(PDF) Jepsen, N., Thorstad, E.B., Havn, T. & Lucas, M.C. (2015) The use of external electronic tags on fish: an evaluation of tag retention and tagging effects. Animal Biotelemetry 3:49 DOI 10.1186/s40317-015-0086-z.

External tagging of fish with electronic tags has been used for decades for a wide range of marine and freshwater species. In the early years of fish telemetry research, it was the most commonly used attachment method, but later internal implants became preferred. Recently, the number of telemetry studies using external tagging has increased, especially with the development of archival tags (data storage tags, DSTs), pop-up satellite archival tags (PSATs) and other environment-sensing tags. Scientific evaluations of the tagging method are rather scarce for most species. We identified 89 publications, reporting effects of external tagging for 80 different fish species, which constitute the main basis for this review. External attachment holds certain benefits compared to other tagging methods, for example, speed of application, and it may be the only option for fishes with a body shape unsuitable for surgical implantation, or when using tags with sensors recording the external environment. The most commonly reported problems with external tags are tissue damage, premature tag loss, and decreased swimming capacity, but the effects are highly context dependent and species specific. Reduced growth and survival have also been recorded, but direct mortality caused by external tagging seems rare. Most of the studies reviewed evaluate tag retention, survival, and tissue reactions. There is a general need for more research on the effects of external tagging of fish with electronic tags, but particularly there are few studies on predation risk, social interactions, and studies distinguishing capture and handling effects from tagging effects. For PSATs, especially those that are large relative to fish size, there are particular problems with a high proportion of premature tag losses, reduced swimming capacity, and likely increased predation, but there remains a paucity of tag effect studies related to the use of PSATs. Before embarking on a field study employing external tagging with electronic tags, we recommend the use of appropriate pilot studies, controlled where possible, to quantify potential impacts of tagging.

The use of external electronic tags on ish: an evaluation of tag retention and tagging efects Jepsen et al. Jepsen et al. Anim Biotelemetry (2015) 3:49 DOI 10.1186/s40317-015-0086-z Jepsen et al. Anim Biotelemetry (2015) 3:49 DOI 10.1186/s40317-015-0086-z Open Access REVIEW The use of external electronic tags on ish: an evaluation of tag retention and tagging efects Niels Jepsen1*, Eva B. Thorstad2, Torgeir Havn2 and Martyn C. Lucas3 Abstract External tagging of fish with electronic tags has been used for decades for a wide range of marine and freshwater species. In the early years of fish telemetry research, it was the most commonly used attachment method, but later internal implants became preferred. Recently, the number of telemetry studies using external tagging has increased, especially with the development of archival tags (data storage tags, DSTs), pop-up satellite archival tags (PSATs) and other environment-sensing tags. Scientific evaluations of the tagging method are rather scarce for most species. We identified 89 publications, reporting effects of external tagging for 80 different fish species, which constitute the main basis for this review. External attachment holds certain benefits compared to other tagging methods, for example, speed of application, and it may be the only option for fishes with a body shape unsuitable for surgical implantation, or when using tags with sensors recording the external environment. The most commonly reported problems with external tags are tissue damage, premature tag loss, and decreased swimming capacity, but the effects are highly context dependent and species specific. Reduced growth and survival have also been recorded, but direct mortality caused by external tagging seems rare. Most of the studies reviewed evaluate tag retention, survival, and tissue reactions. There is a general need for more research on the effects of external tagging of fish with electronic tags, but particularly there are few studies on predation risk, social interactions, and studies distinguishing capture and handling effects from tagging effects. For PSATs, especially those that are large relative to fish size, there are particular problems with a high proportion of premature tag losses, reduced swimming capacity, and likely increased predation, but there remains a paucity of tag effect studies related to the use of PSATs. Before embarking on a field study employing external tagging with electronic tags, we recommend the use of appropriate pilot studies, controlled where possible, to quantify potential impacts of tagging. Keywords: Telemetry, Tag attachment, Archival tag, PSAT, Survival, Tissue damage, Tag retention, Growth, Swimming, Drag, Entanglement, Biofouling, Predation Background More than four decades ago, Bruce Shepherd [1] wrote: “Although many researchers have looked in a cursory fashion at transmitter attachment and its efect on ish behavior, none have done so in detail. Results from a study of ish activity have convinced me of the need for careful examination of this problem”. his statement is *Correspondence: nj@aqua.dtu.dk 1 Section for Freshwater Fisheries and Ecology, Technical University of Denmark, 8600 Silkeborg, Denmark Full list of author information is available at the end of the article still valid. In general, the combined efect of capture, handling and tagging may change an animal’s behavior, and lead to lawed results in telemetry studies. Electronic tagging (referred to as telemetry and bio-logging) of free-ranging animals is widely used to study ish spatial ecology, survival, and responses to the environment [2–4]. he main methods for attaching electronic tags to ish are surgical implantation in the body cavity, gastric insertion, and external attachment [5, 6]. External attachment was the most common telemetry tag attachment method for ish studied in the irst two decades (1956– 1975) of application [2], but was overtaken in popularity © 2015 Jepsen et al. