Abstract
Populations of most freshwater mussels (Unionidae) are declining worldwide; these includes Sinanodonta spp., which inhabit artificial ponds in Japan. The detection of environmental DNA (eDNA) would be a rapid and efficient method for monitoring the distribution of Sinanodonta populations. Accordingly, the aim of the present study was to compare the results of real-time PCR-based eDNA detection to those of hand collection in 24 ponds in Japan. Sinanodonta eDNA was detected in most of the study ponds where Sinanodonta spp. were found by hand collection, and there was a positive correlation between the eDNA detection rate and the number of Sinanodonta specimens collected by hand. These findings demonstrate that eDNA detection is a valuable alternative method of evaluating the distribution of Sinanodonta spp., and that this method has a similar detection sensitivity to that of hand collection. The eDNA method can be used to monitor freshwater mussels at broad scales and prohibitive depths where hand collection is difficult.
Change history
13 March 2020
In the original publication of the article the sentence under the heading “Primer and probe design” was published incorrectly. The correct sentence is given in this correction.
13 March 2020
In the original publication of the article the sentence under the heading ���Primer and probe design��� was published incorrectly. The correct sentence is given in this correction.
References
Aldridge DC, Fayle TM, Jackson N (2007) Freshwater mussel abundance predicts biodiversity in UK lowland rivers. Aquat Conserv 17:554–564
Ardura A, Zaiko A, Martinez J, Samulioviene A, Semenova A, Garcia-Vazquez E (2015a) eDNA and specific primers for early detection of invasive species—a case study on the bivalve Rangia cuneata, currently spreading in Europe. Mar Environ Res 112:48–55
Ardura A, Zaiko A, Martinez JL, Samulioviene A, Semenova A, Garcia-Vazquez E (2015b) Environmental DNA evidence of transfer of North Sea mollusks across tropical waters through ballast water. J Molluscan Stud 81:1–7
Bohmann K, Evans A, Gilbert MTP et al (2014) Environmental DNA for wildlife biology and biodiversity monitoring. Trends Ecol Evol 29:358–367
Clusa L, Miralles L, Basanta A, Escot C, Garcia-Vazquez E (2017) eDNA for detection of five highly invasive molluscs. A case study in urban rivers from the Iberian Peninsula. PLoS One 12:e0188126
Cowart DA et al (2018) Development and field validation of an environmental DNA (eDNA) assay for invasive clams of the genus Corbicula. Manag Biol Invasions 9:27–37
Dejean T, Valentini A, Miquel C, Taberlet P, Bellemain E, Miaud C (2012) Improved detection of an alien invasive species through environmental DNA barcoding: the example of the American bullfrog Lithobates catesbeianus. J Appl Ecol 49:953–959
Doi H, Uchii K, Takahara T, Matsuhashi S, Yamanaka H, Minamoto T (2015) Use of droplet digital PCR for estimation of fish abundance and biomass in environmental DNA surveys. PLoS One 10:e0122763
Doi H, Katano I, Sakata Y, Souma R, Kosuge T, Nagano M, Ikeda K, Yano K, Tojo K (2017a) Detection of an endangered aquatic heteropteran using environmental DNA in a wetland ecosystem. R Soc Open Sci 4:170568
Doi H, Inui R, Akamatsu Y, Kanno K, Yamanaka H, Takahara T et al (2017b) Environmental DNA analysis for estimating the abundance and biomass of stream fish. Freshw Biol 62:30–39
Dysthe JC, Rodgers T, Franklin TW, Carim KJ, Young MK, McKelvey KS, Mock KE, Schwartz MK (2018) Repurposing environmental DNA samples—detecting the western pearlshell (Margaritifera falcata) as a proof of concept. Ecol Evol 8:2659–2670
Edgar C (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Fujii K, Doi H, Matsuoka S, Nagano M, Sato H, Yamanaka H (2019) Environmental DNA metabarcoding for fish community analysis in backwater lakes: a comparison of capture methods. PLoS One 14:e0210357
Geist J (2015) Seven steps towards improving freshwater conservation. Aquat Conserv Mar Freshw Ecosyst 25:447–453
Goldberg CS et al (2016) Critical considerations for the application of environmental DNA methods to detect aquatic species. Methods Ecol Evol 7:1299–1307
Hartman LJ, Coyne SR, Norwood DA (2005) Development of a novel internal positive control for Taqman® based assays. Mol Cell Probes 19(1):51–59
Ikeda K, Doi H, Tanaka K, Kawai T, Negishi JN (2016) Using environmental DNA to detect an endangered crayfish Cambaroides japonicus in streams. Conserv Genet Resour 8:231–234
Katano I, Harada K, Doi H, Souma R, Minamoto T (2017) Environmental DNA method for estimating salamander distribution in headwater streams, and a comparison of water sampling methods. PLoS One 12:e0176541
