Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (2024)

Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (1) https://doi.org/10.1007/s10201-023-00740-7

Journal: Limnology, 2024

Publisher: Springer Science and Business Media LLC

Authors:

  1. Shunsuke Hidaka
  2. Toshiaki S. Jo
  3. Satoshi Yamamoto
  4. Koki R. Katsuhara
  5. Sei Tomita
  6. Masaki Miya
  7. Makihiko Ikegami
  8. Atushi Ushimaru
  9. Toshifumi Minamoto

Abstract

AbstractJapanese giant salamander (Andrias japonicus) is one of the largest amphibian species in the world and an iconic species in Japan. However, as its distribution has recently declined across the country, rapid and extensive monitoring of the distribution is urgently needed for its efficient conservation. Here, we used environmental DNA (eDNA) analysis to assess the Japanese giant salamander’s distribution in western Japan and, for that purpose, we collected 410 water samples from 12 rivers. We then developed a new eDNA assay for multi-copy nuclear DNA (nuDNA) of the giant salamander and compared the eDNA detectability of the nuDNA marker with that of a previous mitochondrial DNA (mtDNA) marker. Throughout the survey, we detected target eDNA from 162 water samples using either of the markers, which generally corresponded to the known natural distribution of the species. Additionally, the use of the nuDNA marker allowed for higher detection rate of target eDNA than the mtDNA marker. Moreover, the detection rate of target eDNA decreased substantially in water samples with higher conductivity and also partly in those with higher pH, suggesting their negative impacts on the salamander’s ecology. Our results demonstrated that eDNA analysis with multi-copy nuDNA marker is highly useful for efficient and sensitive surveillance of Japanese giant salamander’s distribution. Our study provided the methodology for efficiently monitoring the Japanese giant salamander’s distribution via eDNA analysis and facilitating conservation activities for them.

Funders

  1. Japan Society for the Promotion of Science
  2. 2014 Academic Research Grant from Hyogo Science and Technology Association
  3. Kobe University