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Jepsen et al. Anim Biotelemetry (2015) 3:49 in the 1980s by surgical implantation in the body cavity, largely due to tag miniaturization and extended battery life [2]. While surgical implantation remains the most commonly used method for electronic tag attachment to ish [3], external attachment is widely used, especially, but certainly not only, with the increased use of archival (data storage tags, DSTs) and satellite tags [3], particularly popup satellite archival tags (PSATs, or PATs) [7]. While there are several review papers focusing on surgical implantation of tags and of their efects [8, 9], or wider comparison of tag attachment methodologies [5], there are relatively few studies on the efects of externally attached tags and no papers summarizing the experiences with, and evaluations of, external tagging of ish, across the breadth of taxa and habitats. Over 20 years ago, Baras [10] reviewed more than 1000 papers from studies using aquatic telemetry and found only 14 to evaluate the efects of external attachment of electronic tags on ish. In 2012, Drenner et al. [11], reviewed tagging studies of salmonids in marine environments and commented on the lack of evaluations of tagging/handling efects. A generic problem in such evaluations is to disentangle the various efects of capture, handling, tagging, holding, and transporting wild ish. When studies try to estimate the efect of tagging it is often the combination of efects that is measured. his makes it diicult to directly compare diferent tagging methods in terms of adverse efects and the critical reader should bear this in mind. In this paper, our aim is to summarize and evaluate experiences with external tagging of ish with electronic tags, based on published studies and the authors’ own experiences. We do not provide a comparison of the main tagging methods, which is available elsewhere [3–6]. Instead, we provide a detailed overview of the utility and problems associated with external attachment of electronic tags, with the aim of helping researchers to determine the suitability of this method for planned studies, and to be able to interpret data collected by using such methods and draw appropriate conclusions from the studies done. We also highlight key advantages and disadvantages of external tagging with electronic tags and suggest some important research areas that need to be addressed for the better evaluation of external tag efects. he following sections examine the important issue of tag retention and appraise evidence for the extent and nature of impacts of external tags on key attributes of ish health. he main sections cover tag retention and efects of tagging on swimming performance, growth, social interactions, and survival. Review Literature searches for this review were made through the homson Reuters Web of Science database and Page 3 of 23 ProQuest Biological Sciences database with diferent combinations of the key words: extern*, tag*, efect*, ish, telemetry, transmit*. In addition, the authors have undertaken research on tagging efects and performed tagging studies for many years, and their collections of scientiic literature were used, as well as searching through reference lists of previous publications. he aim was to cover publications on efects of external tagging as extensively as possible. hus, we identiied 89 publications describing various efects of externally attached electronic tags, ranging from detailed experimental evaluations to more descriptive, but in our opinion relevant, reports of observed efects. A body of literature exists reporting the efects of external conventional tags [e.g. 12], but here we focus only on externally attached electronic tags. Many of the same issues apply for attachment of conventional tags, but fundamental diferences are the larger size of electronic tags and that they usually, but not always, take longer to attach than conventional tags and often involve induction of general anesthesia as part of the tag attachment procedure [3, 6]. In the 89 papers (Table 1), information on 80 species, representing 20 orders is presented (Fig. 1), giving a total of 122 “species studies” (several papers cover multiple species). Of these, 45 % were carried out in marine/brackish environments and 55 % in freshwater. For marine/brackish environments, 38 % of the studies were wholly or partially conducted in controlled laboratory/mesocosm conditions, while in freshwater, this applied to 64 % of cases. Of 24 studies examining tag efects (including tag retention) on elasmobranchs, coelacanth, tarpon, tunas, and billishes, only three were under controlled conditions. Most of the publications concern tag retention (44), survival (38), tissue reaction to tag presence (31), general behavior (27), swimming performance (21), growth (17), and feeding (17). Few papers reported efects regarding physiology (6), predation (5), catchability (3), and social interactions (3) (Fig. 2). A variety of attachment methods have been used for external tags (Table 2) often optimized/tailored for the species and study in question, and reined over time. Early studies often used external attachment methods based on easily available materials, including ish hooks [13], alligator clips [14] and pull ties [15], and included descriptive evaluation of the most efective tagging methods and body locations under semi-controlled conditions, but without detailed evaluation of efects by comparison to controls [16]. his lack of detailed studies was also because early electronic tags were short-lived and so only the most obvious acute impact efects were considered. For fusiform and laterally compressed species, electronic tags are often ixed with steel wires or nylon ilaments through the muscle at the base of the dorsal in (Fig. 3), Species Buoyancy General behaviour/ activity Sea lamprey (Petromyzon marinus) × Catch- Migraability tion Equilib- Feeding Growth rium Infections, PhysiPredawounds, ological tion tissue efects reactions, healing Repro- Response Retention/ Social Survival Swimming Referduction to transmit-expulsion interacperformance ences ter output tions [99] × Basking shark (Cetorhinus maximus) × [17] Basking shark (Cetorhinus maximus) × [58] Bigeye