Kitamura J (2005) Factors affecting seasonal mortality of rosy bitterling (Rhodeus ocellatus kurumeus) embryos on the gill soft heir host mussel. Popul Ecol 47:41–51
Kitamura J (2007) Reproductive ecology and host utilization of four sympatric bitterling (Acheilognathinae, Cyprinidae) in a lowland reach of the Harai River in Mie, Japan. Environ Biol Fishes 78:37–55
Kondo T (2008) Monograph of Unionoida in Japan (Mollusca: Bivalvia). Spec Publ Malacol Soc Jpn 3:1–69
Kuwahara A, Matsuba H, Inoue M, Hata H (2017) Population decline in unionid mussels in the Matsuyama Plain, Ehime Prefecture. Jpn J Conserv Ecol 22:91–103
Lacoursière-Roussel A, Rosabal M, Bernatchez L (2016) Estimating fish abundance and biomass from eDNA concentrations: variability among capture methods and environmental conditions. Mol Ecol Resour 16:1401–1414
Minamoto T, Yamanaka H, Takahara T, Honjo MN, Kawabata Z (2012) Surveillance of fish species composition using environmental DNA. Limnology 13:193–197
Miya M, Sato Y, Fukunaga T, Sado T, Poulsen JY, Sato K et al (2015) MiFish, a set of universal PCR primers for metabarcoding environmental DNA from fishes: detection of > 230 subtropical marine species. R Soc Open Sci 2:150088
Negishi JN, Nagayama S, Kume M, Sagawa S, Kayaba Y, Yamanaka Y (2013) Unionoid mussels as an indicator of fish communities: a conceptual framework and empirical evidence. Ecol Indic 24:127–137
Pilliod DS, Goldberg CS, Arkle RS, Waits LP, Richardson J (2013) Estimating occupancy and abundance of stream amphibians using environmental DNA from filtered water samples. Can J Fish Aquat Sci 70:1123–1130
R Core Team (2018) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available from https://www.Rproject.org/
Sano I, Shirai A, Kondo T, Miyazaki J (2017) Phylogenetic relationships of Japanese Unionoida (Mollusca: Bivalvia) based on mitochondrial 16S rDNA sequences. J Water Resour Protect 9:493–509
Sansom BJ, Sassoubre LM (2017) Environmental DNA (eDNA) shedding and decay rates to model freshwater mussel eDNA transport in a river. Environ Sci Technol 51:14244–14253
Smith R, Villella R, Lemarie D (2003) Application of adaptive cluster sampling to low-density populations of freshwater mussels. Environ Ecol Stat 10:7–15
Smith C, Reichard M, Jurajda P, Przybylski M (2004) The reproductive ecology of the European bitterling (Rhodeus sericeus). J Zool 262:107–124
Takahara T, Minamoto T, Yamanaka H, Doi H, Kawabata Z (2012) Estimation of fish biomass using environmental DNA. PLoS One 7:e35868
Takahara T, Minamoto T, Doi H (2013) Using environmental DNA to estimate the distribution of an invasive fish species in ponds. PLoS One 8:e56584
Takahara T, Ikebuch T, Doi H, Minamoto T (2019) Using environmental DNA to estimate the seasonal distribution and habitat preferences of a Japanese basket clam in Lake Shinji, Japan. Estuar Coast Shelf Sci 221:15–20
Thomsen PF, Willerslev E (2015) Environmental DNA—an emerging tool in conservation for monitoring past and present biodiversity. Biol Conserv 183:4–18
Uchii K, Doi H, Minamoto T (2015) A novel environmental DNA approach to quantify the cryptic invasion of non-native genotypes. Mol Ecol Res 16(2):415–422
Vaughn C, Hakenkamp C (2001) The functional role of burrowing bivalves in freshwater ecosystems. Freshw Biol 46:1431–1446
Vaughn C, Spooner E (2006) Unionid mussels influence macroinvertebrate assemblage structure in streams. J N Am Benthol Soc 25:691–700
Yamamoto S, Masuda R, Sato Y, Sado T, Araki H, Kondoh M, Minamoto T, Miya M (2017) Environmental DNA metabarcoding reveals local fish communities in a species-rich coastal sea. Sci Rep 7:40368
Acknowledgements
We thank Rio Souma and Aozora Kakuda, University of Hyogo, for their help with laboratory experiments, and Hiroki Yamanaka, Ryukoku University, for advice about the PCR inhibitation test. This study was supported by the Environment Research and Technology Development Fund (4-1602) of the Environmental Restoration and Conservation Agency, Japan, and by JSPS KAKENHI grant numbers 15K00596 and 18K11678 to IK.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling Editor: Eric Larson.
Rights and permissions
About this article
Cite this article
Togaki, D., Doi, H. & Katano, I. Detection of freshwater mussels (Sinanodonta spp.) in artificial ponds through environmental DNA: a comparison with traditional hand collection methods. Limnology 21, 59–65 (2020). https://doi.org/10.1007/s10201-019-00584-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10201-019-00584-0