List of references

  1. Alavi SMH, Cosson J (2006) Sperm motility in fishes. (II) Effects of ions and osmolality: a review. Cell Biol Int 30:1–14
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (2) https://doi.org/10.1016/j.cellbi.2005.06.004
  2. Andres KJ, Sethi SA, Lodge DM, Andrés J (2021) Nuclear eDNA estimates population allele frequencies and abundance in experimental mesocosms and field samples. Mol Ecol 30:685–697
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (3) https://doi.org/10.1111/mec.15765
  3. Bálint M, Nowak C, Márton O, Pauls SU, Wittwer C, Aramayo JL, Schulze A, Chambert T, Cocchiararo B, Jansen M (2018) Accuracy, limitations and cost efficiency of eDNA-based community survey in tropical frogs. Mol Ecol Resour 18:1415–1426
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (4) https://doi.org/10.1111/1755-0998.12934
  4. Bhateria R, Jain D (2016) Water quality assessment of lake water: a review. Sustain Water Resour Manage 2:161–173
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (5) https://doi.org/10.1007/s40899-015-0014-7
  5. Biggs J, Ewald N, Valentini A, Gaboriaud C, Dejean T, Griffiths RA, Foster J, Wilkinson JW, Arnell A, Brotherton P, Williams P, Dunn F (2015) Using eDNA to develop a national citizen science-based monitoring programme for the great crested newt (Triturus cristatus). Biol Conserv 183:19–28
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (6) https://doi.org/10.1016/j.biocon.2014.11.029
  6. Biodiversity Center of Japan, Ministry of the Environment (2001) 5th National basic survey on natural environment. https://www.biodic.go.jp/reports2/5th/ap_rep/5_ap_rep.pdf. Accessed 6 December 2022
  7. Boczkaj G, Fernandes A (2017) Wastewater treatment by means of advanced oxidation processes at basic pH conditions: a review. J Chem Eng 320:608–633
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (7) https://doi.org/10.1016/j.cej.2017.03.084
  8. Bodinof Jachowski CM, Millspaugh JJ, Hopkins WA (2016) Current land use is a poor predictor of hellbender occurrence: why assumptions matter when predicting distributions of data-deficient species. Divers Distrib 22:865–880
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (8) https://doi.org/10.1111/ddi.12446
  9. Bowles BD, Sanders MS, Hansen RS (2006) Ecology of the Jollyville Plateau salamander (Eurycea tonkawae: Plethodontidae) with an assessment of the potential effects of urbanization. Hydrobiologia 553:111–120
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (9) https://doi.org/10.1007/s10750-005-5440-0
  10. Browne RK, Li H, Wang Z, Okada S, Hime P, McMillan A, Wu M, Diaz R, McGinnity D, Briggler JT (2014) The giant salamanders (Cryptobranchidae): part B. Biogeography, ecology and reproduction. Amphib Reptile Conserv 5:30–50
  11. Butchart SH, Walpole M, Collen B, Van Strien A, Scharlemann JP, Almond RE, Baillie JE, Bomhard B, Brown C, Bruno J, Carpenter KE, Carr GM, Chanson J, Chenery AM, Csirke J, Davidson NC, Dentener F, Foster M, Galli A, Galloway JN, Genovesi P, Gregory RD, Hockings M, Kapos V, Lamarque J, Leverington F, Loh J, McGeoch MA, McRae L, Minasyan A, Morcillo MH, Oldfield TE, Pauly D, Quader S, Revenga C, Sauer JR, Skolnik B, Spear D, Stanwell-Smith D, Stuart SN, Symes A, Tierney M, Tyrrell TD, Vié J, Watson R (2010) Global biodiversity: indicators of recent declines. Science 328:1164–1168
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (10) https://doi.org/10.1126/science.1187512
  12. Bylemans J, Furlan EM, Hardy CM, McGuffie P, Lintermans M, Gleeson DM (2017) An environmental DNA-based method for monitoring spawning activity: a case study, using the endangered Macquarie perch (Macquaria australasica). Methods Ecol Evol 8:646–655
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (11) https://doi.org/10.1111/2041-210X.12709
  13. Bylemans J, Furlan EM, Gleeson DM, Hardy CM, Duncan RP (2018) Does size matter? An experimental evaluation of the relative abundance and decay rates of aquatic environmental DNA. Environ Sci Technol 52:6408–6416
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (12) https://doi.org/10.1021/acs.est.8b01071
  14. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naeem S (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (13) https://doi.org/10.1038/nature11148