thresher shark (Alopias superciliosus) × × [7] Great white shark (Carcharodon carcharias) × × [7] Shortfin mako shark (Isurus oxyrinchus) × × [7] Blacktip reef shark (Carcharhinus melanopterus) × Blue shark (Prionace glauca) × [100] [7] × Lemon shark (Negaprion brevirostris) × Oceanic whitetip shark (Carcharhinus longimanus) [73] × × [7] × × [7] School shark (Galeorhinus galeus) × [101] Silky shark (Carcharhinus falciformis) Cownose ray (Rhinoptera bonasus) Cownose ray (Rhinoptera bonasus) × × [102] × [55] Cowtail stingray (Pastinachus atrus) × [100] Porcupine ray (Urogymnus asperrimus) × [100] Southern stingray (Dasyatis americana) West Indian ocean coelacanth (Latimeria chalumnae) [103] × [59] Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus) × [29] Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus) × [104] × [31] × × × Page 4 of 23 × Lake sturgeon (Acipenser fulvescens) Jepsen et al. Anim Biotelemetry (2015) 3:49 Table 1 Summary table of studies that incorporate an evaluation of one or more efects of external tagging Species Buoyancy General behaviour/ activity Catch- Migraability tion Equilib- Feeding Growth rium Lake sturgeon (Acienser fulvescens) Infections, PhysiPredawounds, ological tion tissue efects reactions, healing × Survival Swimming ReferRepro- Response Retention/ Social performance ences duction to transmit-expulsion interactions ter output × Shortnose sturgeon (Acipenser brevirostrum) [32] × [29] × Shortnose sturgeon (Acipenser brevirostrum) × White sturgeon (Acipenser transmontanus) Tarpon (Megalops atlanticus) American eel (Anguilla rostrata) × × American eel (Anguilla rostrata) × × × × × × × × × [30] × [33] × [38] [7] [91] × European eel (Anguilla anguilla) × European eel (Anguilla anguilla) × European eel (Anguilla anguilla) × × × × × Longfin eel (Anguilla dieffenbachia) × Common carp (Cyprinus carpio) × × × × × × × Tigerfish (Hydrocynus vittatus) Mekong giant catfish (Pangasianodon gigas) × Chinook salmon (Oncorhynchus tshawytscha) [85] × [106] × × × [34] × × [36] × [81] × × × [40] × × × [41] × × × [23] × × × × × [72] × [67] Page 5 of 23 Chinook salmon (Oncorhynchus tshawytscha) Chinook salmon (Oncorhynchus tshawytscha) [82] [77] × Chinook salmon (Oncorhynchus tshawytscha) Chinook salmon (Oncorhynchus tshawytscha) × × × Blue catfish (Ictalurus furcatus) Chinook salmon (Oncorhynchus tshawytscha) [105] × × × [78] × Common carp (Cyprinus carpio) Tench (Tinca tinca) [71] [75] × Common bream (Abramis brama) × Dace (Leuciscus leuciscus) [70] [54] × Barbel (Barbus barbus) [69] [19] × European eel (Anguilla anguilla) Jepsen et al. Anim Biotelemetry (2015) 3:49 Table 1 continued Species Buoyancy General behaviour/ activity Catch- Migraability tion Equilib- Feeding Growth rium Masu salmon (Oncorhynchus masou) Rainbow trout (Oncorhynchus mykiss) × Infections, PhysiPredawounds, ological tion tissue efects reactions, healing × Repro- Response Retention/ Social Survival Swimming Referduction to transmit-expulsion interacperformance ences ter output tions × × × × [68] [1] × Rainbow trout (Oncorhynchus mykiss) Rainbow trout (Oncorhynchus mykiss) × Atlantic salmon (Salmo salar) × × × [63] × [64] [74] × Atlantic salmon (Salmo salar) [107] × Atlantic salmon (Salmo salar) [108] × Atlantic salmon (Salmo salar) × [65] Atlantic salmon (Salmo salar) × [66] × [109] × [27] Atlantic salmon (Salmo salar) × × × Atlantic salmon (Salmo salar) × × × Atlantic salmon (Salmo salar) × × Brown trout (Salmo trutta) × Brown trout (Salmo trutta) × Brown trout (Salmo trutta) × × × [46] [110] × × × Brown trout (Salmo trutta) × Brown trout (Salmo trutta) × × [93] × × × × [93] × × × × × × × × Northern pike (Esox ucius) × Northern pike (Esox lucius) × × × [42] × [44] [113] × × [24] × [48] × × Eulachon (Thaleichthys pacificus) × × × × × × × × × [113] × [86] × [88] [50] × × × [62] Page 6 of 23 Opah (Lampris guttatus) Atlantic cod (Gadus morhua) [1] [25] × × Muskellunge (Esox masquinongy) Atlantic cod (Gadus morhua) [28] × × Inconnu (Stenodus nelma) Northern pike (Esox lucius) [26] × Cutthroat trout (Salmo clarki) Arctic char (Salvelinus alpinus) [111] [112] × × Brown trout (Salmo trutta) Lake whitefish (Coregonus clupeaformis) [76] × × Brown trout (Salmo trutta) Arctic char (Salvelinus alpinus) Jepsen et al. Anim Biotelemetry (2015) 3:49 Table 1 continued Species Buoyancy General behaviour/ activity Atlantic cod (Gadus morhua) × Equilib- Feeding Growth rium × Atlantic cod (Gadus morhua) Long-snouted seahorse (Hippocampus guttulatus) Catch- Migraability tion Infections, PhysiPredawounds, ological tion tissue efects reactions, healing Repro- Response Retention/ Social Survival Swimming Referduction to transmit-expulsion interacperformance ences ter output tions [114] × × × × [49] × [115] × European plaice (Pleuronectes platessa) × Sole (Solea solea) × × × × × [49] [53] × Copper rockfish (Sebastes caurinus) × × × × [116] Quillback rockfish (Sebastes maliger) × × × × [116] Bluegill (Lepomis macrochirus) × Largemouth bass (Micropterus salmoides) × Smallmouth bass (Micropterus dolmieui) × × Rock bass (Ambloplites rupestris) × × × × [80] [117] [117] × × European seabass (Dicentrarchus × labrax) × European sea bass (Dicentrarchus labrax) × × × × × × Yellow perch (Perca flavescens) × × Yellow perch (Perca flavescens) × × Yellow perch (Perca flavescens) × × × × [119] × × × [20] × [80] × × × × × × × [64] × × × [47] × × [43] × × [52] × × [43] × × [22] Page 7 of 23 Yellowfin bream (Acanthopagrus × australis) × [117] × × Mulloway (Argyrosomus japonicus) [53] × × × [16] [114] × Two-spined blackfish (Gadopsis bispinosus) Silver perch (Bidyanus bidyanus) × [118] White perch (Morone americana) Salema porgy (Sarpa salpa) [79] × Yellowtail (Seriola quinqueradiata) × River blackfish (Gadopsis marmoratus) [47] × × Rock bass (Ambloplites rupestris) × European seabass (Dicentrarchus labrax) Jepsen et al. Anim Biotelemetry (2015) 3:49 Table 1 continued Species Buoyancy General behaviour/ activity Golden perch (Macquaria ambigua) × Macquarie perch (Macquaria australasica) Catch- Migraability tion Equilib- Feeding Growth rium × Infections, PhysiPredawounds, ological tion tissue efects reactions, healing Repro- Response Retention/ Social Survival Swimming Referduction to transmit-expulsion interacperformance ences ter output tions × × × × [105] × [21] Pink happy (Sargochromis giardia) × [60] Three spot tilapia (Oreochromis andersonii) × [60] Monkeyface prickleback (Cebidi- × chthys violaceus) × Black cod (Paranotothenia angustata) × × Bigeye tuna (Thunnus obesus) × [120] × [121] × [122] × Bluefin tuna (Thunnus thynnus) Yellowfin tuna (Thunnus albacares) × × × × [7] [122] × Yellowfin tuna (Thunnus albacares) × [7] Swordfish (Xiphias gladius) × × [7] Black marlin (Istiompax indica) × × [7] Blue marlin (Makaira nigricans) × × [7] Striped marlin (Kajikia audax) × × [7] White marlin (Tetrapturus albidus) White marlin (Tetrapturus albidus) Jepsen et al. Anim Biotelemetry (2015) 3:49 Table 1 continued × × × [88] × [90] Ranked in taxonomic order Page 8 of 23 Jepsen et al. Anim Biotelemetry (2015) 3:49 Page 9 of 23 25 proportion of premature releases in many studies have been strong drivers for improved attachment reliability [7, 17]. 