Limitations of eDNA analysis for Carcinus maenas abundance estimations

Ariella M. Danziger1, Zachary H. Olson2, Markus Frederich1
1School of Marine and Environmental Programs, University of New England, 11 Hills Beach Rd, Biddeford, ME, USA
2University of New England, School of Social and Behavioral Sciences, Animal Behavior Program, 11 Hills Beach Rd, Biddeford, ME, USA

Tóm tắt

Abstract Background Environmental DNA (eDNA) is an effective tool for the detection and monitoring of presence or absence of rare and invasive species. These techniques have been extended to quantify biomass in vertebrates, particularly in fish species. However, the efficacy of eDNA techniques to quantify biomass in invertebrate species has rarely been examined. This study tested whether eDNA could be used to determine the biomass of the world-wide invasive green crab, Carcinus maenas. In a controlled laboratory study, the relationship between biomass and C. maenas eDNA concentration was examined in the context of different biotic (activity) and abiotic (temperature) parameters. Results When incubating different numbers of crabs in sterile saltwater for up to 7 days, a relationship between eDNA concentration and biomass was observed at temperatures of 6.7 ℃ and 18.7 ℃, but not at 12.8 ℃. Additionally, motor activity, aggression level, time of sampling, and features of organismal decay had significant impact on the concentration of C. maenas eDNA collected. Conclusions We show that eDNA concentration did not correlate with biomass, and that biomass, temperature, organismal characteristics, and potentially many more parameters affect shedding and degradation rates for eDNA in this species, thus, impacting the recoverable eDNA concentration. Therefore, eDNA techniques are not likely to provide a reliable signal of biomass in the invasive invertebrate species C. maenas.

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Tài liệu tham khảo

Taberlet P, Coissac E, Hajibabaei M, Rieseberg LH. Environmental DNA. Molec Ecol. 2012;21(8):1789–93.

Thomsen PF, Willerslev E. Environmental DNA—an emerging tool in conservation for monitoring past and present biodiversity. Biol Conserv. 2015;183:4–18.

Deiner K, Altermatt F. Transport distance of invertebrate environmental DNA in a natural river. PLoS ONE. 2014;9(2):e88786.

Strickler KM, Fremier AK, Goldberg CS. Quantifying effects of UV-B, temperature, and pH on eDNA degradation in aquatic microcosms. Biol Conserv. 2015;183:85–92.

Foote AD, Thomsen PF, Sveegaard S, Wahlberg M, Kielgast J, Salling AB, Galatius A, Orlando L, Gilbert MTP. Investigating the potential use of environmental DNA (eDNA) for genetic monitoring of marine mammals. PLoS ONE. 2012;7(8):e41781.

Thomsen PF, Kielgast J, Iversen LL, Møller PR, Rasmussen M. Detection of a diverse marine fish fauna using environmental DNA from seawater samples. PLoS ONE. 2012;7(8):41732.

Thomsen PF, Kielgast J, Iversen LL, Wiuf C, Rasmussen M, Gilbert MTP, Orlando L, Willerslev E. Monitoring endangered freshwater biodiversity using environmental DNA. Mol Ecol. 2012;21:2565–73.

Barnes MA, Turner CR, Jerde CL, Renshaw MA, Chadderton WL, Lodge DM. Environmental conditions influence eDNA persistence in aquatic systems. Env Sci Technol. 2014;48(3):1819–27.

Eichmiller JJ, Best SE, Sorensen PW. Effects of temperature and trophic state on degradation of environmental DNA in lake water. Env Sci Technol. 2016;50:1859–67.

Sassoubre LM, Yamahara KM, Gardner LD, Block BA, Boehm AB. Quantification of environmental DNA (eDNA) shedding and decay rates for three marine fish. Env Sci Technol. 2016;50:10456–64.

Dejean T, Valentini A, Duparc A, Pellier-Cuit S, Pompanon F, Taberlet P, Miaud C. Persistence of environmental DNA in freshwater ecosystems. PLoS ONE. 2011;6(8):e23398.

Barnes MA, Turner CR. The ecology of environmental DNA and implications for conservation genetics. Conserv Genetics. 2016;17(1):1–17.

Harrison JB, Sunday JM, Rogers SM. Predicting the fate of eDNA in the environment and implications for studying biodiversity. Proc Royal Soc B Biol Sci. 2019;286:20191409.

Goldberg CS, Pilliod DS, Arkle RS, Waits LP. Molecular detection of vertebrates in stream water: a demonstration using Rocky Mountain tailed frogs and Idaho giant salamanders. PLoS ONE. 2011;6:e22746.

