Abstract
Identifying and tracking individuals across time are a prerequisite to uncover key traits of their ecology and behavior. However, obtaining fine-grain individual data at multiple locations, especially in aquatic environments, is challenging due to trade-offs between time constraints and detection probabilities. Aquatic telemetry of passive integrated transponder (PIT)-tagged organisms has been proposed to cope with detectability issues, but its efficiency has not been tested in stagnant waters. This technology was evaluated in ponds by monitoring marsh frogs (Pelophylax ridibundus). Multivariate survival models were fitted to quantify the success of detection rates over detection times and across ponds characterized by different habitat features. An average detection rate of 81% was obtained in less than 18 min on average, whereas a maximum detection rate was achieved in almost a quarter of the surveys. The detection rates were lower in the deeper and larger ponds but increasing detection times improved detection probabilities. Altogether, these results show that PIT-tag telemetry is a powerful tool to survey aquatic organisms, such as pond-breeding amphibians. The generalization of the use of this monitoring technique in ponds can therefore encompass fine-grain analyses over numerous sites and fill the gap between studies at local and landscape scales.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Aldridge, H. D. J. N. & R. M. Brigham, 1988. Load carrying and maneuverability in an insectivorous bat: a test of the 5% ‘rule’ of radio-telemetry. Journal of Mammalogy 69: 379–382.
Arntzen, J. W., I. B. J. Goudie, J. Halley & R. Jehle, 2003. Cost comparison of marking techniques in long-term population studies: PIT-tags versus pattern maps. Amphibia-Reptilia 25: 305–315.
Bailey, L. L., T. R. Simons & K. H. Pollock, 2004. Spatial and temporal variation in detection probability of Plethodon salamanders using the robust capture-recapture design. Journal of Wildlife Management 68: 14–24.
Banish, N. P., S. M. Burdick & K. R. Moyer, 2016. Efficiency of portable antennas for detecting passive integrated transponder tags in stream-dwelling salmonids. PLoS ONE 11: e0149898.
Barbin Zydlewski, G., A. Haro, K. G. Whalen & S. D. McCormick, 2001. Performance of stationary and portable passive transponder detection systems for monitoring of fish movements. Journal of Fish Biology 58: 1471–1475.
Beranek, C. T., C. Maynard, C. McHenry, J. Clulow & M. Mahony, 2022. Identifying a limiting factor in the population dynamics of a threatened amphibian: The influence of extended female maturation on operational sex ratio. Austral Ecology 47: 239–250. https://doi.org/10.1111/aec.13098.
Blomquist, S. M., J. D. Zydlewski & M. L. Hunter, 2008. Efficacy of PIT tags for tracking the terrestrial anurans Rana pipiens and Rana sylvatica. Herpetological Review 39: 174–179.
Brown, L. J., 1997. An evaluation of some marking and trapping techniques currently used in the study of anuran population dynamics. Journal of Herpetology 31: 410–419.
Bubb, D. H., M. C. Lucas, T. J. Thom & P. Rycroft, 2002. The potential use of PIT telemetry for identifying and tracking crayfish in their natural environment. Hydrobiologia 483: 225–230.
Burnett, N. J., K. M. Stamplecoskie, J. D. Thiem & S. J. Cooke, 2013. Comparison of detection efficiency among three sizes of half-duplex passive integrated transponders using manual tracking and fixed antenna arrays. North American Journal of Fisheries Management 33: 7–13.
Canessa, S., G. W. Heard, K. M. Parris & M. A. McCarthy, 2012. Integrating variability in detection probabilities when designing wildlife surveys: a case study of amphibians from south-eastern Australia. Biodiversity and Conservation 21: 729–744.
Capellà-Marzo, B., G. Sánchez-Montes & Í. Martínez-Solano, 2020. Contrasting demographic trends and asymmetric migration rates in a spatially structured amphibian population. Integrative Zoology 15: 482–497.
Cayuela, H., A. Valenzuela-Sánchez, L. Teulier, Í. Martínez-Solano, J. P. Léna, J. Merilä, et al., 2020. Determinants and consequences of dispersal in vertebrates with complex life cycles: a review of pond-breeding amphibians. The Quarterly Review of Biology 95: 1–36.