20 Tag retention Nu mb e r o f p u b lic a tio n s 30 15 10 5 Characiformes Coelacanthiformes Gasterosteiformes Elopiformes Lampriformes Petromyzontiformes Osmeriformes Scorpaeniformes Pleuronectiformes Siluriformes Esociformes Gadiformes Lamniformes Carcharhiniformes Myliobatiformes Acipenseriformes Anguilliforme s Cypriniforme s Sa lmoniforme s Pe rciforme s 0 Fig. 1 Number of publications on effects of externally attached electronic tags according to taxonomic order Nu mb e r o f p u b lic a tio n s 50 40 30 20 10 Response to transmitter output Reproduction Social interactions Predation Catchability Physiological effects Buoyancy Equilibrium Migration Growth Sw imming pe rforma nce Feeding Infe ctions, w ounds, tissue re a ctions, he a ling Ge ne ra l be ha viour / a ctivity Re te ntion / e x pulsion Survival 0 Fig. 2 Number of publications on various effects of externally attached electronic tags but many variations of this method are used. For tagging larger, marine ish, much development has recently been carried out to reine methods of pole- and spear gun-deployed dart attachments and tethers associated with PSATs. he high cost of these tags and the high Given the substantial cost of electronic tags, it is no surprise that studies have frequently evaluated rates and duration of tag retention, in some cases under laboratory or mesocosm conditions, but often under ield conditions. he use of laboratory or mesocosm environments enables easy recording of tag loss, but may not be representative of the natural conditions, particularly in terms of snagging and fouling risks, which may increase the loss rate of external tags under natural compared to laboratory conditions [e.g. 4, 11, 25]. In the ield, retention of electronic tags is most often demonstrated by recapture, which can be habitat- and sampling eiciency dependent. Alternatively, tag loss may be demonstrated by premature release and reporting of pop-up tags [7, 18, 19]. Double tagging, where a conventional tag or PIT tag is used in combination with the main telemetry tag, can provide estimates of tag retention for recaptured ish. A marked change in movement patterns (most commonly an absence of movement as most tags are heavier than water and sink to the bottom), depth or temperature, can be indicative of electronic tag loss, although it can also indicate mortality [3]. hus deinitive records of external electronic tag retention, gained from recapture or direct observation, are most easily recorded in shallow, accessible environments, notably freshwater and clear inshore, marine environments. he recent, rapid development and application of pop-up tags has encouraged greater attention to efective attachment methods due to the high proportion of premature (before the pre-set time) releases when the attachment fails [7, 19]. However, problems with retention of radio, acoustic, and data storage tags may be just as evident across many species in freshwater habitats. Broadhurst et al. [20] tagged wild two-spined blackish (Gadopsis bispinosus) with external transmitters and kept them in aquaria and found that all (100 %) of the tags were shed within 8 days after tagging. In contrast, they found no loss of external tags on Macquarie perch (Macquaria australasica) after 28 days in a similar study [21]. he two species were tagged the same way, but with very diferent results, demonstrating the importance of not uncritically transferring results from one species to others. For wild silver perch (Bidyanus bidyanus) equipped with external tags, more than 50 % of the ish had rejected their external tags within 146 days in tanks or sea-cages [22]. Corbett et al. [23] also reported 100 % tag loss during a 50-day laboratory experiment with adult Chinook salmon (Oncorhynchus tshawytscha). Jepsen et al. Anim Biotelemetry (2015) 3:49 Page 10 of 23 Table 2 Examples of the range of methods used to externally attach electronic tags to ish, several of which are suited to the speciic morphology or taxa involved Method Example taxon Reference Fishing hook at base of dorsal fin attached by nylon tether to transmitter Roccus chrysops white bass [13] Small fishing hook at base of dorsal fin, attached by stiff nylon tether to PIT tag (highly temporary, minimal handling) Alosa sapidissima American shad [97] Dorsal fin attachment using miniature alligator clip Oncorhynchus clarki cutthroat trout [14] Three nylon T-bar tags anchored on pterygiphores used to mount an H-shaped rubber saddle housing the transmitter Paranotothenia angustata black cod [121] Pop-up satellite transmitter on monofilament tether with medical grade nylon dart harpoon attached at base of dorsal fin (other studies have used stainless steel/titanium darts) Thunnus thynnus bluefin tuna [123] Steel dart attached to transmitter deployed by pneumatic gun; dart aimed at lateral surface of fish, posterior to second dorsal fin (no internal organs) Latimeria chalumnae coelacanth [59] Archival tag attached to a barbed nylon pin passed through pre-punched hole in dorsal fin and secured by female half of cattle ear tag Galeorhinus galeus school shark [101] Pull tie covered in soft tubing attached around caudal peduncle, tag attached to main pull tie Sciaenops ocellata red drum [15] Absorbable suture attachment through caudal peduncle, tag on one side, soft plate on other Esox lucius northern pike [24] Ventral attachment