Tracking individual animals with small-sized passive integrated transponder tags (PIT tags) has become a popular and widespread method, one which can be used for investigating life history traits, including dispersal patterns of small protected animals such as newts. In this study, we tested the applicability of PIT tag usage for individual marking with the Great crested newt (Triturus cristatus) as a model amphibian species, and to test the detection of the newts in nature using a passive telemetry system. Clove oil was used as an anaesthetic before surgery. We implanted PIT tags under the skin of 140 newts. The survival rate of newts was 98.57%. X-ray images were taken to check the exact positions of the PIT tags. Since approximately 15.71% of the newts were capable of expelling the tag from their bodies, tag loss has to be accounted for in future behavioural studies dealing with newts and other amphibians potentially capable of frequent tag expulsion. Lastly, we detected by passive telemetry 97 individuals out of 100 released into a natural breeding pond. Males had higher activity (13 detected males vs 7 females per hour) than females, thus males could be detected if present with more certainty. The result of the movement behaviour showed that e.g. the male of T. cristatus in a breeding pond can travel up to 20 m in 78 seconds. In summary, this promising method could allow the automatic data collection of marked newts in aquatic as well as in terrestrial biotopes, providing data on their dispersal, diurnal activity and movement behaviour.

Biology Centre of the Czech Academy of Sciences Institute of Hydrobiology České Budějovice Czech Republic

Department of Ecology and Environmental Sciences Faculty of Science Palacký University Olomouc Czech Republic

Zobrazit více v PubMed

Houlahan JE, Findlay CS, Schmidt BR, Meyer AH, Kuzmin SL. Quantitative evidence for global amphibian population declines. Nature. 2000; 404: 752–755. 10.1038/35008052 PubMed DOI

Beebee TJC, Griffiths RA. Amphibians and Reptiles A Natural History of the British Herpetofauna. Harper Collins Publishers, London, UK: 2000; 270 pp.

Arntzen JW, Kuzmin S, Jehle R, Beebee T, Tarkhnishvili D, Ishchenko V et al. Triturus cristatus. The IUCN Red List of Threatened Species 2009: e.T22212A9365894. 10.2305/IUCN.UK.2009.RLTS.T22212A9365894.en. Downloaded on 02 June 2019. DOI

Gustafson D. Choosing the Best of Both Worlds, The Double Life of the Great Crested Newt. Doctoral Thesis. Swedish University of Agricultural Sciences Skinnskatteberg. 2011; 64 pp.

Vojar J. Ochrana obojživelníků: ohrožení, biologické principy, metody studia, legislativní a praktická ochrana. Doplněk k metodice č. 1 Českého svazu ochránců přírody. ZO ČSOP Hasina Louny. 2007; 156 pp.

Nathan R, Getz WM, Revilla E, Holyoak M, Kadmon R, Saltz D et al. A movement ecology paradigm for unifying organismal movement research. Proc Natl Acad Sci USA. 2008; 105: 19052–19059. 10.1073/pnas.0800375105 PubMed DOI PMC

Fahrig L. Non-optimal animal movement in human-altered landscapes. Funct Ecol. 2007; 21:1003–1015.

Clobert J, Le Galliard J-F, Cote J, Meylan S, Massot M. Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol Lett. 2009; 12:197–209. 10.1111/j.1461-0248.2008.01267.x PubMed DOI

Ousterhout BH, Semlitsch RD. Measuring terrestrial movement behavior using passive integrated transponder (PIT) tags: effects of tag size on detection, movement, survival, and growth. Behav Ecol Sociobiol. 2014; 68:343–350.

Schmidt BR, Feldmann R, Schaub M. Demographic processes underlying population growth and decline in Salamandra salamandra. Conserv Biol. 2005; 19(4):1149–1156.

Chevalier H, Calvez O, Martínez-Silvestre A, Picard D, Guérin S, Isselin-Nondedeu F et al. Marking techniques in the Marbled newt (Triturus marmoratus): PIT-Tag and tracking device implant protocols. Acta Herpetol. 2017; 12(1):79–88.

Drechsler A, Helling T, Steinfartz S. Genetic fingerprinting proves cross-correlated automatic photoidentification of individuals as highly efficient in large capture–mark–recapture studies. Ecol. Evol. 2015; 5: 141–151. 10.1002/ece3.1340 PubMed DOI PMC

Mettouris O, Megremis G, Giokas S. A newt does not change its spots: using pattern mapping for the identification of individuals in large populations of newt species. Ecol. Res. 2016; 31: 483–489.

Bubb DH, Lucas MC, Thom TJ, Rycroft P. The potential use of PIT telemetry for identifying and tracking crayfish in their natural environment. Hydrobiologia. 2002; 483:225–230.