Cayuela, H., Y. Dorant, B. R. Forester, D. L. Jeffries, R. M. Mccaffery, L. A. Eby, et al., 2021. Genomic signatures of thermal adaptation are associated with clinal shifts of life history in a broadly distributed frog. Journal of Animal Ecology 10: 1–17.
Christy, M., 1996. The efficacy of using Passive Integrated Transponder (PIT) tags without anaesthetic in free-living frogs. Australian Zoologist 30: 139–142.
Connette, G. M. & R. D. Semlitsch, 2012. Successful use of a passive integrated transponder (PIT) system for below-ground detection of plethodontid salamanders. Wildlife Research 39: 1–6.
Connock, J. R., B. F. Case, S. T. Button, J. Groffen, T. M. Galligan & W. A. Hopkins, 2019. Factors influencing in-situ detection of PIT-tagged hellbenders (Cryptobranchus alleganiensis) occupying artificial shelters using a submersible antenna. Herpetological Conservation and Biology 14: 429–437.
Cooke, S. J., S. G. Hinch, M. Wikelski, R. D. Andrews, L. J. Kuchel, T. G. Wolcott, et al., 2004. Biotelemetry: a mechanistic approach to ecology. Trends in Ecology & Evolution 19: 334–343.
Cooke, S. J., J. D. Midwood, J. D. Thiem, P. Klimley, M. C. Lucas, E. B. Thorstad, et al., 2013. Tracking animals in freshwater with electronic tags: past, present and future. Animal Biotelemetry 1: 1–19.
Cox, D. R., 1972. Regression models and life-tables. Journal of the Royal Statistical Society: Series B (methodological) 34: 187–202.
Cox, D. R. & D. Oakes, 2018. Analysis of Survival Data, Chapman and Hall, London.
Cucherousset, J., J. M. Roussel, R. Keeler, R. A. Cunjak & R. Stump, 2005. The use of two new portable 12-mm PIT tag detectors to track small fish in shallow streams. North American Journal of Fisheries Management 25: 270–274.
Cucherousset, J., P. Marty, L. Pelozuelo & J. M. Roussel, 2008. Portable PIT detector as a new tool for non-disruptively locating individually tagged amphibians in the field: a case study with Pyrenean brook salamanders (Calotriton asper). Wildlife Research 35: 780–787.
Cucherousset, J., J. R. Britton, W. R. C. Beaumont, M. Nyqvist, K. Sievers & R. E. Gozlan, 2010. Determining the effects of species, environmental conditions and tracking method on the detection efficiency of portable PIT telemetry. Journal of Fish Biology 76: 1039–1045.
Delcourt, J., M. Ovidio, M. Denoël, M. Muller, H. Pendeville, J. L. Deneubourg, et al., 2018. Individual identification and marking techniques for zebrafish. Reviews in Fish Biology and Fisheries 28: 839–864.
Denoël, M., S. Dalleur, E. Langrand, A. Besnard & H. Cayuela, 2018. Dispersal and alternative breeding site fidelity strategies in an amphibian. Ecography 41: 1543–1555.
Denoël, M., G. F. Ficetola, N. Sillero, G. Džukić, M. L. Kalezić, T. Vukov, et al., 2019. Traditionally managed landscapes do not prevent amphibian decline and the extinction of paedomorphosis. Ecological Monographs 89: e01347.
Dessai, S. & V. Patil, 2019. Testing and interpreting assumptions of COX regression analysis. Cancer Research, Statistics, and Treatment 2: 108–111.
Donnelly, M. A., C. Guyer, J. E. Juterbock & R. A. Alford, 1994. Techniques for marking amphibians. In Heyer, R., M. A. Donnelly, M. Foster & R. W. McDiarmid (eds), Measuring and monitoring biological diversity: standard methods for amphibians. Smithsonian Institution Press, Washington, DC: 277–284.
Dufresnes, C., M. Denoël, L. di Santo & S. Dubey, 2017. Multiple uprising invasions of Pelophylax water frogs, potentially inducing a new hybridogenetic complex. Scientific Reports 7: 1–10.
