Abstract
Despite the roles they play in ecosystem function, animals have have long been neglected in the monitoring of ecological restoration. Vertebrate surveys can be time consuming and costly, often requiring multiple methodologies and taxonomic expertise, making comprehensive monitoring cost prohibitive. Here, we evaluate a new method of assessing mammal and bird diversity through the genetic identification of scat collections. Using DNA metabarcoding of scat collections from three bioregions, we generated bird and mammalian assemblage data and distinguished between sites with different restoration histories. However, scat detectability was affected by environmental conditions (e.g. rainfall and vegetative cover), suggesting that our approach is most applicable at certain times of year or in arid (or semi-arid) environments with rocky soils, where conditions are favourable for scat preservation. Taken together these data provide a pathway to: plan, monitor and establish best-practice when restoring landscapes and add to the growing body of literature on the value of DNA metabarcoding in biomonitoring applications.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Sequencing and sample data and is available at the Dryad Digital Repository: https://doi.org/10.5061/dryad.p2ngf1vnt.
References
Adams CIM, Hoekstra LA, Muell MR, Janzen FJ (2019) A brief review of non-avian reptile environmental DNA (eDNA), with a case study of painted turtle (Chrysemys picta) eDNA under field conditions. Diversity. https://doi.org/10.3390/d11040050
Andersen K, Bird KL, Rasmussen M et al (2012) Meta-barcoding of “dirt” DNA from soil reflects vertebrate biodiversity. Mol Ecol 21:1966–1979. https://doi.org/10.1111/j.1365-294X.2011.05261.x
Arteaga Claramunt AM, White NE, Bunce M et al (2018) Determination of the diet of the ghost bat (Macroderma gigas) in the Pilbara region of Western Australia from dried prey remains and DNA metabarcoding. Aust J Zool 66:195. https://doi.org/10.1071/ZO18040
Australian Museum (2019) Reptiles: A diverse group of animals including turtles, lizards, snakes and crocodiles. In: https://australian.museum/learn/animals/reptiles/. Accessed 14 Aug 2020
Baker SJ, Niemiller ML, Stites AJ et al (2020) Evaluation of environmental DNA to detect Sistrurus catenatus and Ophidiomyces ophiodiicola in crayfish burrows. Conserv Genet Resour 12:13–15. https://doi.org/10.1007/s12686-018-1053-9
Bartholomew GA, Tucker VA (1963) Control of changes in body temperature, metabolism and circulation by the agamid lizard, Amphibolurus barbatus. Physiol Zool 36:199–218
Benayas JMR, Newton AC, Diaz A, Bullock JM (2009) Enhancement of biodiversity and ecosystem services by ecological restoration: a meta-analysis. Science 325:1121–1124. https://doi.org/10.1126/science.1172460
Benigno SM, Dixon KW, Stevens JC (2013) Increasing soil water retention with native-sourced mulch improves seedling establishment in postmine Mediterranean sandy soils. Restor Ecol 21:617–626. https://doi.org/10.1111/j.1526-100X.2012.00926.x
Benjamini Y, Hochberg Y (2007) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300
Berry TE, Osterrieder SK, Murray DC et al (2017) DNA metabarcoding for diet analysis and biodiversity: a case study using the endangered Australian sea lion (Neophoca cinerea). Ecol Evol. https://doi.org/10.1002/ece3.3123
Boyer F, Mercier C, Bonin A et al (2016) obitools: a unix-inspired software package for DNA metabarcoding. Mol Ecol Resour 16:176–182. https://doi.org/10.1111/1755-0998.12428
Brodie JF (2006) An experimentally determined persistence-rate correction factor for scat-based abundance indices. Wildl Soc Bull 34:1216–1219. https://doi.org/10.2193/0091-7648(2006)34[1216:aedpcf]2.0.co;2
