, L., Trinanes, J., Muller-Karger, F. E., Ambo-Rappe, R., Boström, C., Buschmann, A. H., Byrnes, J., Coles, R. G., Creed, J., Cullen-Unsworth, L. C., Diaz-Pulido, G., Duarte, C. M., Edgar, G. J., Fortes, M., Goni, G., Hu, C., Huang, X., Hurd, C. L., Johnson, C., Konar, B., Krause-Jensen, D., Krumhansl, K., Macreadie, P., Marsh, H., McKenzie, L. J., Mieszkowska, N., Miloslavich, P., Montes, E., Nakaoka, M., Norderhaug, K. M., Norlund, L. M., Orth, R. J., Prathep, A., Putman, N. F., Samper-Villarreal, J., Serrao, E. A., Short, F., Pinto, I. S., Steinberg, P., Stuart-Smith, R., Unsworth, R. K. F., van Keulen, M., van Tussenbroek, B. I., Wang, M., Waycott, M., Weatherdon, L. V., Wernberg, T., and Yaakub, S. M. (2019). Toward a coordinated global observing system for seagrasses and marine macroalgae. Frontiers in Marine Science 6, 317.
Toward a coordinated global observing system for seagrasses and marine macroalgae.Crossref | GoogleScholarGoogle Scholar |

Ellegaard, M., Clarke, A. L., Reuss, N., Drew, S., Weckström, K., Juggins, S., Anderson, N. J., and Conley, D. J. (2006). Multi-proxy evidence of long-term changes in ecosystem structure in a Danish marine estuary, linked to increased nutrient loading. Estuarine, Coastal and Shelf Science 68, 567–578.
Multi-proxy evidence of long-term changes in ecosystem structure in a Danish marine estuary, linked to increased nutrient loading.Crossref | GoogleScholarGoogle Scholar |

Epp, L. S., Boessenkool, S., Bellemain, E. P., Haile, J., Esposito, A., Riaz, T., Erseus, C., Gusarov, V. I., Edwards, M. E., Johnsen, A., Stenoien, H. K., Hassel, K., Kauserud, H., Yoccoz, N. G., Brathen, K. A., Willerslev, E., Taberlet, P., Coissac, E., and Brochmann, C. (2012). New environmental metabarcodes for analysing soil DNA: potential for studying past and present ecosystems. Molecular Ecology 21, 1821–1833.
New environmental metabarcodes for analysing soil DNA: potential for studying past and present ecosystems.Crossref | GoogleScholarGoogle Scholar | 22486821PubMed |

Fahner, N. A., Shokralla, S., Baird, D. J., and Hajibabaei, M. (2016). Large-scale monitoring of plants through environmental DNA metabarcoding of soil: recovery, resolution, and annotation of four DNA markers. PLoS One 11, e0157505.
Large-scale monitoring of plants through environmental DNA metabarcoding of soil: recovery, resolution, and annotation of four DNA markers.Crossref | GoogleScholarGoogle Scholar | 27310720PubMed |

Ficetola, G. F., Poulenard, J., Sabatier, P., Messager, E., Gielly, L., Leloup, A., Etienne, D., Bakke, J., Malet, E., and Fanget, B. (2018). DNA from lake sediments reveals long-term ecosystem changes after a biological invasion. Science Advances 4, eaar4292.
DNA from lake sediments reveals long-term ecosystem changes after a biological invasion.Crossref | GoogleScholarGoogle Scholar | 29750197PubMed |

Fordham, D. A., Akçakaya, H. R., Alroy, J., Saltré, F., Wigley, T. M. L., and Brook, B. W. (2016). Predicting and mitigating future biodiversity loss using long-term ecological proxies. Nature Climate Change 6, 909–916.
Predicting and mitigating future biodiversity loss using long-term ecological proxies.Crossref | GoogleScholarGoogle Scholar |

Foster, N. R., Fotheringham, D. G., Brock, D. J., and Waycott, M. (2017). A resourceful and adaptable method to obtain data on the status of seagrass meadows. Aquatic Botany 141, 17–21.
A resourceful and adaptable method to obtain data on the status of seagrass meadows.Crossref | GoogleScholarGoogle Scholar |

