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Tagging of age-0 flatfish with acoustic transmitters: comparison of internal implantation versus external attachment

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Abstract

The selection of a suitable method for tagging fish with transmitters is essential to ensure the feasibility of telemetry studies. Here, using a micro-acoustic transmitter, we examined the effects of tagging methods such as external attachment and surgical implantation on tag retention, and growth and survival of hatchery-reared spotted halibut at the release size (ca. 8–10 cm in total length). Fish with surgical implantation showed higher survival and retention rates than those with external attachments. However, the tagging methods did not influence the growth of the tagged fish. These findings indicated that surgical implantation of acoustic transmitters can be applied to small-sized spotted halibut. Overall, the findings can enhance the study about post-release movement of hatchery-reared fish at the release size to manage and conserve flatfish stocks.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author upon reasonable request.

References

  • Bégout Anras ML, Covés D, Dutto G, Laffargue P, Lagardère F (2003) Tagging juvenile seabass and sole with telemetry transmitters: medium-term effects on growth. ICES J Mar Sci 60:1328–1334. https://doi.org/10.1016/S1054-3139(03)00135-8

    Article  Google Scholar 

  • Bridger CJ, Booth RK (2003) The effects of biotelemetry transmitter presence and attachment procedures on fish physiology and behavior. Rev Fish Sci 11:13–34. https://doi.org/10.1080/16226510390856510

    Article  Google Scholar 

  • Brunsdon EB, Daniels J, Hanke A, Carr J (2019) Tag retention and survival of Atlantic salmon (Salmo salar) smolts surgically implanted with dummy acoustic transmitters during the transition from fresh to salt water. ICES J Mar Sci 76:2471–2480. https://doi.org/10.1093/icesjms/fsz139

    Article  Google Scholar 

  • Clark TD, Furey NB, Rechisky EL, Gale MK, Jeffries KM, Porter AD, Casselman MT, Lotto AG, Patterson DA, Cooke SJ, Farrell AP, Welch DW, Hinch SG (2016) Tracking wild sockeye salmon smolts to the ocean reveals distinct regions of nocturnal movement and high mortality. Ecol Appl 26:959–978. https://doi.org/10.1890/15-0632

    Article  PubMed  Google Scholar 

  • Cooke SJ, Woodley CM, Brad Eppard MB, Brown RS, Nielsen JL (2011) Advancing the surgical implantation of electronic tags in fish: a gap analysis and research agenda based on a review of trends in intracoelomic tagging effects studies. Rev Fish Biol Fish 21:127–151. https://doi.org/10.1007/s11160-010-9193-3

    Article  Google Scholar 

  • Crook DA, Wedd D, Adair BJ, Mooney TJ, Harford AJ, Humphrey CL, Morrongiello JR, King AJ (2023) Evaluation and refinement of a fish movement model for a tropical Australian stream subject to mine contaminant egress. Environ Biol Fish 106:469–490. https://doi.org/10.1007/s10641-022-01381-y

    Article  Google Scholar 

  • Daniels HV, Watanabe WO (2010) Practical flatfish culture and stock enhancement. Wiley-Blackwell, Oxford

    Book  Google Scholar 

  • Daniels J, Sutton S, Webber D, Carr J (2019) Extent of predation bias present in migration survival and timing of Atlantic salmon smolt (Salmo salar) as suggested by a novel acoustic tag. Anim Biotelemetry 7:16. https://doi.org/10.1186/s40317-019-0178-2

    Article  Google Scholar 

  • Earl J, Fowler AJ, Ye Q, Dittmann S (2017) Complex movement patterns of greenback flounder (Rhombosolea tapirina) in the Murray River estuary and Coorong, Australia. J Sea Res 122:1–10. https://doi.org/10.1016/j.seares.2017.01.008

    Article  Google Scholar 

  • Fairchild EA, Howell WH (2004) Factors affecting the post-release survival of cultured juvenile Pseudopleuronectes americanus. J Fish Biol 65(Suppl a):69–87. https://doi.org/10.1111/j.0022-1112.2004.00529.x

    Article  Google Scholar 

  • Fairchild EA, Rennels N, Howell H (2009) Using telemetry to monitor movements and habitat use of cultured and wild juvenile winter flounder in a shallow estuary. In: Nielsen JL, Arrizabalaga H, Fragoso N, Hobday A, Lutcavage M, Sibert J (eds), Tagging and tracking of marine animals with electronic devices. Reviews: methods and technologies in fish biology and fisheries, vol. 9. Springer, Heidelberg, Germany, pp 5–22. https://doi.org/10.1007/978-1-4020-9640-2_1