Durand-Tullou, A., 1959. Un milieu de Civilisation traditionnelle. Le Causse de Blandas. Published PhD Thesis. Faculté des Lettres et Sciences Humaines de Montpellier. Edition du Bedfroie, Millau, France.
Dzul, M. C., W. L. Kendall, C. B. Yackulic, D. L. Winkelman, D. R. Van Haverbeke & M. Yard, 2021. Partial migration and spawning movements of humpback chub in the Little Colorado River are better understood using data from autonomous PIT tag antennas. Canadian Journal of Fisheries and Aquatic Sciences 78: 1057–1072.
Fernández de Larrea, I., G. Sánchez-Montes, J. Gutiérrez-Rodríguez & Í. Martínez-Solano, 2021. Reconciling direct and indirect estimates of functional connectivity in a Mediterranean pond-breeding amphibian. Conservation Genetics 22: 455–463.
Ferner, J. W., 2010. Measuring and marking post-metamorphic amphibians. In Dodd, C. K. (ed), Amphibian Ecology and Conservation: A Handbook of Techniques. Oxford University Press, Oxford: 123–141.
Gibbons, J. W. & K. M. Andrews, 2004. PIT tagging: simple technology at its best. BioScience 54: 447–454.
Girard, I., C. Dussault, J. P. Ouellet, R. Courtois & A. Caron, 2006. Balancing number of locations with number of individuals in telemetry studies. Journal of Wildlife Management 70: 1249–1256.
Hamer, A. J. & M. J. Mahony, 2010. Rapid turnover in site occupancy of a pond-breeding frog demonstrates the need for landscape-level management. Wetlands 30: 287–299.
Hammond, T. T., M. J. Curtis, L. E. Jacobs, M. W. Tobler, R. R. Swaisgood & D. M. Shier, 2020. Behavior and detection method influence detection probability of a translocated, endangered amphibian. Animal Conservation 24: 401–411.
Hebblewhite, M. & D. T. Haydon, 2010. Distinguishing technology from biology: a critical review of the use of GPS telemetry data in ecology. Philosophical Transactions of the Royal Society B: Biological Sciences 365: 2303–2312.
Hill, M. S., G. B. Zydlewski, J. D. Zydlewski & J. M. Gasvoda, 2006. Development and evaluation of portable PIT tag detection units: PITpacks. Fisheries Research 77: 102–109.
Hulbak, M., E. M. Hanssen, R. J. Lennox, A. G. V. Salvanes, B. Barlaup, N. Gharbi, et al., 2021. Validating timing of salmon smolt runs obtained by telemetry studies. Fisheries Management and Ecology 28: 428–436.
Jehle, R. & W. Hödl, 1998. PITs versus patterns: effects of transponders on recapture rate and body condition of Danube crested newts (Triturus dobrogicus) and common spadefoot toads (Pelobates fuscus). Herpetological Journal 8: 181–186.
Joly, P., 2019. Behavior in a changing landscape: using movement ecology to inform the conservation of pond-breeding amphibians. Frontiers in Ecology and Evolution 7: 155.
Kassambara, A., M. Kosinski, P. Biecek & F. Scheipl, 2017. Package ‘survminer’: drawing Survival Curves using ‘ggplot2’. ’ggplot2’. R cran. Available at: https://cran.r-project.org/web/packages/survminer/survminer.pdf
Kelly, B. B., J. B. Cary, A. D. Smith, K. C. Pregler, S. Kim & Y. Kanno, 2017. Detection efficiency of a portable PIT antenna for two small-bodied fishes in a Piedmont stream. North American Journal of Fisheries Management 37: 1362–1369.
Kendall, W. L., K. H. Pollock & C. Brownie, 1995. A likelihood-based approach to capture-recapture estimation of demographic parameters under the robust design. Biometrics 51: 293–308.
Link, W. A., 2003. Nonidentifiability of population size from capture-recapture data with heterogeneous detection probabilities. Biometrics 59: 1123–1130.
Lucas, M. C. & E. Baras, 2000. Methods for studying spatial behaviour of freshwater fishes in the natural environment. Fish and Fisheries 1: 283–316.