Cucherousset J, Britton JR, Beaumont WRC, Nyqvist M, Sievers K, Gozl RE. Determining the effects of species, environmental conditions and tracking method on the detection efficiency of portable PIT telemetry. J Fish Biol. 2010; 76:1039–1045.

Hamed MK, Ledford DP, Laughl TF. Monitoring nonbreeding habitat activity by subterranean detection of ambystomatid salamanders with implanted passive integrated transponder (PIT) tags and a radio frequency identification (FRID) antenna system. Herpetol Rev. 2008; 39:303–306.

Connette GM, Semlitsch RD. Successful use of a passive integrated transponder (PIT) system for below-ground detection of plethodontid salamanders. Wildl Res. 2012; 39:1–6.

Winandy L, Denoël M. The use of visual and automatized behavioural markers to assessasses methodologies: a study case on PIT-tagging in the alpine newt. Behav Res Methods. 2011; 43:568–576. 10.3758/s13428-011-0058-z PubMed DOI

Atkinson-Adams MR, Paszkowski C, Scrimgeour G. Effects of substrate on PIT tag detection with a self-made portable RFID antenna: implications for PIT telemetry. Herpetol Rev. 2016; 47(2):198–201.

Bonter DN, Bridge ES. Applications of radio frequency identification (RFID) in ornithological research: a review. J Field Ornithol. 2001; 82:1–10.

Wilkin TA, King LE, Sheldon BC. Habitat quality, nestling diet, and provisioning behaviour in Great Tits Parus major. J Avian Biol. 2009; 40: 135–145.

Zangmeister JL, Haussmann MF, Cerchiara J, Mauck RA. Incubation failure and nest abandonment by Leach’s Storm-Petrels detected using PIT tags and temperature loggers. J Field Ornithol. 2009; 80: 373–379.

González-Solís J, Becker PH, Wendeln H. Divorce and asynchronous arrival in common terns, Sterna hirundo. Anim Behav. 1999; 58(5): 1123–1129. 10.1006/anbe.1999.1235 PubMed DOI

Thomson RL, Sirkiä PM, Villers A, Laaksonen T. Temporal peaks in social information: prospectors investigate conspecific nests after a simulated predator visit. Behav Ecol Sociobiol. 2013; 67: 905–911.

Becker PH, Dittmann T, Ludwigs JD, Limmer B, Ludwigs SC, Bauch C et al. Timing of initial arrival at the breeding site predicts age at first reproduction in a long-lived migratory bird. Proc Natl Acad Sci USA. 2008; 105: 12349–12352. 10.1073/pnas.0804179105 PubMed DOI PMC

Cooke SJ, Midwood JD, Thiem JD, Klimley P, Lucas MC, Thorstad EB et al. Tracking animals in freshwater with electronic tags: past, present and future. Anim. Biotelem. 2013; 1:5.

Langton TES, Beckett CL, Foster JP. Great Crested Newt Conservation Handbook, Froglife, Halesworth: 2001; 60 pp.

Gvoždík L, Van Damme R. Triturus newts defy the running–swimming dilemma. Evolution. 2006; 60(10): 2110–2121. PubMed

Jehle R, Thiesmeier B, Foster J. The Crested Newt: A dwindling pond–dweller. Laurenti–Verlag, Bielefeld: 2011; 152 pp.

Cayuela H, Schmidt BR, Weinbach A, Besnard A, Joly P. Multiple density dependent processes shape the dynamics of a spatially structured amphibian population. J Anim Ecol. 2019; 88:164–177. 10.1111/1365-2656.12906 PubMed DOI

Mitchell MA. Anaesthetic considerations for amphibians. J Exot Pet Med. 2009; 18:40–49.

ARG UK Advice Note 5: Great Crested Newt habitat suitability index. Amphibian and Reptile Groups of the United Kingdom.2010.

Heyer WR, Donnelly MA, Foster M, McDiarmid RW (eds.). Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians. Smithsonian Institution Press, Washington D.C. 1994; 384 pp.

Hutchens SJ, DePerno CS. Efficacy of sampling techniques for determining species richness estimates of reptiles and amphibians. Wildl. Biol. 2009; 15:113–122.

Willson JD, Gibbons JW. Drift fences, coverboards, and other traps In Dodd CK Jr. (ed.), Amphibian Ecology and Conservation. 2009; pp. 229–245. Oxford University Press, Oxford, United Kingdom.

Pojman JA SR, Pojman JA JR, Fontenot CL JR. Use of clove oil as an anaesthetic for PIT tagging and surgery with the Three-toed Amphiuma (Amphiuma tridactylum) and determination of recovery time as a function of body mass. Herpetol Rev. 2014; 45(1):25–27.