  15. Ceballos G, Ehrlich PR, Barnosky AD, García A, Pringle RM, Palmer TM (2015) Accelerated modern human–induced species losses: entering the sixth mass extinction. Sci Adv 1:e1400253
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (14) https://doi.org/10.1126/sciadv.1400253
  16. Clare EL, Economou CK, Bennett FJ, Dyer CE, Adams K, McRobie B, Drinkwater R, Littlefair JE (2022) Measuring biodiversity from DNA in the air. Curr Biol 32:693–700
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (15) https://doi.org/10.1016/j.cub.2021.11.064
  17. Czeglédi I, Sály P, Specziár A, Preiszner B, Szalóky Z, Maroda Á, Pont D, Meulenbroek P, Valentini A, Erős T (2021) Congruency between two traditional and eDNA-based sampling methods in characterising taxonomic and trait-based structure of fish communities and community–environment relationships in lentic environment. Ecol Indic 129:107952
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (16) https://doi.org/10.1016/j.ecolind.2021.107952
  18. Darling JA, Mahon AR (2011) From molecules to management: adopting DNA-based methods for monitoring biological invasions in aquatic environments. Environ Res 111:978–988
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (17) https://doi.org/10.1016/j.envres.2011.02.001
  19. Deiner K, Bik HM, Mächler E, Seymour M, Lacoursière-Roussel A, Altermatt F, Creer S, Bista I, Lodge DM, de Vere N, Pfrender ME, Bernatchez L (2017) Environmental DNA metabarcoding: transforming how we survey animal and plant communities. Mol Ecol 26:5872–5895
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (18) https://doi.org/10.1111/mec.14350
  20. Dysthe JC, Franklin TW, McKelvey KS, Young MK, Schwartz MK (2018) An improved environmental DNA assay for bull trout (Salvelinus confluentus) based on the ribosomal internal transcribed spacer I. PLoS ONE 13:e0206851
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (19) https://doi.org/10.1371/journal.pone.0206851
  21. Fediajevaite J, Priestley V, Arnold R, Savolainen V (2021) Meta-analysis shows that environmental DNA outperforms traditional surveys, but warrants better reporting standards. Ecol Evol 11:4803–4815
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (20) https://doi.org/10.1002/ece3.7382
  22. Ficetola GF, Miaud C, Pompanon F, Taberlet P (2008) Species detection using environmental DNA from water samples. Biol Lett 4:423–425
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (21) https://doi.org/10.1098/rsbl.2008.0118
  23. f*ckumoto S, Ushimaru A, Minamoto T (2015) A basin-scale application of environmental DNA assessment for rare endemic species and closely related exotic species in rivers: a case study of giant salamanders in Japan. J Appl Ecol 52:358–365
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (22) https://doi.org/10.1111/1365-2664.12392
  24. Goodwin S, McPherson JD, McCombie WR (2016) Coming of age: ten years of next-generation sequencing technologies. Nat Rev Genet 17:333–351
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (23) https://doi.org/10.1038/nrg.2016.49
  25. Handelsman J (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68:669–685
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (24) https://doi.org/10.1128/MMBR.68.4.669-685.2004
  26. Hänfling B, Lawson Handley L, Read DS, Hahn C, Li J, Nichols P, Blackman RC, Oliver A, Winfield IJ (2016) Environmental DNA metabarcoding of lake fish communities reflects long-term data from established survey methods. Mol Ecol 25:3101–3119
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (25) https://doi.org/10.1111/mec.13660
  27. Harper LR, Griffiths NP, Lawson Handley L, Sayer CD, Read DS, Harper KJ, Blackman RC, Li J, Hänfling B (2019) Development and application of environmental DNA surveillance for the threatened crucian carp (Carassius carassius). Freshw Biol 64:93–107
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (26) https://doi.org/10.1111/fwb.13197
  28. Hashemzadeh Segherloo I, Tabatabaei SN, Abdolahi-Mousavi E, Hernandez C, Normandeau E, Laporte M, Boyle B, Amiri M, GhaedRahmati N, Hallerman E, Bernatchez L (2022) eDNA metabarcoding as a means to assess distribution of subterranean fish communities: Iranian blind cave fishes as a case study. Environ DNA 4:402–416