Madison, D. M., V. R. Titus & V. S. Lamoureux, 2010. Movement patterns and radiotelemetry. In Dodd, C. K. (ed), Amphibian Ecology and Conservation: A Handbook of Techniques. Oxford University Press, Oxford: 185–202.
Ott, J. A. & D. E. Scott, 1999. Effects of toe-clipping and PIT-tagging on growth and survival in metamorphic Ambystoma opacum. Journal of Herpetology 33: 344–348.
Ousterhout, B. H. & R. D. Semlitsch, 2014. Measuring terrestrial movement behavior using passive integrated transponder (PIT) tags: effects of tag size on detection, movement, survival, and growth. Behavioral Ecology and Sociobiology 68: 343–350.
Pearson, K. N., W. L. Kendall, D. L. Winkelman & W. R. Persons, 2016. Tradeoffs 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 183: 263–274.
Perret, N. & P. Joly, 2002. Impacts of tattooing and PIT-tagging on survival and fecundity in the Alpine newt (Triturus alpestris). Herpetologica 58: 131–138.
Petit, E. & N. Valiere, 2006. Estimating population size with noninvasive capture-mark-recapture data. Conservation Biology 20: 1062–1073.
Pille, F., L. Pinto & M. Denoël, 2021. Predation pressure of invasive marsh frogs: a threat to native amphibians? Diversity 13: 595.
Pittman, S. E., M. S. Osbourn & R. D. Semlitsch, 2014. Movement ecology of amphibians: a missing component for understanding population declines. Biological Conservation 169: 44–53.
Pradel, R., 1996. Utilization of capture-mark-recapture for the study of recruitment and population growth rate. Biometrics 52: 703–709.
Prentice, E. F. & D. L. Park, 1983. A study to determine the biological feasibility of a new fish tagging system. Seattle: Coastal Zone and Estuarine Studies Division, Northwest and Alaska Fisheries Center, National Marine Fisheries Service, NOAA.
Renet, J., F. Guillaud, A. Xérès, J. Brichard, J. Baudat-Franceschi & G. Rosa, 2021. Assessing reliability of PIT-tagging in an endangered fossorial toad (Pelobates cultripes) and its effect on individual body mass. Herpetological Conservation and Biology 16: 584–593.
Roberts, C. M., 2006. Radio frequency identification (RFID). Computers & Security 25: 18–26.
Roberts, L. S., A. B. Feuka, E. Muths, B. M. Hardy & L. L. Bailey, 2021. Trade-offs in initial and long-term handling efficiency of PIT-tag and photographic identification methods. Ecological Indicators 130: 108110.
Roussel, J. M., A. Haro & R. A. Cunjak, 2000. Field test of a new method for tracking small fishes in shallow rivers using passive integrated transponder (PIT) technology. Canadian Journal of Fisheries and Aquatic Sciences 57: 1326–1329.
Ryan, K. J., J. D. Zydlewski & A. J. K. Calhoun, 2014. Using passive integrated transponder (PIT) systems for terrestrial detection of blue-spotted salamanders (Ambystoma laterale) in situ. Herpetological Conservation and Biology 9: 97–105.
Ryan, K. J., A. J. K. Calhoun, B. C. Timm & J. D. Zydlewski, 2015. Monitoring eastern spadefoot (Scaphiopus holbrookii) response to weather with the use of a passive integrated transponder (PIT) system. Journal of Herpetology 49: 257–263.
Saboret, G., P. Dermond & J. Brodersen, 2021. Using PIT-tags and portable antennas for quantification of fish movement and survival in streams under different environmental conditions. Journal of Fish Biology 99: 581–595.
Schaub, M., O. Gimenez, B. R. Schmidt & R. Pradel, 2004. Estimating survival and temporary emigration in the multistate capture-recapture framework. Ecology 85: 2107–2113.
Schulte, U., D. Küsters & S. Steinfartz, 2007. A PIT tag based analysis of annual movement patterns of adult fire salamanders (Salamandra salamandra) in a Middle European habitat. Amphibia-Reptilia 28: 531–536.
Semlitsch, R. D., 2008. Differentiating migration and dispersal processes for pond-breeding amphibians. Journal of Wildlife Management 72: 260–267.