Brown WE, Ramsey DSL, Gaffney R (2014) Degradation and detection of fox (Vulpes vulpes) scats in Tasmania: evidence from field trials. Wildl Res 41:681–690. https://doi.org/10.1071/WR14152
Callahan BJ, McMurdie PJ, Rosen MJ et al (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869
Calvignac-spencer A, Merkel K, Kutzner N (2013) Carrion fly-derived DNA as a tool for comprehensive and cost-effective assessment of mammalian biodiversity. Mol Ecol. https://doi.org/10.1111/mec.12183
Catterall CP (2018) Fauna as passengers and drivers in vegetation restoration: a synthesis of processes and evidence. Ecol Manag Restor 19:54–62. https://doi.org/10.1111/emr.12306
Clavero M, Brotons L, Pons P, Sol D (2009) Prominent role of invasive species in avian biodiversity loss. Biol Conserv 142:2043–2049. https://doi.org/10.1016/j.biocon.2009.03.034
Comer SJ, Wooller RD (2002) A comparison of the passerine avifaunas of a rehabilitated minesite and a nearby reserve in south-western Australia. Emu 102:305–311. https://doi.org/10.1071/MU00042
Commonwealth of Australia (2016) Banksia woodlands of the Swan Coastal Plain ecological community. https://www.environment.gov.au/cgi-bin/sprat/public/publiclookupcommunities.pl
Cristescu RH, Frère C, Banks PB (2012) A review of fauna in mine rehabilitation in Australia: Current state and future directions. Biol Conserv 149:60–72. https://doi.org/10.1016/j.biocon.2012.02.003
Cristescu RH, Rhodes J, Frére C, Banks PB (2013) Is restoring flora the same as restoring fauna? Lessons learned from koalas and mining rehabilitation. J Appl Ecol 50:423–431. https://doi.org/10.1111/1365-2664.12046
Cross SL, Bateman PW, Cross AT (2020a) Restoration goals: Why are fauna still overlooked in the process of recovering functioning ecosystems and what can be done about it? Ecol Manag Restor 21:4–8. https://doi.org/10.1111/emr.12393
Cross SL, Craig MD, Tomlinson S et al (2020) Using monitors to monitor ecological restoration: presence may not indicate persistence. Austral Ecol. https://doi.org/10.1111/aec.12905
Cross SL, Tomlinson S, Craig MD et al (2019) Overlooked and undervalued: the neglected role of fauna and a global bias in ecological restoration assessments. Pac Conserv Biol 25:331–341. https://doi.org/10.1071/PC18079
Cross SL, Tomlinson S, Craig MD, Bateman PW (2019) The Time Local Convex Hull method as a tool for assessing responses of fauna to habitat restoration: a case study using the perentie (Varanus giganteus: Reptilia: Varanidae). Aust J Zool 67:27–37. https://doi.org/10.1071/ZO19040
De Caceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90:3566–3574
De Cuyper A, Meloro C, Abraham AJ et al (2020) The uneven weight distribution between predators and prey: comparing gut fill between terrestrial herbivores and carnivores. Comp Biochem Physiol Part A Mol Integr Physiol 243:110683. https://doi.org/10.1016/j.cbpa.2020.110683
Doherty TS, Glen AS, Nimmo DG et al (2016) Invasive predators and global biodiversity loss. Proc Natl Acad Sci USA 113:11261–11265. https://doi.org/10.1073/pnas.1602480113
Drummond AJ, Newcomb RD, Buckley TR et al (2015) Evaluating a multigene environmental DNA approach for biodiversity assessment. Gigascience. https://doi.org/10.1186/s13742-015-0086-1
Edgar RC (2016) UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. bioRxiv. https://doi.org/10.1101/081257
Else PL, Hulbert AJ (1981) Comparison of the “mammal machine” and the “reptile machine”: energy production. Am J Physiol Regul Integr Comp Physiol 9:3–9. https://doi.org/10.1152/ajpregu.1981.240.1.r3
Environmental Protection Authority and Department of Environment and Conservation (2010) Technical guide − terrestrial vertebrate fauna surveys for environmental impact assessment. Hyder BM, Dell J, Cowan MA (eds), Perth, Western Australia