at base of anal fin Seriola quinqueradiata yellowtail [16] Ventral attachment in mid-section of abdomen Gadus morhua Atlantic cod [114] Pannier (dorsal saddle) attachment with tag and battery components on either side of the dorsal fin Salmo trutta brown trout [46] Side mount attachment on one side of dorsal musculature, below dorsal fin, with a flexible backing plate Oncorhynchus mykiss on the other side, wire/monofilament through muscle section rainbow trout [64] Side mount attachment with neoprene pad Leuciscus leuciscus dace [77] Side mount attachment with soft, spacing mounds Cyprinus carpio Common carp [105] Anterior-dorsal soft saddle attached superficially Esox lucius northern pike [95] Posterior dorso-lateral soft saddle harness attached through musculature Esox lucius northern pike [48] Flattened tag attached to inside of operculum using two lengths of monofilament, fastened outside with washer and crimp Cebidichthys violaceus [120] Tag attached to bony appendages on back of fish with polyfilament Dacron tether Phycodurus eques Leafy seadragon [124] Tag loss is not necessarily a negative outcome, because shedding of a tag that becomes snagged in such a way that it would immobilize the ish prevents sufering of the animal [24]. his may be achieved if, for example, weak links or absorbable sutures are used. However, it can be diicult to do this in such a way that premature tag losses do not occur before appropriate data have been gathered and while ensuring that such tag losses can be identiied. McCubbing et al. [25] used a single absorbable suture through the dorsal muscle to attach radio tags to pre-spawning adults of a threatened Arctic char (Salvelinus alpinus) population to ensure that tag attachment was temporary, but found in preliminary observations that upon release in the stream, ish sought refuge under boulders and most tags were rapidly shed. he premature shedding (determined by locating and recovering shed tags during mobile tracking) was reduced by releasing ish in the lake from which they had migrated, several hundred meters downstream, but still a 25 % (5/20 ish) tag loss occurred from within a few days after tagging. More conventional, and more invasive, dorsal musculature tag attachments (body-tight, by use of stainless steel wires) in salmonids such as adult Atlantic salmon (Salmo salar) and brown trout (Salmo trutta) in rivers have much higher retention rates [26–28] than those observed for char by McCubbing et al. [25]. Generally, external tag attachment in ishes using benthic habitats causes diiculties in achieving adequate Jepsen et al. Anim Biotelemetry (2015) 3:49 Fig. 3 Example of typical external transmitter placement on a fusiform-bodied fish (Atlantic salmon, Salmo salar). This radio tag has a flattened section that lies close to the body surface and is held in place by stainless steel wires through the musculature. Note that these tags have conspicuous return information, which is not problematic for adult salmon, but could be an issue for smaller fish that may be susceptible to increased predation risk tag retention. Tags must be attached snugly to the body to minimize the risk of entanglement/snagging, biofouling and to minimize drag. Several studies have reported problems with external tagging of sturgeon and catish species. Collins et al. [29] used external radio tagging on shortnose (Acipenser brevirostrum) and Atlantic (A. oxyrinchus) sturgeons in a ield study and found poor retention for both species. In a subsequent tank experiment, only one of 12 individuals retained the tag after 40 days [30]. hey judged external tagging unsuitable for these species. However, Sutton et al. [31] tested different attachment methods on juvenile lake sturgeon (A. fulvescens) kept in tanks and reported that heavier suture material decreased transmitter loss, but the retention was still poor (75 % loss after 26 days). A subsequent test of diferent shapes of external tags resulted in loss of over Page 11 of 23 30 % of the tags in juvenile lake sturgeon after 8 weeks [32]. In contrast, Counihan and Frost [33] tagged juvenile, hatchery-reared white sturgeon (A. transmontanus) using external tags (two tagging methods/locations) and observed no tag-loss during the short laboratory study (7–20 days). Like sturgeon, catishes are known to exhibit low tag retention [e.g. 34]. Bodine and Fleming [35] attempted an alternative tag attachment method for blue catish (Ictalurus furcatus) by using the skeletal structure (supraoccipital bone). In their 2-month laboratory/pond study, tag retention was 100 %, but in the subsequent ield study in a lake, tag retention was 40 % at 6 months and 19 % at 12 months. Mitamura et al. [36] attached dummy (acoustic) tags to the pectoral in of juveniles Mekong catish (Pangasianodon gigas) kept in a pond for 2 months. All tagged ish survived and were retrieved, but all had lost their tags. he reason why catish and sturgeon are shedding both internal and external tags at a higher rate than most other ishes remains to be understood, but generally they seem to have very active tissue reactions to foreign bodies [37]. Adult anguillid eels represent a particularly diicult group for achieving a high retention rate of external tags. his is not only because of their benthic habits (except during migrations in the open sea), but also because of their body shape and lexibility, enabling them to bite at tag attachments midway along the body, and facilitating tag shedding by ‘knotting’ their body or passing through narrow crevices. In a thorough laboratory study of the efects of tagging American eel (Anguilla rostrata), Cottril et al. [38] found poor retention (9 %) of external tags after a 12-week period. Most eels lost the tags within the irst 3–4 weeks after tagging. Furthermore, considerable tissue erosion was evident around the stainless steel wire holding the external tags in place, and major scarring on eels that shed tags was observed. However, in a similar study with smaller (18 × 7.3 mm) external tags, European eels, kept in a perforated tank in a river, showed 100 % retention after 30 days (M. Lowry, pers. comm.). Reduction of electronic tag size to a degree suitable for small ish includes reduction of battery size, and hence results in a short battery