Sievert, C., 2020. Interactive web-based data visualization with R, plotly, and shiny. Chemical Rubber Company Press, Boca Raton.
Silvy, N. J., 2020. The Wildlife Techniques Manual: Volume 1: Research. Johns Hopkins University Press, Baltimore.
Sinsch, U., 1990. Migration and orientation in anuran amphibians. Ethology Ecology & Evolution 2: 65–79.
Sinsch, U., N. Oromi, C. Miaud, J. Denton & D. Sanuy, 2012. Connectivity of local amphibian populations: modelling the migratory capacity of radio-tracked natterjack toads. Animal Conservation 15: 388–396.
Sinsch, U., 2014. Movement ecology of amphibians: from individual migratory behaviour to spatially structured populations in heterogeneous landscapes. Canadian Journal of Zoology 92: 491–502.
Testud, G., A. Vergnes, P. Cordier, D. Labarraque & C. Miaud, 2019. Automatic detection of small PIT-tagged animals using wildlife crossings. Animal Biotelemetry 7: 1–9.
Therneau, T.M. & T. Lumley, 2014. Package ‘survival’. Survival analysis Published on CRAN 2: 119. Available at: https://CRAN.R-project.org/package=survival
Therneau, T.M. & M.T.M. Therneau, 2015. Package ‘coxme’. R package version 2.
Unglaub, B., H. Cayuela, B. R. Schmidt, K. Preißler, J. Glos & S. Steinfartz, 2021. Context-dependent dispersal determines relatedness and genetic structure in a patchy amphibian population. Molecular Ecology 30: 5009–5028.
Want, R., 2006. An introduction to RFID technology. IEEE Pervasive Computing 5: 25–33.
Williams, B. K., J. D. Nichols & M. J. Conroy, 2002. Analysis and Management of Animal Populations. Academic Press, San Diego.
Willson, J. D., C. T. Winne & B. D. Todd, 2011. Ecological and methodological factors affecting detectability and population estimation in elusive species. The Journal of Wildlife Management 75: 36–45.
Winandy, L. & M. Denoël, 2011. The use of visual and automatized behavioral markers to assess methodologies: a study case on PIT-tagging in the Alpine newt. Behavior Research Methods 43: 568–576.
Witmer, G. W., 2005. Wildlife population monitoring: some practical considerations. Wildlife Research 32: 259–263.
Zentner, D. L., S. L. Wolf, S. K. Brewer & D. E. Shoup, 2021. A review of factors affecting PIT tag detection using mobile arrays and use of mobile antennas to detect PIT-tagged suckers in a wadeable ozark stream. North American Journal of Fisheries Management 41: 697–710.
Acknowledgements
We thank L. Pinto, L. Lorrain, P. Levionnois, and L. Seger for their help in the field, the land owners and municipalities for allowing access to their ponds, U. Sinsch and an anonymous reviewer for their constructive comments, and Direction Régionale de l’Environnement, de l’Aménagement et du Logement (DREAL Hérault) for permitting the surveys. C. Duret benefited of an Erasmus Plus grant and M. Denoël is a Research Director of the Fonds de la Recherche Scientifique – FNRS.
Funding
This work was supported by a PDR Grant Number T.0070.19 of the Fonds de la Recherche Scientifique – FNRS.
Author information
Authors and Affiliations
Contributions
CD contributed to conceptualization, data curation, formal analysis, investigation, methodology, software, visualization, writing and preparation of original draft, and writing, reviewing, & editing of the manuscript. FP contributed to data curation, investigation, methodology, and writing, reviewing, & editing of the manuscript. MD contributed to conceptualization, funding acquisition, investigation, methodology, project administration, resources, supervision, validation, writing and preparation of original draft, and writing, reviewing, & editing of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest to declare.
Additional information
Handling editor: Margarita Patricia Florencio Díaz
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
Duret, C., Pille, F. & Denoël, M. Efficiency of aquatic PIT-tag telemetry, a powerful tool to improve monitoring and detection of marked individuals in pond environments. Hydrobiologia 849, 2609–2619 (2022). https://doi.org/10.1007/s10750-022-04888-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-022-04888-8