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (27) https://doi.org/10.1002/edn3.264
  29. Houlahan JE, Findlay CS, Schmidt BR, Meyer AH, Kuzmin SL (2000) Quantitative evidence for global amphibian population declines. Nature 404:752–755
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (28) https://doi.org/10.1038/35008052
  30. Iwai N, Yasumiba K, Takahara T (2019) Efficacy of environmental DNA to detect and quantify stream tadpoles of Odorrana splendida. Royal Soc Open Sci 6:181798
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (29) https://doi.org/10.1098/rsos.181798
  31. Jerde CL, Mahon AR, Chadderton WL, Lodge DM (2011) “Sight-unseen” detection of rare aquatic species using environmental DNA. Conserv Lett 4:150–157
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (30) https://doi.org/10.1111/j.1755-263X.2010.00158.x
  32. Jo T, Yamanaka H (2022) Meta-analyses of environmental DNA downstream transport and deposition in relation to hydrogeography in riverine environments. Freshw Biol 67:1333–1343
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (31) https://doi.org/10.1111/fwb.13920
  33. Jo T, Murakami H, Masuda R, Sakata MK, Yamamoto S, Minamoto T (2017) Rapid degradation of longer DNA fragments enables the improved estimation of distribution and biomass using environmental DNA. Mol Ecol Resour 17:e25–e33
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (32) https://doi.org/10.1111/1755-0998.12685
  34. Jo T, Arimoto M, Murakami H, Masuda R, Minamoto T (2020a) Estimating shedding and decay rates of environmental nuclear DNA with relation to water temperature and biomass. Environ DNA 2:140–151
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (33) https://doi.org/10.1002/edn3.51
  35. Jo T, f*ckuoka A, Uchida K, Ushimaru A, Minamoto T (2020b) Multiplex real-time PCR enables the simultaneous detection of environmental DNA from freshwater fishes: a case study of three exotic and three threatened native fishes in Japan. Biol Invasions 22:455–471
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (34) https://doi.org/10.1007/s10530-019-02102-w
  36. Jo T, Tomita S, Kohmatsu Y, Osathanunkul M, Ushimaru A, Minamoto T (2020c) Seasonal monitoring of Hida salamander Hynobius kimurae using environmental DNA with a genus-specific primer set. Endanger Species Res 43:341–352
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (35) https://doi.org/10.3354/esr01073
  37. Jo TS, Tsuri K, Yamanaka H (2022) Can nuclear aquatic environmental DNA be a genetic marker for the accurate estimation of species abundance? Sci Nat 109:38
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (36) https://doi.org/10.1007/s00114-022-01808-7
  38. Johnson PT, McKenzie VJ, Peterson AC, Kerby JL, Brown J, Blaustein AR, Jackson T (2011) Regional decline of an iconic amphibian associated with elevation, land-use change, and invasive species. Conserv Biol 25:556–566
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (37) https://doi.org/10.1111/j.1523-1739.2010.01645.x
  39. Kawamichi T, Ueda H (1998) Spawning at nests of extra-large males in the giant salamander Andrias japonicus. J Herpetol 32:133–136
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (38) https://doi.org/10.2307/1565495
  40. Keitzer SC, Pauley TK, Burcher CL (2013) Stream characteristics associated with site occupancy by the eastern hellbender, Cryptobranchus alleganiensis alleganiensis, in southern West Virginia. Northeast Nat 20:666–677
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (39) https://doi.org/10.1656/045.020.0418
  41. Klymus KE, Merkes CM, Allison MJ, Goldberg CS, Helbing CC, Hunter ME, Jackson CA, Lance RF, Mangan AM, Monroe EM, Piaggio AJ, Stokdyk JP, Wilson CC, Richter CA (2020) Reporting the limits of detection and quantification for environmental DNA assays. Environ DNA 2:271–282
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (40) https://doi.org/10.1002/edn3.29
  42. Kuznetsova A, Brockhoff PB, Christensen RH (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (41) https://doi.org/10.18637/jss.v082.i13
  43. Li W, Hou X, Xu C, Qin M, Wang S, Wei L, Wang Y, Liu X, Li Y (2021) Validating eDNA measurements of the richness and abundance of anurans at a large scale. J Animal Ecol 90:1466–1479