life. hus, since the life of small electronic tags is usually low (but see [39]), external tagging can be preferred due to lower acute health efects compared to surgical implantation, where a longer recovery period may be evident. In a ield study on Chinook salmon smolts, Brown et al. [40] observed 10 % tag loss 9–17 days after tagging, as well as a high proportion of tags that were loose or displaced. In another laboratory study on Chinook smolts, only 5 % of the ish lost the external tags within 2 weeks [41], but tearing and loosening of the sutures holding the tags were also observed. In lake whiteish (Coregonus clupeaformis), Bégout Anras Jepsen et al. Anim Biotelemetry (2015) 3:49 et al. [42] observed tag loss for 92 % of the ish within 20 days in tanks. Pursche et al. [43] observed 100 % retention of external miniature acoustic tags (5 days battery life) on mulloway (Argyrosomus japonicus) and yellowin bream (Acanthopagrus australis) kept in an aquarium, after a study period of 7 days. Brown and Eiler [44] externally tagged gravid female inconnu (Stenodus nelma) and found no evidence of tag loss or mortality in a 2-week ield tracking study. Some studies have sought to divide mass and volume between two elements of a tag on either side of the ish, attached in a pannier-mount, assuming that this should reduce disequilibrium, and especially in cases of high tag to body mass ratio [3, 45]. In general, use of this method [e.g. 46] is less frequent today due not only to technical advances in reducing tag size, but also because saddle type tags, straddling the dorsal surface, are often associated with reduced tag retention rates and because of greater tissue reaction efects (see below). In a laboratory-based comparison of single-side mounted and pannier type transmitters on bluegill (Lepomis macrochirus) and yellow perch (Perca lavescens), Weimer et al. [47] found that 40 % of the perch and 14 % of the bluegill held in tanks shed their pannier type tags within 40 days. None of the ish tagged with single-side mounts lost these. Herke and Moring [48] tested a novel “harnessixed-tag” to attach large radio-tags to pike (Esox lucius) and concluded that the method gave a high retention rate, but two of six ish shed their tags during the 115-day ield study. One pike was recaptured after 54 days with the tag still in place, but some abrasion and tissue tearing were evident. A variety of marine-based studies have used modiications of conventional tagging methods (Floy, T-bar, Carlin, Peterson disc, etc.), to attach acoustic tags and DSTs. A common method has been to attach a loose-hanging tether from the electronic tag to a wire saddle through the dorso-lateral musculature, secured by a Peterson disc on the other side, for species such as Atlantic cod (Gadus morhua) and plaice (Pleuronectes platessa) [49, 50] or through in musculature for thornback ray (Raja clavata) [51]. he purpose of the Peterson tag is to spread the tension and reduce cutting of the wire through the skin and muscle. Righton et al. [50] tagged Atlantic cod in the laboratory with external DSTs in this way and observed 100 % retention of tags over a 6-month period. Arnold and Holford [49] reported recaptures of a ‘signiicant proportion’ of plaice with acoustic tags (attached to Petersen discs with a loose tether) and cod from the North Sea that had lost acoustic tags, but did not quantify this. In a comparison of tagging methods for sea bream (Sarpa salpa) in experimental tanks, all ish with externally mounted acoustic transmitters retained their tag Page 12 of 23 over a 14-day period, but on all ish some abrasion, injuries, and fouling occurred [52]. In a study of the efects of tagging on growth of juvenile European seabass (Dicentrarchus labrax) and juvenile sole (Solea solea) in saltmarsh ponds, Bégout Anras et al. [53] observed a tagloss of 60 % after 47 days in sea bass, but reported 100 % retention of tags by sole during 72 days. When using PSATs, tag retention until the planned release date is a crucial element of experimental planning and has been diicult to achieve across a wide variety of taxa [7, 19, 54]. his is particularly so for migrating eels, which in the early stages of sea migration inhabit highly structured environments. PSAT tagging of longin eel (Anguilla diefenbachii) revealed a high rate of tag loss, with only three of 10 tags providing data [54]. Results from 275 silver European eel (A. anguilla) released on European coasts equipped with PSATs to study the ocean spawning migration indicated a large premature tag release [19]. his was partly related to mechanical tag loss, but also to a high predation rate (>20 % conirmed predation of eels with PSATs). he natural predation rate is unknown, so it is unclear to what extent the tag contributed to an increased predation risk. Mean time from tagging to premature tag release was 14–21 days (maximum 9 months). In a laboratory test of four different attachment methods for PSATs on European eel, Økland et al. [19] observed an overall tag retention after 6 months of 54 %. Retention varied from 0 to 100 % among the attachment methods, but the method that achieved no tag loss was regarded as less suitable because of a strong negative reaction (the tagged ish were struggling to try to shed the tag and did not swim normally) in the irst 2 days after tagging and showed consequent damage to the swimming musculature. PSAT attachment for inshore and demersal ish is most commonly achieved under sedation or anesthetization by harness attachment to the ish while in a tagging trough, in a manner similar to tagging with radio or acoustic transmitters. However, for large pelagic species, tagging with a pole-mounted dart placed at the base of the dorsal in, usually with the ish still in the water, is the most common method. Onboard tagging is routinely performed with large bluein tuna (hunnus thynnus) in Nova Scotia, with no apparent problems for the ish or tag retention (M. Stokesbury, pers. comm.). However, a meta-analysis demonstrated that onboard tagging did not improve tag retention for tunas and billishes, while for sharks it reduced tag retention duration [7] and suggests that unless landing is needed (e.g. for insertion of sensors), in situ tag attachment may be more efective. A wide