  • Fujita N, Ito H, Oikawa H (2005) Marking methods of spotted halibut Verasper variegatus. Miyagi Pref Rep Fish Sci 5:43–45 (in Japanese)

    Google Scholar 

  • Furey NB, Dance MA, Rooker JR (2013) Fine-scale movements and habitat use of juvenile southern flounder Paralichthys lethostigma in an estuarine seascape. J Fish Biol 82:1469–1483. https://doi.org/10.1111/jfb.12074

    Article  CAS  PubMed  Google Scholar 

  • Gibson AJF, Halfyard EA, Bradford RG, Stokesbury MJW, Redden AM (2015) Effects of predation on telemetry-based survival estimates: insights from a study on endangered Atlantic salmon smolts. Can J Fish Aquat Sci 72:728–741. https://doi.org/10.1139/cjfas-2014-0245

    Article  Google Scholar 

  • Halfyard EA, Webber D, Del Papa J, Leadley T, Kessel ST, Colborne SF, Fisk AT (2017) Evaluation of an acoustic telemetry transmitter designed to identify predation events. Methods Ecol Evol 8:1063–1071. https://doi.org/10.1111/2041-210X.12726

    Article  Google Scholar 

  • Hanssen EM, Vollset KW, Salvanes AGV, Barlaup B, Whoriskey K, Isaksen TE, Normann ES, Hulbak M, Lennox RJ (2022) Acoustic telemetry predation sensors reveal the tribulations of Atlantic salmon (Salmo salar) smolts migrating through lakes. Ecol Freshw Fish 31:424–437. https://doi.org/10.1111/eff.12641

    Article  Google Scholar 

  • Herrera M, Rodiles A, Salamanca N, Navas JI, Cordero ML, Hachero I (2023) First releases of hatchery-produced Senegal sole (Solea senegalensis), brill (Scophthalmus rhombus), and wedge sole (Dicologoglossa cuneata) juveniles in the South-Western Spanish coast. Hydrobiologia 850:203–214. https://doi.org/10.1007/s10750-022-05054-w

    Article  CAS  Google Scholar 

  • Klinard NV, Matley JK (2020) Living until proven dead: addressing mortality in acoustic telemetry research. Rev Fish Biol Fish 30:485–499. https://doi.org/10.1007/s11160-020-09613-z

    Article  Google Scholar 

  • Larocque SM, Johnson TB, Fisk AT (2020) Survival and migration patterns of naturally and hatchery-reared Atlantic salmon (Salmo salar) smolts in a Lake Ontario tributary using acoustic telemetry. Freshw Biol 65:835–848. https://doi.org/10.1111/fwb.13467

    Article  Google Scholar 

  • Le Pichon C, Trancart T, Lambert P, Daverat F, Rochard E (2014) Summer habitat use and movements of late juvenile European flounder (Platichthys flesus) in tidal freshwaters: results from an acoustic telemetry study. J Exp Mar Biol Ecol 461:441–448. https://doi.org/10.1016/j.jembe.2014.09.015

    Article  Google Scholar 

  • Lennox RJ, Nilsen CI, Nash A, Hanssen EM, Johannesen HL, Berhe S, Barlaup B, Wiik Vollset KW (2021) Laboratory and field experimental validation of two different predation sensors for instrumenting acoustic transmitters in fisheries research. Fisheries 46:565–573. https://doi.org/10.1002/fsh.10669

    Article  Google Scholar 

  • Liss SA, Znotinas KR, Blackburn SE, Fischer ES, Hughes JS, Harnish RA, Li H, Deng ZD (2021) From 95 to 59 millimetres: a new active acoustic tag size guideline for salmon. Can J Fish Aquat Sci 78:943–957. https://doi.org/10.1139/cjfas-2020-0222

    Article  CAS  Google Scholar 

  • Loher T, Rensmeyer R (2011) Physiological responses of Pacific halibut, Hippoglossus stenolepis, to intracoelomic implantation of electronic archival tags, with a review of tag implantation techniques employed in flatfishes. Rev Fish Biol Fish 21:97–115. https://doi.org/10.1007/s11160-010-9192-4

    Article  Google Scholar 

  • Matley JK, Klinard NV, Barbosa Martins APB, Aarestrup K, Aspillaga E, Cooke SJ, Cowley PD, Heupel MR, Lowe CG, Lowerre-Barbieri SK, Mitamura H, Moore JS, Simpfendorfer CA, Stokesbury MJW, Taylor MD, Thorstad EB, Vandergoot CS, Fisk AT (2022) Global trends in aquatic animal tracking with acoustic telemetry. Trends Ecol Evol 37:79–94. https://doi.org/10.1016/j.tree.2021.09.001