Stokes WS. Humane Endpoints for Laboratory Animals Used in Regulatory Testing. ILAR J. 2002; 43(1):31–38. PubMed

Goulet F, Hélie P, Vachon P. Eugenol anesthesia in African clawed frogs (Xenopus laevis) of different body weights. J Am Assoc Lab Anim Sci. 2010; 49:460–463. PubMed PMC

R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria: 2017.

Hill MS, Zydlewski GB, Zydlewski JD, Gasvoda JM. Development and evaluation of portable PIT tag detection units: PITpacks. Fish Res. 2006; 77:102–109.

Linnansaari T, Roussel JM, Cunjak RA, Halleraker JH. Efficacy and accuracy of portable PIT-antennae when locating fish in ice-covered streams. Hydrobiologia. 2007; 582:281–287.

Ryan KJ, Zydlewski JD, Calhoun AJK. Using passive integrated transponder (PIT) systems for terrestrial detection of bluespotted salamanders (Ambystoma laterale) in situ. Herpetol Conserv Biol. 2014; 9:97–105.

Adams NS, Rondorf DW, Evans SD, Kelly JE. Effects of surgically and gastrically implanted radio transmitters on growth and feeding behavior of juvenile Chinook Salmon. Trans Am Fish Soc. 1998; 55(4): 781–787.

Bateman DS, Gresswell RE. Survival and Growth of Age-0 Steelhead after Surgical Implantation of 23-mm Passive Integrated Transponders. N Am J Fish Manag. 2006; 26: 545–550.

Zakęś Z, Wunderlich K, Szczepkowski M, Rożyński M. Tagging juvenile European whitefish (Coregonus lavaretus (L.)) with passive integrated transponders. Impact of fish size on growth performance and tag retention. Aquacult Res. 2017; 48, 5791–5796.

Jehle R, Hödl W. PITs versus patterns: effects of transponders on recapture rate and body condition of Danube crested newts (Triturus dobrogicus) and common spadefoot toads (Pelobates fuscus). Herpetol J. 1998; 8:181–186.

Arntzen JW, Smithson A, Oldham RS. Marking and tissue sampling effects on body condition and survival in the newt Triturus cristatus. J Herpetol. 1999; 33(4):567–576.

Perret N, Joly P. Impacts of tattooing and PIT-tagging on survival and fecundity in the alpine newt (Triturus alpestris). Herpetologica. 2002; 58(1): 131–138.

Dervo B, Skei JK, Berg OK, Kraabøl M., Arnemo JM, Dolmen D. A comparison of external and internal attachments of radiotransmitters on adult crested newts Triturus cristatus. Amphib-Reptil. 2010; 31 (2010): 229–237.

Dieterman DJ, Hoxmeier RJH. Instream evaluation of passive integrated transponder retention in brook trout and brown trout: effects of season, anatomical placement, and fish length. North Am J Fish Manag. 2009; 29(1):109–15

Mamer ERJM, Meyer KA. Retention rates of passive integrated transponder tags, visible implant elastomer tags, and maxillary marks in wild trout. North Am J Fish Manag. 2016; 36(5):1119–24.

Rittenhouse TAG, Semlitsch RD. Grasslands as movement barriers for a forest associated salamander: migration behaviour of adult and juvenile salamanders in a distinct habitat edge. Biol. Conserv. 2006; 131: 14–22.

McDonough C, Paton PWC. Salamander dispersal across a forested landscape fragmented by a golf course. J. Wildl. Manage. 2007; 71: 1163–1169.

Semlitsch RD, Metts BS, Greene JL. Observations on emigration and habitat use by eastern tiger salamanders, Ambystoma tigrinum, in South Carolina. Herpetol. Rev. 2007; 38: 399–402.

Peterman WE, Crawford JA & Semlitsch RD. Productivity and significance of headwater streams: population structure and biomass of the black-bellied salamander (Desmognathus quadramaculatus). Fresh. Biol. 2008; 53: 347–357.

Ward DL, David J. Evaluation of Pit Tag Loss and Tag-induced Mortality in Bluehead Sucker (Catostomus discobolus). J Ariz Nev Acad Sci. 2018; 38:2, 74–76.

Pearson KN, Kendall WL, Winkelman DL, Persons WR. Trade-offs between physical captures and PIT tag antenna array detections: A case study for the Lower Colorado River Basin population of humpback chub (Gila cypha). Fisheries Research. 2016; 183 (2016) 263–274.

Wedemeyer GA, Barton BA, McLeay DJ. Stress and acclimation In:Schreck C.B., Moyle P.B. (Eds.), Methods for Fish Biology. American Fisheries Society, Bethesda, Maryland; 1990. pp. 451–489.