Fernandes K, van der Heyde M, Bunce M et al (2018) DNA metabarcoding—a new approach to fauna monitoring in mine site restoration. Restor Ecol 26:1098–1107. https://doi.org/10.1111/rec.12868
Fiske I, Chandler R (2011) Unmarked: an R package for fitting hierarchical models of wildlife occurrence and abundance. J Stat Softw 43(10):1–23
Fleming TH, Muchhala N (2008) Nectar-feeding bird and bat niches in two worlds: pantropical comparisons of vertebrate pollination systems. J Biogeogr 35:764–780. https://doi.org/10.1111/j.1365-2699.2007.01833.x
Frøslev TG, Kjøller R, Bruun HH et al (2017) Algorithm for post-clustering curation of DNA amplicon data yields reliable biodiversity estimates. Nat Commun. https://doi.org/10.1038/s41467-017-01312-x
Galimberti A, Spinelli S, Bruno A et al (2016) Evaluating the efficacy of restoration plantings through DNA barcoding of frugivorous bird diets. Conserv Biol. https://doi.org/10.1111/cobi.12687
Goldberg CS, Pilliod DS, Arkle RS, Waits LP (2011) Molecular detection of vertebrates in stream water: a demonstration using Rocky Mountain tailed frogs and Idaho giant salamanders. PLoS One. https://doi.org/10.1371/journal.pone.0022746
Gole CA (2006) Bird surveys in selected Perth metropolitan reserves: round 3 survey report bird surveys in selected Perth metropolitan reserves. Birds Australia WA, Perth, Australia
Harrington LA, Harrington AL, Hughes J et al (2010) The accuracy of scat identification in distribution surveys: American mink, Neovison vison, in the northern highlands of Scotland. Eur J Wildl Res 56:377–384. https://doi.org/10.1007/s10344-009-0328-6
Havel JJ (1975) Site-vegetation mapping in the northern Jarrah forest. I. Definition of site‐vegetation types. For Dep WA Bull 86:1–115
Herrera CM (1995) Plant-vertebrate seed dispersal systems in the Mediterranean: ecological, evolutionary, and historical determinants. Annu Rev Ecol Syst 26:705–727. https://doi.org/10.1146/annurev.es.26.110195.003421
Jerde CL, Mahon AR, Chadderton WL, Lodge DM (2011) “Sight-unseen” detection of rare aquatic species using environmental DNA. Conserv Lett 4:150–157. https://doi.org/10.1111/j.1755-263X.2010.00158.x
Kolowski JM, Forrester TD (2017) Camera trap placement and the potential for bias due to trails and other features. PLoS One 12:1–20. https://doi.org/10.1371/journal.pone.0186679
Kucherenko A, Herman JE III, Urakawa EME H (2018) Terrestrial snake environmental DNA accumulation and degradation dynamics and its environmental application. Herpetologica 74:38–49
La VT, Nudds TD (2016) Estimation of avian species richness: biases in morning surveys and efficient sampling from acoustic recordings. Ecosphere 7:1–13. https://doi.org/10.1002/ecs2.1294
Lonsinger RC, Gese EM, Knight RN et al (2016) Quantifying and correcting for scat removal in noninvasive carnivore scat surveys. Wildl Biol 22:45–54. https://doi.org/10.2981/wlb.00179
Mazurek MJ, Zielinski WJ (2004) Individual legacy trees influence vertebrate wildlife diversity in commercial forests. For Ecol Manage 193:321–334. https://doi.org/10.1016/j.foreco.2004.01.013
Mcdonald T, Gann GD, Jonson J, Dixon KW (2016) International standards for the practice of ecological restoration—including principles and key concepts. Commun Stand. https://doi.org/10.1016/b978-0-08-034092-0.50030-2
McInnes JC, Alderman R, Deagle BE et al (2017) Optimised scat collection protocols for dietary DNA metabarcoding in vertebrates. Methods Ecol Evol 8:192–202. https://doi.org/10.1111/2041-210X.12677