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (42) https://doi.org/10.1111/1365-2656.13468
  44. Matsui M, Hayashi T (1992) Genetic uniformity in the Japanese giant salamander, Andrias japonicus. Copeia 1992:232–235
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (43) https://doi.org/10.2307/1446557
  45. Matsui M, Tominaga A, Liu WZ, Tanaka-Ueno T (2008) Reduced genetic variation in the Japanese giant salamander, Andrias japonicus (Amphibia: Caudata). Mol Phylogenet Evol 49:318–326
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (44) https://doi.org/10.1016/j.ympev.2008.07.020
  46. Minamoto T, Yamanaka H, Takahara T, Honjo MN, Kawabata Z (2012) Surveillance of fish species composition using environmental DNA. Limnology 13:193–197
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (45) https://doi.org/10.1007/s10201-011-0362-4
  47. Minamoto T, Uchii K, Takahara T, Kitayoshi T, Tsuji S, Yamanaka H, Doi H (2017) Nuclear internal transcribed spacer-1 as a sensitive genetic marker for environmental DNA studies in common carp Cyprinus carpio. Mol Ecol Resour 17:324–333
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (46) https://doi.org/10.1111/1755-0998.12586
  48. Minamoto T, Hayami K, Sakata MK, Imamura A (2019) Real-time polymerase chain reaction assays for environmental DNA detection of three salmonid fish in Hokkaido, Japan: application to winter surveys. Ecol Res 34:237–242
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (47) https://doi.org/10.1111/1440-1703.1018
  49. Ministry of the Environment, Japan (2020) Ministry of the Environment, Japan, Red list, 4th edn. http://www.env.go.jp/press/files/jp/114457.pdf. Accessed on 6 December 2020 (in Japanese)
  50. Okada S, Utsunomiya T, Okada T, Felix ZI, Ito F (2008) Characteristics of Japanese giant salamander (Andrias japonicus) populations in two small tributary streams in Hiroshima Prefecture, western Honshu, Japan. Herpetol Conserv Biol 3:192–202
  51. Okada S, f*ckuda Y, Takahashi MK (2015) Paternal care behaviors of Japanese giant salamander Andrias japonicus in natural populations. J Ethol 33:1–7
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (48) https://doi.org/10.1007/s10164-014-0413-5
  52. Pilliod DS, Goldberg CS, Arkle RS, Waits LP (2013) Estimating occupancy and abundance of stream amphibians using environmental DNA from filtered water samples. Can J Fish Aquat Sci 70:1123–1130
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (49) https://doi.org/10.1139/cjfas-2013-0047
  53. Pitt AL, Shinskie JL, Tavano JJ, Hartzell SM, Delahunty T, Spear SF (2017) Decline of a giant salamander assessed with historical records, environmental DNA and multi-scale habitat data. Freshw Biol 62:967–976
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (50) https://doi.org/10.1111/fwb.12917
  54. R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 13 September 2023
  55. Riaz M, Kuemmerlen M, Wittwer C, Cocchiararo B, Khaliq I, Pfenninger M, Nowak C (2020) Combining environmental DNA and species distribution modeling to evaluate reintroduction success of a freshwater fish. Ecol Appl 30:e02034
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (51) https://doi.org/10.1002/eap.2034
  56. Sakata MK, Watanabe T, Maki N, Ikeda K, Kosuge T, Okada H, Yamanaka H, Sado T, Miya M, Minamoto T (2021) Determining an effective sampling method for eDNA metabarcoding: a case study for fish biodiversity monitoring in a small, natural river. Limnology 22:221–235
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (52) https://doi.org/10.1007/s10201-020-00645-9
  57. Schrader C, Schielke A, Ellerbroek L, Johne R (2012) PCR inhibitors—occurrence, properties and removal. J Appl Microbiol 113:1014–1026
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (53) https://doi.org/10.1111/j.1365-2672.2012.05384.x
  58. Sigsgaard EE, Nielsen IB, Bach SS, Lorenzen ED, Robinson DP, Knudsen SW, Pedersen MW, Jaidah MA, Orlando L, Willerslev E, Møller PR, Thomsen PF (2016) Population characteristics of a large whale shark aggregation inferred from seawater environmental DNA. Nat Ecol Evol 1:0004
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (54) https://doi.org/10.1038/s41559-016-0004