García, C. (2019). From ecological indicators to ecological functioning: integrative approaches to seize on ecological, climatic and socio-economic databases. Ecological Indicators 107, 105612.
From ecological indicators to ecological functioning: integrative approaches to seize on ecological, climatic and socio-economic databases.Crossref | GoogleScholarGoogle Scholar |

Gedan, K. B., Silliman, B. R., and Bertness, M. D. (2009). Centuries of human-driven change in salt marsh ecosystems. Annual Review of Marine Science 1, 117–141.
Centuries of human-driven change in salt marsh ecosystems.Crossref | GoogleScholarGoogle Scholar | 21141032PubMed |

Geraldi, N. R., Ortega, A., Serrano, O., Macreadie, P. I., Lovelock, C. E., Krause-Jensen, D., Kennedy, H., Lavery, P. S., Pace, M. L., Kaal, J., and Duarte, C. M. (2019). Fingerprinting blue carbon: rationale and tools to determine the source of organic carbon in marine depositional environments. Frontiers in Marine Science 6, 263.
Fingerprinting blue carbon: rationale and tools to determine the source of organic carbon in marine depositional environments.Crossref | GoogleScholarGoogle Scholar |

Giguet-Covex, C., Pansu, J., Arnaud, F., Rey, P. J., Griggo, C., Gielly, L., Domaizon, I., Coissac, E., David, F., Choler, P., Poulenard, J., and Taberlet, P. (2014). Long livestock farming history and human landscape shaping revealed by lake sediment DNA. Nature Communications 5, 3211.
Long livestock farming history and human landscape shaping revealed by lake sediment DNA.Crossref | GoogleScholarGoogle Scholar | 24487920PubMed |

Giguet-Covex, C., Ficetola, G. F., Walsh, K. J., Poulenard, J., Bajard, M., Fouinat, L., Sabatier, P., Gielly, L., Messager, E., Develle, A.-L., David, F., Taberlet, P., Brisset, E., Guiter, F., Sinet, R., and Arnaud, F. (2019). New insights on lake sediment DNA from the catchment: importance of taphonomic and analytical issues on the record quality. Scientific Reports 9, .
New insights on lake sediment DNA from the catchment: importance of taphonomic and analytical issues on the record quality.Crossref | GoogleScholarGoogle Scholar | 31604959PubMed |

Hart, M. L., Forrest, L. L., Nicholls, J. A., and Kidner, C. A. (2016). Retrieval of hundreds of nuclear loci from herbarium specimens. Taxon 65, 1081–1092.
Retrieval of hundreds of nuclear loci from herbarium specimens.Crossref | GoogleScholarGoogle Scholar |

Jackson, J. B., Kirby, M. X., Berger, W. H., Bjorndal, K. A., Botsford, L. W., Bourque, B. J., Bradbury, R. H., Cooke, R., Erlandson, J., and Estes, J. A. (2001). Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–637.
Historical overfishing and the recent collapse of coastal ecosystems.Crossref | GoogleScholarGoogle Scholar | 11474098PubMed |

Jeunen, G. J., Knapp, M., Spencer, H. G., Lamare, M. D., Taylor, H. R., Stat, M., Bunce, M., and Gemmell, N. J. (2019). Environmental DNA (eDNA) metabarcoding reveals strong discrimination among diverse marine habitats connected by water movement. Molecular Ecology Resources 19, 426–438.
Environmental DNA (eDNA) metabarcoding reveals strong discrimination among diverse marine habitats connected by water movement.Crossref | GoogleScholarGoogle Scholar | 30576077PubMed |

Johnson, B. J., Moore, K. A., Lehmann, C., Bohlen, C., and Brown, T. A. (2007). Middle to late Holocene fluctuations of C3 and C4 vegetation in a Northern New England Salt Marsh, Sprague Marsh, Phippsburg Maine. Organic Geochemistry 38, 394–403.
Middle to late Holocene fluctuations of C3 and C4 vegetation in a Northern New England Salt Marsh, Sprague Marsh, Phippsburg Maine.Crossref | GoogleScholarGoogle Scholar |