    Article  PubMed  Google Scholar 

  • Melnychuk MC, Christensen V, Walters CJ (2013) Meso-scale movement and mortality patterns of juvenile coho salmon and steelhead trout migrating through a coastal fjord. Environ Biol Fish 96:325–339. https://doi.org/10.1007/s10641-012-9976-6

    Article  Google Scholar 

  • Mitamura H, Arai N, Hori M, Uchida K, Kajiyama M, Ishii M (2020) Occurrence of a temperate coastal flatfish, the marbled flounder Pseudopleuronectes yokohamae, at high water temperatures in a shallow bay in summer detected by acoustic telemetry. Fish Sci 86:77–85. https://doi.org/10.1007/s12562-019-01384-2

    Article  CAS  Google Scholar 

  • Mitamura H, Mitsunaga Y, Arai N, Viputhanumas T (2006) Comparison of two methods of attaching telemetry transmitters to the Mekong giant catfish, Pangasianodon gigas. Zool Sci 23:235–238. https://doi.org/10.2108/zsj.23.235

    Article  Google Scholar 

  • Mitamura H, Mitsunaga Y, Arai N, Yamagishi Y, Khachaphichat M, Viputhanumas T (2008) Horizontal and vertical movement of Mekong giant catfish Pangasianodon gigas measured using acoustic telemetry in Mae Peum Reservoir, Thailand. Fish Sci 74:787–795. https://doi.org/10.1111/j.1444-2906.2008.01590.x

    Article  CAS  Google Scholar 

  • Mitamura H, Thorstad EB, Uglem I, Bjørn PA, Økland F, Næsje TF, Dempster T, Arai N (2012) Movements of lumpsucker females in a northern Norwegian fjord during the spawning season. Environ Biol Fish 93:475–481. https://doi.org/10.1007/s10641-011-9942-8

    Article  Google Scholar 

  • Munroe TA (2015) Systematic diversity of the Pleuronectiformes. In: Gibson RN, Nash RDM, Geffen AJ, Van der Veer HW (eds) Flatfishes: biology and exploitation, 2nd edn. Wiley-Blackwell, Oxford, pp 13–51

    Google Scholar 

  • Munroe TA (2015) Tropical flatfish fisheries. In: Gibson RN, Nash RDM, Geffen AJ, Van der Veer HW (eds) Flatfishes: biology and exploitation, 2nd edn. Wiley-Blackwell, Oxford, pp 418–460

    Google Scholar 

  • Neely BC, Koch JD, Kramer NW (2021) A review of marking and tagging methods for blue catfish, channel catfish, and flathead catfish. North Am J Fish Manage 41:S415–S427. https://doi.org/10.1002/nafm.10612

    Article  Google Scholar 

  • Neves V, Silva D, Martinho F, Antunes C, Ramos S, Freitas V (2018) Assessing the effects of internal and external acoustic tagging methods on European flounder Platichthys flesus. Fish Res 206:202–208. https://doi.org/10.1016/j.fishres.2018.05.015

    Article  Google Scholar 

  • Noda T, Wada T, Mitamura H, Kume M, Komaki T, Fujita T, Sato T, Narita K, Yamada M, Matsumoto A, Hori T, Takagi J, Kutzer A, Arai N, Yamashita Y (2021) Migration, residency and habitat utilisation by wild and cultured Japanese eels (Anguilla japonica) in a shallow brackish lagoon and inflowing rivers using acoustic telemetry. J Fish Biol 98:507–525. https://doi.org/10.1111/jfb.14595

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2022) R: a language and environment for statistical computing. http://www.r-project.org/. Accessed Oct 30, 2022. Foundation for Statistical Computing, Vienna

  • Scheffel TK, Hightower JE, Buckel JA, Krause JR, Scharf FS (2020) Coupling acoustic tracking with conventional tag returns to estimate mortality for a coastal flatfish with high rates of emigration. Can J Fish Aquat Sci 77:1–22. https://doi.org/10.1139/cjfas-2018-0174

    Article  Google Scholar 

  • Sekino M, Saitoh K, Shimizu D, Wada T, Kamiyama K, Gambe S, Chen S, Aritaki M (2011) Genetic structure in species with shallow evolutionary lineages: a case study of the rare flatfish Verasper variegatus. Conserv Genet 12:139–159. https://doi.org/10.1007/s10592-010-0128-2