  59. Spear SF, Groves JD, Williams LA, Waits LP (2015) Using environmental DNA methods to improve detectability in a hellbender (Cryptobranchus alleganiensis) monitoring program. Biol Conserv 183:38–45
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (55) https://doi.org/10.1016/j.biocon.2014.11.016
  60. Strickler KM, Fremier AK, Goldberg CS (2015) Quantifying effects of UV-B, temperature, and pH on eDNA degradation in aquatic microcosms. Biol Conserv 183:85–92
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (56) https://doi.org/10.1016/j.biocon.2014.11.038
  61. Toju H, Tanabe AS, Yamamoto S, Sato H (2012) High-coverage ITS primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PLoS ONE 7:e40863
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (57) https://doi.org/10.1371/journal.pone.0040863
  62. Turvey ST, Marr MM, Barnes I, Brace S, Tapley B, Murphy RW, Zhao E, Cunningham AA (2019) Historical museum collections clarify the evolutionary history of cryptic species radiation in the world’s largest amphibians. Ecol Evol 9:10070–10084
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (58) https://doi.org/10.1002/ece3.5257
  63. Wakimura K, Uchii K, Kikko T (2023) Evaluation of genetic diversity in an endangered fish Gnathopogon caerulescens using environmental DNA and its potential use in fish conservation. Environ DNA 5:973–986. https://doi.org/10.1002/edn3.408
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (59) https://doi.org/10.1002/edn3.408
  64. Wilcox TM, Young MK, McKelvey KS, Isaak DJ, Horan DL, Schwartz MK (2018) Fine-scale environmental DNA sampling reveals climate-mediated interactions between native and invasive trout species. Ecosphere 9:e02500
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (60) https://doi.org/10.1002/ecs2.2500
  65. Willson JD, Dorcas ME (2003) Effects of habitat disturbance on stream salamanders: implications for buffer zones and watershed management. Conserv Biol 17:763–771
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (61) https://doi.org/10.1046/j.1523-1739.2003.02069.x
  66. Wineland SM, Welch SM, Pauley TK, Apodaca JJ, Olszack M, Mosher JJ, Holmes JN, Waldron JL (2019) Using environmental DNA and occupancy modelling to identify drivers of eastern hellbender (Cryptobranchus alleganiensis alleganiensis) extirpation. Freshw Biol 64:208–221
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (62) https://doi.org/10.1111/fwb.13210
  67. Wu L, Yamamoto Y, Yamaguchi S, Minamoto T (2022) Spatiotemporal changes in environmental DNA concentrations caused by fish spawning activity. Ecol Indic 142:109213
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (63) https://doi.org/10.1016/j.ecolind.2022.109213
  68. Yao M, Zhang S, Lu Q, Chen X, Zhang SY, Kong Y, Zhao J (2022) Fishing for fish environmental DNA: ecological applications, methodological considerations, surveying designs, and ways forward. Mol Ecol 31:5132–5164
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (64) https://doi.org/10.1111/mec.16659
  69. Yoshikawa N, Kaneko S, Kuwabara K, Okumura N, Matsui M, Isagi Y (2011) Development of microsatellite markers for the two giant salamander species (Andrias japonicus and A. davidianus). Curr Herpetol 30:177–180
    Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (65) https://doi.org/10.5358/hsj.30.177

About this publication

Number of citations 0
Number of works in the list of references 69
Journal indexed in Scopus Yes
Journal indexed in Web of Science Yes

ASJC classification

1104 Aquatic Science
2312 Water Science and Technology
2303 Ecology
Sensitive and efficient surveillance of Japanese giant salamander (Andrias japonicus) distribution in western Japan usi… (2024)

References

Top Articles
Latest Posts
Article information

Author: Sen. Ignacio Ratke

Last Updated:

Views: 6214

Rating: 4.6 / 5 (76 voted)

Reviews: 83% of readers found this page helpful

Author information

Name: Sen. Ignacio Ratke

Birthday: 1999-05-27

Address: Apt. 171 8116 Bailey Via, Roberthaven, GA 58289

Phone: +2585395768220

Job: Lead Liaison

Hobby: Lockpicking, LARPing, Lego building, Lapidary, Macrame, Book restoration, Bodybuilding

Introduction: My name is Sen. Ignacio Ratke, I am a adventurous, zealous, outstanding, agreeable, precious, excited, gifted person who loves writing and wants to share my knowledge and understanding with you.