range of dart heads and associated attachment elements have been designed and used to try to maximize retention. Musyl et al. [7] emphasized the importance of Jepsen et al. Anim Biotelemetry (2015) 3:49 a small entry wound to minimize tissue damage and aid healing. While ‘umbrella’ and ‘lopper’ dart head types, with retaining elements that open after dart entry, are often employed to improve retention, a meta-analysis demonstrated nylon tag heads to have lower retention characteristics than all other dart head designs [7]. Key factors likely contributing to PSAT loss in ield studies are the relatively high drag and buoyancy of these devices, causing local pressure at the attachment point [55], increased by biofouling [7, 18]. Biofouling has also been reported for standard telemetry tags [56]. Most PSAT tags in large, pelagic species are lost from tens to a few hundred days after attachment, while conventional tag losses in tunas, for example, are typically 2–5 % per year [57]. Witt et al. [58] reported high premature loss rates of PAT (pop-up archival transmitting) tags attached to basking shark (Cetorhinus maximus) at the base of the dorsal in. Eight of nine tags released prematurely, and four of these were lost after just 2 months. hey found that nine of 12 smaller PAT tags attached the same way were retained after 7 months. his supports a causal relationship between tag-size, drag, and tag loss in this species. As tag size continues to shrink with technological advances, this should give improved retention in most species when dart-head deployments of PSATs are used. In deep-water environments, darting may be more efective than other external tagging methods, since other methods than darting require the ish’s ascent to the surface for tagging. Shauer et al. [59] used in situ darting to tag 11 coelacanths (Latimeria chalumnae) with large (30 g) transmitters. Despite the hard ganoid scales of the coelacanth, the dart was shot into the ish using a pneumatic gun from a manned submersible. Tracking records demonstrated that the tags stayed in place for “at least 3–4 weeks”. After a period, the tags eventually came of and apparently caused minimal harm to the ish. As evident from the above-referred studies, tag retention is a major problem in many studies using external tagging. Even for short-term studies this problem can occur. It can be diicult to mount a tag so that it stays in place without injuring the ish or resulting in premature tag-loss. External tagging is particularly problematic for ish that live in close contact with sediment, vegetation or that take shelter in hard structures (roots, woody debris, rocks or crevices). In general, the best success with external tagging has been with large, robust freeswimming ish like adult Atlantic salmon, brown trout; large, open-ocean ishes, or bottom dwelling latishes that live on lat sediments. Likewise, experience with external tags for large cichlids has been good [60, 61]. For fusiform and laterally compressed ishes tagged ex situ, a tag lattened on one side, mounted close to the body, below the dorsal in and aixed by wire or nylon Page 13 of 23 through the musculature, seems to be the best method, whereas most pannier-saddle-type mounts have been problematic. For many large marine pelagic and deepwater species, external tags may best be applied in situ by darting. Swimming performance Reduced swimming performance is one of the expected efects of attaching external tags to ish because of the additional drag exerted by the tag as the ish moves through the water. External tags will change the streamlined body shape that many ish species possess, disturb balance and, at worst, cause loss of equilibrium if the tag is too heavy compared to the mass of the ish. Predatory species that rely on speed to catch prey may be less successful and sufer reduced growth. For prey species dependent on escaping predators, the additional drag and weight of a tag (tag burden) may skew the balance between life and death. he most commonly used metric of tag burden is the ratio of tag mass to ish body mass in air, though for external tags it may not be the most relevant, since tag shape and volume strongly inluence drag imparted and may inluence swimming, especially at higher speeds, since drag increases as the square of velocity. For migrating species, changes in swimming performance may delay or reduce migration success. Such indirect efects of tagging are diicult to assess, but we identiied 21 studies that have used diferent methods to evaluate efects on swimming performance by externally tagged ish. In an early study, Shepherd [1] reported a swim trial where the oxygen consumption rate of externally tagged wild cutthroat trout (Salmo clarki) was compared with control ish. he study demonstrated a higher oxygen demand of tagged ish. A similar approach with small numbers of tagged and untagged cod showed a higher mass-speciic oxygen consumption rate of tagged ish during swimming, indicating that there is a measurable drag efect from the tag [62], as predicted by Arnold and Holford [49]. In a study of the efect of external tagging on juvenile rainbow trout (Oncorhynchus mykiss), Lewis and Muntz [63] used tail beat frequency, opercular beat rate, and drag measurements as indicators of swimming performance. All three indicators were elevated in tagged ish compared to controls, and a pannier-saddle-mounted tag, generating more drag than a single-side mount, caused a greater impact. Tests with a dorsal saddle-type tag on the same species showed that time to exhaustion was shorter for externally tagged ish than for surgically implanted and control ish [64]. he same test with white perch (Morone americana) showed large individual variation, but no diference was found between treatments [64]. Jepsen et al. Anim Biotelemetry (2015) 3:49 A common approach to determine tagging impacts on the swimming performance of ishes is to measure the critical swimming speed (Ucrit), which is based on incremental increases in water velocity, and hence swimming velocity, in a lume. Peake et al. [65] detected a diference in Ucrit between tagged and untagged wild Atlantic salmon smolts, both for surgically implanted and externally tagged ish. his diference was not found in hatchery ish. In a