    Article  Google Scholar 

  • Serafy JE, Ault JS, Capo TR, Schultz DR (1999) Red drum, Sciaenops ocellatus L., stock enhancement in Biscayne Bay, FL, USA: assessment of releasing unmarked early juveniles. Aquac Res 30:737–750. https://doi.org/10.1046/j.1365-2109.1999.00390.x

    Article  Google Scholar 

  • Shimizu D, Fujinami Y, Aono H (2013) Effectiveness of punching as a new method of marking for juvenile spotted halibut Verasper variegatus based on the small regenerated scales on the ocular side. Nippon Suisan Gakkai-shi 79:394–399. https://doi.org/10.2331/suisan.79.394

    Article  Google Scholar 

  • Szedlmayer ST, Able KW (1993) Ultrasonic telemetry of age-0 summer flounder, Paralichthys dentatus, movements in a southern New Jersey estuary. Copeia 1993:728–736. https://doi.org/10.2307/1447234

    Article  Google Scholar 

  • Therneau T (2023) A package for survival analysis in R. R package version 3.4.0. https://CRAN.R-project.org/package=survival. Accessed 30 Aug 2023

  • Tominaga O, Watanabe Y (1998) Geographical dispersal and optimum release size of hatchery-reared Japanese flounder Paralichthys olivaceus released in Ishikari Bay, Hokkaido, Japan. J Sea Res 40:73–81. https://doi.org/10.1016/S1385-1101(98)00011-2

    Article  Google Scholar 

  • Tomiyama T, Ebe K, Kawata G, Fujii T (2009) Post-release predation on hatchery-reared Japanese flounder Paralichthys olivaceus in the coast of Fukushima, Japan. J Fish Biol 75:2629–2641. https://doi.org/10.1111/j.1095-8649.2009.02456.x

    Article  CAS  PubMed  Google Scholar 

  • Tsitrin E, McLean MF, Gibson AJF, Hardie DC, Stokesbury MJW (2020) Feasibility of using surgical implantation methods for acoustically tagging alewife (Alosa pseudoharengus) with V5 acoustic transmitters. PLOS ONE 15:e0241118. https://doi.org/10.1371/journal.pone.0241118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wada T, Kamiyama K, Mitamura H, Arai N (2017) Horizontal movement and emigration of juvenile spotted halibut Verasper variegatus released in a shallow brackish lagoon: Matsukawa-ura, northeastern Japan, revealed by acoustic telemetry. Fish Sci 83:573–585. https://doi.org/10.1007/s12562-017-1099-8

    Article  CAS  Google Scholar 

  • Wada T, Kamiyama K, Shimamura S, Matsumoto I, Mizuno T, Nemoto Y (2011) Habitat utilization, feeding, and growth of wild spotted halibut Verasper variegatus in a shallow brackish lagoon: Matsukawa-ura, northeastern Japan. Fish Sci 77:785–793. https://doi.org/10.1007/s12562-011-0385-0

    Article  CAS  Google Scholar 

  • Wada T, Kamiyama K, Shimamura S, Mizuno T, Nemoto Y (2012) Effectiveness of stock enhancement of a rare species, spotted halibut Verasper variegatus, in Fukushima, Japan. Aquaculture 364–365:230–239. https://doi.org/10.1016/j.aquaculture.2012.08.030

    Article  Google Scholar 

  • Wada T, Kamiyama K, Shimamura S, Murakami O, Misaka T, Sasaki M, Kayaba T (2014a) Fishery characteristics of barfin flounder Verasper moseri in southern Tohoku, the major spawning ground, after the start of large-scale stock enhancement in Hokkaido, Japan. Fish Sci 80:1169–1179. https://doi.org/10.1007/s12562-014-0803-1

    Article  CAS  Google Scholar 

  • Wada T, Shimamura S, Nemoto Y (2014b) Feeding, growth, and dispersal of hatchery-reared spotted halibut Verasper variegatus released in a shallow brackish lagoon: Matsukawa-ura, northeastern Fukushima, Japan. Aquac Sci 62:75–88. https://doi.org/10.11233/aquaculturesci.62.75

  • Wada T, Yamada T, Shimizu D, Aritaki M, Sudo H, Yamashita Y, Tanaka M (2010) Successful stocking of a depleted species, spotted halibut Verasper variegatus in Miyako Bay, Japan: evaluation from post-release surveys and landings. Mar Ecol Progr Ser 407:243–255. https://doi.org/10.3354/meps08553