Klymus KE, Richter CA, Chapman DC, Paukert C. Quantification of eDNA shedding rates from invasive bighead carp Hypophthalmichthys nobilis and silver carp Hypophthalmichthys molitrix. Biol Conserv. 2015;183:77–84.

Pilliod DS, Goldberg CS, Arkle RS, Waits LP. Factors influencing detection of eDNA from a stream-dwelling amphibian. Molec Ecol Res. 2014;14(1):109–16.

Song JW, Small MJ, Casman EA. Making sense of the noise: the effect of hydrology on silver carp eDNA detection in the Chicago area waterway system. Sci Total Env. 2017;605–606:713–20.

Maruyama A, Nakamura K, Yamanaka H, Kondoh M, Minamoto T. The release rate of environmental DNA from juvenile and adult fish. PLoS ONE. 2014;9(12):e114639.

Turner CR, Barnes MA, Xu CCY, Jones SE, Jerde CL, Lodge DM. Particle size distribution and optimal capture of aqueous macrobial eDNA. Methods Ecol Evol. 2014;5(7):676–84.

Zhu B. Degradation of plasmid and plant DNA in water microcosms monitored by natural transformation and real-time polymerase chain reaction (PCR). Water Res. 2006;40:3231–8.

Doi H, Inui R, Akamatsu Y, Kanno K, Yamanaka H, Takahara T, Minamoto T. Environmental DNA analysis for estimating the abundance and biomass of stream fish. Freshwater Biol. 2017;62(1):30–9.

Lacoursière-Roussel A, Rosabal M, Bernatchez L. Estimating fish abundance and biomass from eDNA concentrations: variability among capture methods and environmental conditions. Molec Ecol Resources. 2016;16(6):1401–14.

Takahara T, Minamoto T, Yamanaka H, Doi H, Kawabata Z. Estimation of fish biomass using environmental DNA. PLoS ONE. 2012;7(4):e35868.

Wu Q, Kawano K, Uehara Y, Okuda N, Hongo M, Tsuji S, Yamanaka T, Minamoto T. Environmental DNA reveals nonmigratory individuals of Palaemon paucidens overwintering in Lake Biwa shallow waters. Freshwater Sci. 2018;37(2):307–14.

Ficetola GF, Miaud C, Pompanon F, Taberlet P. Species detection using environmental DNA from water samples. Biol Lett. 2008;4(4):423–5.

Olson ZH, Briggler JT, Williams RN. An eDNA approach to detect eastern hellbenders (Cryptobranchus a. alleganiensis) using samples of water. Wildlife Res. 2012;39(7):629–36.

Gherardi F, Aquiloni L, Diéguez-Uribeondo J, Tricarico E. Managing invasive crayfish: is there a hope? Aquat Sci. 2011;73:185–200.

Hinlo R, Furlan E, Suitor L, Gleeson D. Environmental DNA monitoring and management of invasive fish: comparison of eDNA and fyke netting. Manage Biol Invasions. 2017;8(1):89–100.

Tréguier A, Paillisson JM, Dejean T, Valentini A, Schlaepfer MA, Roussel JM. Environmental DNA surveillance for invertebrate species: advantages and technical limitations to detect invasive crayfish Procambarus clarkii in freshwater ponds. J Appl Ecol. 2014;51(4):871–9.

Dougherty MM, Larson ER, Renshaw MA, Gantz CA, Egan SP, Erickson DM, Lodge DM. Environmental DNA (eDNA) detects the invasive rusty crayfish Orconectes rusticus at low abundances. J Appl Ecol. 2016;53(3):722–32.

Larson ER, Renshaw MA, Gantz CA, Umek J, Chandra S, Lodge DM, Egan SP. Environmental DNA (eDNA) detects the invasive crayfishes Orconectes rusticus and Pacifastacus leniusculus in large lakes of North America. Hydrobiologia. 2017;800(1):173–85.

Griffen BD, Riley ME. Potential impacts of invasive crabs on one life history strategy of native rock crabs in the Gulf of Maine. Biol Invasions. 2015;17(9):2533–44.

Tan EBP, Beal BF. Interactions between the invasive European green crab, Carcinus maenas (L.), and juveniles of the soft-shell clam, Mya arenaria L., in eastern Maine, USA. J Exp Mar Biol Ecol. 2015;462:62–73.