Paukert CP, Chvala PJ, Heikes BL, Brown ML. Effects of implanted transmitter size and surgery on survival, growth, and wound healing of bluegill. Trans. Am. Fish. Soc. 2001; 130, 975–980.

Trochet A, Le Chevalier H, Calvez O, Barthe L, Isselin-Nondedeu F, Picard D, Debelgarric M, Pégourié N, Rocher R, Ribéron A. Post-breeding movements in marbled newts (Caudata, Salamandridae): a comparative radiotracking study in two habitat types. Herpetologica. 2017; 73: 1–9.

Olders JHJ, van Gelder JJ, Krammer J. A thermo-sensitive transmitter for radiotracking small animals. Neth. J. Zool. 1985; 35: 479–485.

Madison DM, Farrand L. Habitat use during breeding and emigration in radio-implanted tiger salamanders, Ambystoma tigrinum. Copeia. 1998; 402–410.

Johnson JR. Success of intracoelomic radiotransmitter implantation in the treefrog, Hyla versicolor. Lab. Animal. 2006; 35: 29–33. PubMed

Marcec R, Kouba A, Zhang L, Zhang H, Wang Q, Zhao H, Jiang W, Willard S. Surgical implantation of coelomic radiotransmitters and postoperative survival of Chinese giant salamanders (Andrias davidianus) following reintrodution. J. Zoo.Wildl. Med. 2016; 47: 187–95. 10.1638/2015-0044.1 PubMed DOI

Naef-Daenzer B, Früh D, Stalder M, Wetli P, Weise E. Miniaturization (0.2 g) and evaluation of attachment techniques of telemetry transmitters. J. Exp. Biol. 2005; 208: 4063–4068. 10.1242/jeb.01870 PubMed DOI

Richards SJ, Sinsch U, Alford R. Radio tracking In: Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians; 1994. pp 155–158. Heyer W.R., Donnelly M.A., McDiarmid R.W., Heyek L.C., Foster M.S., Eds, Smithsonian, Washington.

Jehle R. The terrestrial summer habitat of radiotracked great crested newts (Triturus cristatus) and marbled newts (T. marmoratus). Herp. J. 2000; 10: 137–142.

Gibbons WJ, Andrews KM.PIT Tagging: Simple Technology at Its Best. BioScience. 2004; 54(5):447–454.

Skov C, Brodersen J, Brönmark Ch, Hansson L-A, Hertonsson P, Nilsson A. Evaluation of PITtagging in cyprinids. J Fish Biol. 2005; 67:1195–1201.

Ratnayake CP, Morosinotto C, Ruuskanen S, Villers, Thomson RL. Passive Integrated Transponders (PIT) on a small migratory passerine bird: absence of deleterious short and long-term effects. Ornis Fennica. 2014; 91:244–255.

Jepsen N et al. Surgical implantation of telemetry transmitters in fish: how much have we learned? Hydrobiologia. 2002; 483:239–248.

Foldvik A, Kvingedal E. Long-term PIT tag retention rates in Atlantic salmon (Salmo salar). Anim Biotelemetry. 2018; 6:3 10.1186/s40317-018-0147-1. DOI

Bateman DS, Gresswell RE, Berger AM. Passive integrated transponder tag retention rates in headwater populations of coastal cutthroat trout. North Am J Fish Manag. 2009; 29(3):653–657.

Meyer KA, High B, Gastelecutto N, Mamer E, Steven EF. Retention of passive integrated transponder tags in stream-dwelling rainbow trout. North Am J Fish Manag. 2011; 31(2):236–239.

Clarke J, Kerry K. Implanted transponders in penguins: implantation, reliability, and long-term effects. J Field Ornithol. 1998; 69: 149–159.

Becker PH, Wendeln H. A new application for transponders in population ecology of the Common Tern. Condor. 1997; 99: 534–538.

Lebl K & Ruf T 2010 An easy way to reduce PIT-tag loss in rodents. Ecol Res. 2010; 25: 251–253.

Himstedt W. Die Tagesperiodik von Salamandriden. Oecologia. 1971; 8:194–208. PubMed

Dolmen D. Diel rhythms and microhabitat preference of the newts Triturus vulgaris and T. cristatus at the northern border of their distribution. J Herpetol.1983; 17:23–31.

Pojman JA Sr, Pojman JA Jr, Fontenot CL Jr. Comparison of immobilization methods for PIT tagging three-toed amphiuma (Amphiuma tridactylum). Herpetol. Rev. 2011; 42:362–363.

Wright KM, Whitaker BR. Amphibian Medicine and Captive Husbandry. Krieger Pub Co; 1. edition 2001. (October), Malabar.

Negative feedback concept in tagging: Ghost tags imperil the long-term monitoring of fishes