McKenzie NL, van Leeuwen S, Pinder AM (2009) Introduction to the Pilbara biodiversity survey, 2002–2007. Records of the Western Australian Museum, Supplement 78(1):3. https://doi.org/10.18195/issn.0313-122x.78(1).2009.003-089
McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. https://doi.org/10.1371/journal.pone.0061217
Mendiburu F de (2019) agricolae: Statistical Procedures for Agricultural Research. R package version 1.3-1. https://CRANR-project.org/package=agricolae. Accessed 30 Oct 2019
Miller BP, Sinclair EA, Menz MHM et al (2017) A framework for the practical science necessary to restore sustainable, resilient, and biodiverse ecosystems. Restor Ecol 25:605–617. https://doi.org/10.1111/rec.12475
Monterroso P, Castro D, Silva TL et al (2013) Factors affecting the (in)accuracy of mammalian mesocarnivore scat identification in South-Western Europe. J Zool 289:243–250. https://doi.org/10.1111/jzo.12000
Munn AJ, Tomlinson S, Savage T, Clauss M (2012) Retention of different-sized particles and derived gut fill estimate in tammar wallabies (Macropus eugenii): physiological and methodological considerations. Comp Biochem Physiol Mol Integr Physiol 161:243–249. https://doi.org/10.1016/j.cbpa.2011.11.003
Murray DC, Coghlan ML, Bunce M (2015) From benchtop to desktop: important considerations when designing amplicon sequencing workflows. PLoS One 10:e0124671. https://doi.org/10.1371/journal.pone.0124671
Myers N, Mittermeier RA, Mittermeier CG et al (2007) Biodiversity hotspots for conservation priorities. Biodivers Conserv 16:853–858. https://doi.org/10.1080/21564574.1998.9650003
Nichols OG, Nichols FM (2003) Long-term trends in faunal recolonization after bauxite mining in the Jarrah forest of Southwestern Australia. Restor Ecol 11:261–272. https://doi.org/10.1046/j.1526-100X.2003.00190.x
Palmer MA, Ambrose RF, Poff NL (1997) Ecological Theory and Community Restoration Ecology. Restor Ecol 5:291–300. https://doi.org/10.1046/j.1526-100X.1997.00543.x
Pinder AM, Halse SA, Shiel RJ, McRae JM (2010) An arid zone awash with diversity: patterns in the distribution of aquatic invertebrates in the Pilbara region of Western Australia. Rec West Aust Mus Suppl 78:205. https://doi.org/10.18195/issn.0313-122x.78(1).2010.205-246
Poggenburg C, Nopp-Mayr U, Coppes J, Sachser F (2018) Shit happens and persists: decay dynamics of capercaillie (Tetrao urogallus L.) droppings under natural and artificial conditions. Eur J Wildl Res. https://doi.org/10.1007/s10344-018-1187-9
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rhodes JR, Lunney D, Moon C et al (2011) The consequences of using indirect signs that decay to determine species’ occupancy. Ecography 34:141–150. https://doi.org/10.1111/j.1600-0587.2010.05908.x
Riaz T, Shehzad W, Viari A et al (2011) EcoPrimers: inference of new DNA barcode markers from whole genome sequence analysis. Nucleic Acids Res 39:1–11. https://doi.org/10.1093/nar/gkr732
Sarkar S, Pressey RL, Faith DP et al (2006) Biodiversity conservation planning tools: present status and challenges for the future. Annu Rev Environ Resour 31:123–159. https://doi.org/10.1146/annurev.energy.31.042606.085844
Schnell IB, Sollmann R, Calvignac-Spencer S et al (2015) iDNA from terrestrial haematophagous leeches as a wildlife surveying and monitoring tool - prospects, pitfalls and avenues to be developed. Front Zool 12:1–14. https://doi.org/10.1186/s12983-015-0115-z
Suding K, Higgs E, Palmer M et al (2015) Committing to ecological restoration. Science 348:638–640. https://doi.org/10.1126/science.aaa4216
Taberlet P, Coissac E, Hajibabaei M, Rieseberg LHLH (2012) Environmental DNA. Mol Ecol 21:1789–1793. https://doi.org/10.1111/j.1365-294X.2012.05542.x
Telfer WR, Griffiths AD, Bowman DMJS (2006) Scats can reveal the presence and habitat use of cryptic rock-dwelling macropods. Aust J Zool 54:325–334. https://doi.org/10.1071/ZO05074