    Article  Google Scholar 

  • Walsh S, Díaz de Astarloa JM, Poos JJ (2015) Atlantic flatfish fisheries. In: Gibson RN, Nash RDM, Geffen AJ, Van der Veer HW (eds) Flatfishes: biology and exploitation, 2nd edn. Wiley-Blackwell, Oxford, pp 346–394

    Google Scholar 

  • Weinz AA, Matley JK, Klinard NV, Fisk AT, Colborne SF (2020) Identification of predation events in wild fish using novel acoustic transmitters. Anim Biotelemetry 8:28. https://doi.org/10.1186/s40317-020-00215-x

    Article  Google Scholar 

  • Wilderbuer T, Leaman B, Zhang CI (2015) Pacific flatfish fisheries. In: Gibson RN, Nash RDM, Geffen AJ, Van der Veer HW (eds) Flatfishes: biology and exploitation, 2nd edn. Wiley-Blackwell, Oxford, pp 395–417

    Google Scholar 

  • Winter ER, Hindes AM, Lane S, Britton JR (2020) Predicting the factors influencing the inter- and intraspecific survival rates of riverine fishes implanted with acoustic transmitters. J Fish Biol 97:1209–1219. https://doi.org/10.1111/jfb.14504

    Article  PubMed  Google Scholar 

  • Yamamoto S, Mitamura H, Obitsu N, Sato M (2021) Residence and movement patterns of the marbled flounder Pseudopleuronectes yokohamae around a spawning ground in southern Suo Nada, Seto Inland Sea, Japan. Fish Sci 87:161–171. https://doi.org/10.1007/s12562-020-01482-6

    Article  CAS  Google Scholar 

  • Yamashita Y, Aritaki M (2010) Stock enhancement of Japanese flounder in Japan enhancement programmes. In: Daniels HV, Watanabe WO (eds) Practical flatfish culture and stock enhancement. Wiley-Blackwell, Oxford, pp 239–255

    Google Scholar 

  • Yamashita Y, Nagahora S, Yamada H, Kitagawa D (1994) Effects of release size on survival and growth of Japanese flounder Paralichthys olivaceus in coastal waters off Iwate Prefecture, northeastern Japan. Mar Ecol Prog Ser 105:269–276. https://doi.org/10.3354/meps105269

    Article  Google Scholar 

  • Yamashita Y, Yamada H (1999) Release strategy for Japanese flounder fry in stock enhancement programmes. In: Howell BR, Moksness E, Svåsand T (eds) Stock enhancement and sea ranching. Blackwell Publishing, Oxford, pp 191–204

    Google Scholar 

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Acknowledgements

We thank Kotaro Ichikawa, Yushi Arai, Nanami Hashizoe, Takumi Honda, and Hare Nishida for assistance with fish measurements. We also thank the staff of the Fukushima Prefectural Research Institute of Fisheries Resource for rearing specimens. This study was conducted under an Advanced Technology Deployment Project for Agriculture, Forestry, and Fisheries (Research ID 21453627), supported by the Ministry of Agriculture, Forestry, and Fisheries of Japan.

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  1. Manabu Kume and Junichi Takagi contributed equally to this work.

Authors and Affiliations

  1. Field Science Education and Research Center, Kyoto University, Kitashirakawa-Oiwake, Sakyo, Kyoto, Kyoto, 606-8502, Japan

    Manabu Kume, Yoh Yamashita & Hiromichi Mitamura

  2. School of Platforms, Kyoto University, Yoshida-honmachi, Sakyo, Kyoto, Kyoto, 606-8501, Japan

    Junichi Takagi

  3. Graduate School of Agriculture, Kyoto University, Kitashirakawa-Oiwake, Sakyo, Kyoto, Kyoto, 606-8502, Japan

    Junichi Takagi, Yurika Dantsuji & Hiromichi Mitamura

  4. Institute of Environmental Radioactivity, Fukushima University, Kanayagawa 1, Fukushima, Fukushima, 960-1296, Japan

    Toshihiro Wada

  5. Fukushima Prefectural Research Institute of Fisheries Resource, Koyo 1-1-14, Soma, Fukushima, 976-0005, Japan

    Takayuki Ito

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  1. Manabu Kume
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Correspondence to Manabu Kume.

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Kume, M., Takagi, J., Dantsuji, Y. et al. Tagging of age-0 flatfish with acoustic transmitters: comparison of internal implantation versus external attachment. Environ Biol Fish 106, 2011–2019 (2023). https://doi.org/10.1007/s10641-023-01481-3

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