Jørgensen, T., Kjaer, K. H., Haile, J., Rasmussen, M., Boessenkool, S., Andersen, K., Coissac, E., Taberlet, P., Brochmann, C., Orlando, L., Gilbert, M. T., and Willerslev, E. (2012). Islands in the ice: detecting past vegetation on Greenlandic nunataks using historical records and sedimentary ancient DNA meta-barcoding. Molecular Ecology 21, 1980–1988.
Islands in the ice: detecting past vegetation on Greenlandic nunataks using historical records and sedimentary ancient DNA meta-barcoding.Crossref | GoogleScholarGoogle Scholar | 21951625PubMed |

Lemmon, A. R., Emme, S. A., and Lemmon, E. M. (2012). Anchored hybrid enrichment for massively high-throughput phylogenomics. Systematic Biology 61, 727–744.
Anchored hybrid enrichment for massively high-throughput phylogenomics.Crossref | GoogleScholarGoogle Scholar | 22605266PubMed |

McAfee, D., Alleway, H. K., and Connell, S. D. (2019). Environmental solutions sparked by environmental history. Conservation Biology , .
Environmental solutions sparked by environmental history.Crossref | GoogleScholarGoogle Scholar | 31385623PubMed |

Mcleod, E., Chmura, G. L., Bouillon, S., Salm, R., Björk, M., Duarte, C. M., Lovelock, C. E., Schlesinger, W. H., and Silliman, B. R. (2011). A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Frontiers in Ecology and the Environment 9, 552–560.
A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2.Crossref | GoogleScholarGoogle Scholar |

Nogués-Bravo, D., Rodriguez-Sanchez, F., Orsini, L., de Boer, E., Jansson, R., Morlon, H., Fordham, D. A., and Jackson, S. T. (2018). Cracking the code of biodiversity responses to past climate change. Trends in Ecology & Evolution 33, 765–776.
Cracking the code of biodiversity responses to past climate change.Crossref | GoogleScholarGoogle Scholar |

Pansu, J., Giguet-Covex, C., Ficetola, G. F., Gielly, L., Boyer, F., Zinger, L., Arnaud, F., Poulenard, J., Taberlet, P., and Choler, P. (2015). Reconstructing long-term human impacts on plant communities: an ecological approach based on lake sediment DNA. Molecular Ecology 24, 1485–1498.
Reconstructing long-term human impacts on plant communities: an ecological approach based on lake sediment DNA.Crossref | GoogleScholarGoogle Scholar | 25735209PubMed |

Parducci, L., Alsos, I. G., Unneberg, P., Pedersen, M. W., Han, L., Lammers, Y., Salonen, J. S., Väliranta, M. M., Slotte, T., and Wohlfarth, B. (2019). Shotgun environmental DNA, pollen, and macrofossil analysis of late glacial lake sediments from southern Sweden. Frontiers in Ecology and Evolution 7, .
Shotgun environmental DNA, pollen, and macrofossil analysis of late glacial lake sediments from southern Sweden.Crossref | GoogleScholarGoogle Scholar |

Paus, A., Boessenkool, S., Brochmann, C., Epp, L. S., Fabel, D., Haflidason, H., and Linge, H. (2015). Lake Store Finnsjøen: a key for understanding Lateglacial/early Holocene vegetation and ice sheet dynamics in the central Scandes Mountains. Quaternary Science Reviews 121, 36–51.
Lake Store Finnsjøen: a key for understanding Lateglacial/early Holocene vegetation and ice sheet dynamics in the central Scandes Mountains.Crossref | GoogleScholarGoogle Scholar |

Powell, T. M., and Steele, J. H. (1995). ‘Ecological Time Series.’ (Chapman & Hall: New York, NY, USA.)

Reef, R., Atwood, T. B., Samper-Villarreal, J., Adame, M. F., Sampayo, E. M., and Lovelock, C. E. (2017). Using eDNA to determine the source of organic carbon in seagrass meadows. Limnology and Oceanography 62, 1254–1265.
Using eDNA to determine the source of organic carbon in seagrass meadows.Crossref | GoogleScholarGoogle Scholar |

Rogers, K., Saintilan, N., Mazumder, D., and Kelleway, J. J. (2019). Mangrove dynamics and blue carbon sequestration. Biological Letters 15, 20180471.
Mangrove dynamics and blue carbon sequestration.Crossref | GoogleScholarGoogle Scholar |