Thompson SA, Thompson GG (2004) Adequacy of rehabilitation monitoring practices in the Western Australian mining industry. Ecol Manag Restor 5:30–33. https://doi.org/10.1111/j.1442-8903.2004.00172.x
Trudgen M (1977) A report on the flora and floristic communitytypes found on parts of sand mining leases held by Rocla in the Gnangara area. Report prepared for Rocla Quarry Prod-ucts, Perth
UN Environment Programme (2020) Decade on ecosystem restoration 2021–2030. In: https://www.decadeonrestoration.org/. Accessed 5 Feb 2020
van der Heyde M, Bunce M, Wardell-Johnson G et al (2020) Testing multiple substrates for terrestrial biodiversity monitoring using environmental DNA metabarcoding. Mol Ecol Resour. https://doi.org/10.1111/1755-0998.13148
Wadley JJ, Austin JJ, Fordham DA (2013) Rapid species identification of eight sympatric northern Australian macropods from faecal-pellet DNA. Wildl Res 40:241. https://doi.org/10.1071/WR13005
West KM, Stat M, Harvey ES et al (2020) eDNA metabarcoding survey reveals fine-scale coral reef community variation across a remote, tropical island ecosystem. Mol Ecol 29:1069–1086. https://doi.org/10.1111/mec.15382
Whitaker D, Christman M (2014) clustsig: Significant Cluster Analysis. R package version 1.1. https://CRANR-project.org/package=clustsig. Accessed 9 Apr 2020
Williams K, Mitchell D (2002) Jarrah Forest 1 (JF1 - Northern Jarrah Forest subregion). Biodivers Audit West Aust Biogeogr Subreg 1:369–381
Wilson GJ, Delahay RJ (2001) A review of methods to estimate the abundance of terrestrial carnivores using field signs and observation. Wildl Res 28:151–164
Yu DW, Ji Y, Emerson BC et al (2012) Biodiversity soup: Metabarcoding of arthropods for rapid biodiversity assessment and biomonitoring. Methods Ecol Evol 3:613–623. https://doi.org/10.1111/j.2041-210X.2012.00198.x
Zann RA, Morton SR, Jones KR, Burley NT (1995) The timing of breeding by zebra finches in relation to rainfall in central Australia. Emu 95:208–222. https://doi.org/10.1071/MU9950208
Acknowledgements
This work was supported by resources provided by the Pawsey Supercomputing Centre with funding from the Australian Government and the Government of Western Australia. This work was supported by the Australian Research Council Industrial Transformation Training Centre for Mine Site Restoration (ICI150100041). We thank the mining companies BHP, Hanson Construction Materials, and South32 for facilitating access to sites for sampling. We would also like to thank Sheree Walters for help with sample collection and the members of the Trace and Environmental DNA (TrEnD) Laboratory for support with metabarcoding workflows and bioinformatics. We acknowledge the traditional owners of the land on which this research was undertaken and pay our respects to Elders past, present and emerging.
Author information
Authors and Affiliations
Contributions
MvH conducted the study and wrote the manuscript. MvH, PN, MB, NW, and GW-J were involved in the experimental design. Samples were collected and processed by MvH; molecular and bioinformatics work was performed by MvH; all data was analyzed and processed by MvH; statistical analysis was done by MvH; the manuscript was edited by all authors.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Rajeev Raghavan.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
van der Heyde, M., Bateman, P.W., Bunce, M. et al. Scat DNA provides important data for effective monitoring of mammal and bird biodiversity. Biodivers Conserv 30, 3585–3602 (2021). https://doi.org/10.1007/s10531-021-02264-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-021-02264-x