Neckles HA. Loss of Eelgrass in Casco Bay, Maine, linked to green crab disturbance. Northeast Nat. 2015;22(3):478–500.

Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL, Hughes HR, Kendrick GA, Kenworthy WJ, Olyarnik S, Short FT, Waycott M, Williams SL. A global crisis for seagrass ecosystems. Bioscience. 2006;56(12):987–96.

Carlton JT, Cohen AN. Episodic global dispersal in shallow water marine organisms: the case history of the European shore crabs Carcinus maenas and C. aestuarii. J Biogeogr. 2003;30:1809–20.

Hidalgo FJ, Barón PJ, Orensanz JM. A prediction come true: the green crab invades the Patagonian coast. Biol Invasions. 2005;7:547–52.

Roman J. Diluting the founder effect: cryptic invasions expand a marine invader’s range. Proc Royal Soc B: Biol Sci. 2006;273:2453–9.

Aronson RB, Frederich M, Price R, Thatje S. Prospects for the return of shell-crushing crabs to Antarctica. J Biogeogr. 2015;42(1):1–7.

Danziger AM, Frederich M. Challenges in eDNA detection of the invasive European green crab, Carcinus maenas. Biol Invasions. 2022 (in press).

Mountain DG. Labrador slope water entering the Gulf of Maine-response to the North Atlantic Oscillation. Continent Shelf Res. 2012;47:150–5.

Torre MP, Tanaka KR, Chen Y. A spatiotemporal evaluation of Atlantic Sea Scallop Placopecten magellanicus habitat in the Gulf of Maine using a bioclimate envelope model. Mar Coast Fish. 2018;10:224–35.

Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL. Effects of size and temperature on metabolic rate. Science. 2001;293(5538):2248–51.

Rayner G, McGaw IJ. Effects of the invasive green crab (Carcinus maenas) on American lobster (Homarus americanus): Food acquisition and trapping behaviour. J Sea Res. 2019;144:95–104.

Botta W. Why are crabs so crabby? Possible role of biogenic amines in aggression in the European green crab Carcinus maenas. Master’s Thesis, University of New England, 2020; pp. 52.

Saito T, Doi H. Environmental DNA degradation simulation from water temperature and DNA fragment length: a meta-analysis approach. Frontiers Ecol Evol. 2021;9:623831.

Crane LC, Goldstein JS, Thomas DW, Rexroth KS, Watts AW. Effects of life stage on eDNA detection of the invasive European green crab (Carcinus maenas) in estuarine systems. Ecol Indicators. 2021;124:107412.

Lindahl T. Instability and decay of the primary structure of DNA. Nature. 1993;363(6422):709–15.

Smith CI, Chamberlain AT, Riley MS, Cooper A, Stringer CB, Collins MJ. Neanderthal DNA: not just old but old and cold? Nature. 2001;10:771–2.

Okabe S, Shimazu Y. Persistence of host-specific Bacteroides-Prevotella 16S rRNA genetic markers in environmental waters: effects of temperature and salinity. Appl Microbiol Biotechnol. 2007;76:935–44.

Spear SF, Groves JD, Williams LA, Waits LP. Using environmental DNA methods to improve detectability in a hellbender (Cryptobranchus alleganiensis) monitoring program. Biol Conserv. 2015;183:38–45.

Biggs J, Ewald N, Valentini A, Gaboriaud C, Dejean T, Griffiths RA, Foster J, Wilkinson JW, Arnell A, Brotherton P, Williams P, Dunn F. Using eDNA to develop a national citizen science-based monitoring programme for the great crested newt (Triturus cristatus). Biol Conserv. 2015;183:19–28.

Curtis AN, Larson ER. No evidence that crayfish carcasses produce detectable environmental DNA (eDNA) in a stream enclosure experiment. Peer J. 2020;8:e9333.

Pennoyer KE, Himes AR, Frederich M. Effects of sex and color phase on ion regulation in the invasive European green crab, Carcinus maenas. Marine Biol. 2016;163(6):1–15.

Logan L. One crab to rule them all: a comparison between Carcinus maenas populations with stress physiology behavior and habitat destruction. Master’s Thesis, University of New England, 2018; pp. 83.

Wobbrock JO, Findlater L, Gergle D, Higgins JJ. The Aligned Rank Transform for nonparametric factorial analyses using only ANOVA procedures. Proceedings of the ACM Conference on Human Factors in Computing Systems (CHI '11). Vancouver, British Columbia (May 7–12, 2011). New York: ACM Press, 2001; pp. 143–146.