Shackleton, M. E., Rees, G. N., Watson, G., Campbell, C., and Nielsen, D. (2019). Environmental DNA reveals landscape mosaic of wetland plant communities. Global Ecology and Conservation 19, e00689.
Environmental DNA reveals landscape mosaic of wetland plant communities.Crossref | GoogleScholarGoogle Scholar |

Sønstebø, J., Gielly, L., Brysting, A., Elven, R., Edwards, M., Haile, J., Willerslev, E., Coissac, E., Rioux, D., and Sannier, J. (2010). Using next‐generation sequencing for molecular reconstruction of past Arctic vegetation and climate. Molecular Ecology Resources 10, 1009–1018.
Using next‐generation sequencing for molecular reconstruction of past Arctic vegetation and climate.Crossref | GoogleScholarGoogle Scholar | 21565110PubMed |

Taberlet, P., Coissac, E., Pompanon, F., Gielly, L., Miquel, C., Valentini, A., Vermat, T., Corthier, G., Brochmann, C., and Willerslev, E. (2007). Power and limitations of the chloroplast trnL (UAA) intron for plant DNA barcoding. Nucleic Acids Research 35, e14.
Power and limitations of the chloroplast trnL (UAA) intron for plant DNA barcoding.Crossref | GoogleScholarGoogle Scholar | 17169982PubMed |

Taberlet, P., Coissac, E., Hajibabaei, M., and Rieseberg, L. H. (2012). Environmental DNA. Molecular Ecology 21, 1789–1793.
Environmental DNA.Crossref | GoogleScholarGoogle Scholar | 22486819PubMed |

Thomsen, P. F., and Willerslev, E. (2015). Environmental DNA: an emerging tool in conservation for monitoring past and present biodiversity. Biological Conservation 183, 4–18.
Environmental DNA: an emerging tool in conservation for monitoring past and present biodiversity.Crossref | GoogleScholarGoogle Scholar |

Watson, E. B., Wasson, K., Pasternack, G. B., Woolfolk, A., Van Dyke, E., Gray, A. B., Pakenham, A., and Wheatcroft, R. A. (2011). Applications from paleoecology to environmental management and restoration in a dynamic coastal environment. Restoration Ecology 19, 765–775.
Applications from paleoecology to environmental management and restoration in a dynamic coastal environment.Crossref | GoogleScholarGoogle Scholar |

Waycott, M., Duarte, C. M., Carruthers, T. J., Orth, R. J., Dennison, W. C., Olyarnik, S., Calladine, A., Fourqurean, J. W., Heck, K. L., and Hughes, A. R. (2009). Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences of the United States of America 106, 12377–12381.
Accelerating loss of seagrasses across the globe threatens coastal ecosystems.Crossref | GoogleScholarGoogle Scholar | 19587236PubMed |

Yoccoz, N. G., Brathen, K. A., Gielly, L., Haile, J., Edwards, M. E., Goslar, T., Von Stedingk, H., Brysting, A. K., Coissac, E., Pompanon, F., Sonstebo, J. H., Miquel, C., Valentini, A., De Bello, F., Chave, J., Thuiller, W., Wincker, P., Cruaud, C., Gavory, F., Rasmussen, M., Gilbert, M. T., Orlando, L., Brochmann, C., Willerslev, E., and Taberlet, P. (2012). DNA from soil mirrors plant taxonomic and growth form diversity. Molecular Ecology 21, 3647–3655.
DNA from soil mirrors plant taxonomic and growth form diversity.Crossref | GoogleScholarGoogle Scholar | 22507540PubMed |

Zinger, L., Bonin, A., Alsos, I. G., Balint, M., Bik, H., Boyer, F., Chariton, A. A., Creer, S., Coissac, E., Deagle, B. E., De Barba, M., Dickie, I. A., Dumbrell, A. J., Ficetola, G. F., Fierer, N., Fumagalli, L., Gilbert, M. T. P., Jarman, S., Jumpponen, A., Kauserud, H., Orlando, L., Pansu, J., Pawlowski, J., Tedersoo, L., Thomsen, P. F., Willerslev, E., and Taberlet, P. (2019). DNA metabarcoding: need for robust experimental designs to draw sound ecological conclusions. Molecular Ecology 28, 1857–1862.
DNA metabarcoding: need for robust experimental designs to draw sound ecological conclusions.Crossref | GoogleScholarGoogle Scholar | 31033079PubMed |