similar study of hatchery smolts, McCleave and Stred [66] found external tags to reduce the critical swimming speed in comparison with untagged control ish and intragastrically tagged ish. In a recent, comprehensive study by Janak et al. [67] on hatchery-reared Chinook smolts, the mean Ucrit for control ish was 11 and 22 % higher than the mean for ish tagged with small and large external transmitters, respectively. For juvenile masu salmon (Oncorhynchus masou), the Ucrit of externally tagged ish was lower than that of surgically implanted and sham-tagged (surgical procedure without a tag inserted) groups [68]. Externally tagged juvenile white sturgeon also exhibited lower Ucrit than control ish [33]. Cottril et al. [38] did not ind any diferences in swimming performance between American eels tagged with dummy acoustic tags (0.5 % tag/bm ratio) by external, surgically implanted, and gastric methods and untagged ish. However, for larger PSAT tags (2–3 % tag/bm), several studies have reported strong efects on swimming performance of eels, including up to three-fold increases in energy cost of transport [69–71]. Using spherical PSAT dummies of varying sizes, in a series of respirometry measurements and kinematic analyses, Tudorache et al. [71] suggested that the optimal location for single point attachment of PSAT tags is more anterior than at the middle of the body length in eels. For adult Atlantic salmon, horstad et al. [27] compared swimming endurance between ish with large external tags, small external tags, surgically implanted tags, and control ish, and found no diferences among groups in endurance, nor in values of plasma glucose, haematocrit and plasma chloride. In a ield evaluation, Gray and Haynes [72] compared rates of upstream movement of adult Chinook salmon tagged externally and with gastric implanted tags in a ield study in the Columbia River, and found no diference in upstream movements between the groups. Sundström and Gruber [73] attached large speed sensing tags to seven juvenile lemon sharks (Negaprion brevirostris) in the ield and observed “elevated swimming speed” during the irst 24 h after tagging, but after that “normal” behaviour was observed. In general, these studies document a measurable efect on oxygen demand and swimming performance from ishes carrying an external electronic tag. his efect is Page 14 of 23 most pronounced in relatively small ish, or when large buoyant tags have been applied, as in the case of PSATs and related devices. No marked efect was observed for adult Atlantic salmon and lemon sharks with closely attached traditional telemetry tags of less than 3 % tag mass to body mass ratio [72, 73]. Growth External tags may afect feeding and thus growth, because movement can be impaired by the presence of the tag. Furthermore, capture, handling, holding, and tagging may compromise the health of a ish, afecting the motivation and physical capability for feeding. External tags also involve additional mass and drag, which may result in increased energy expenditure and reduced growth, even if the ish is feeding normally. hus, growth integrates a range of efects into one measurable parameter, because reduced performance will likely result in a reduced growth. Growth rate can, therefore, be a good indicator of long-term efects by tagging and a useful metric of impact. Field experiments where a tagged ish must compete with untagged conspeciics for food and habitat provide the best test, but most evaluations of tag efects on growth are based on laboratory/mesocosm studies. he challenges of doing ield-based growth experiments on identiiable individual ish (from which individual growth rates can be measured) are signiicant and it is both costly and risky for data capture to move from laboratory to ield, thus limiting the number of studies. For hatchery-reared juvenile Atlantic salmon, Greenstreet and Morgan [74] observed a negative efect of dorsal saddle-type external tags on growth (in tanks) for all size classes, with the smallest ish losing weight during a 17-day period. Weimer et al. [47] found a similar negative efect on growth in yellow perch and bluegill in tanks carrying a saddle-type tag. hese species tagged with a single-side mounted external tag also showed reduced growth during the 40-day period, but the efect was less pronounced than for the ish with saddle-type tags [47]. A similar pattern was also observed in hatchery-reared juvenile Chinook salmon, tested for three tagging methods, with reduced growth evident after 2 weeks, and the most pronounced negative efect seen in the saddletagged group [41]. Tank-reared barbel (Barbus barbus) with side-mounted external dummy tags (2 % of body mass) lost an average of 10 % of their body mass in the 60 days post tagging, compared to controls that gained 2 % of body mass. Externally tagged barbel had a signiicantly lower growth rate than surgically tagged ish [75]. Externally tagged sub-adult farmed Atlantic salmon exhibited normal activity and feeding in tanks the day after intervention (unlike surgically implanted ish), but Jepsen et al. Anim Biotelemetry (2015) 3:49 after 6 weeks, their growth rate was still only half that of controls [76]. In a study of wild Atlantic cod, the use of externally attached data-storage tags was tested both in the laboratory and in a large ield experiment [49]. he laboratory results showed that growth of tagged cod did not differ from untagged control ish. In the ield experiment, growth of recaptured cod was compared to the growth of wild untagged cod and a slightly (but not signiicantly) lower growth rate (length) was observed for the tagged cod. Cottrill et al. [38] compared length and weight of European eels in a laboratory study (control, gastric, surgically implanted, external) 8–10 weeks after treatment and found no efect of tagging. Likewise, Økland et al. [19] found no diference in growth (weight loss) between tagged and untagged silver eels after 4 weeks. In the case of silver eel, growth is not a strong indicator of tagging efects because silver eels, like many other semelparous ish species, are known not to feed after they start their seaward migration. However, during migration, energy use and weight loss of eels with large external tags may be elevated due to increased drag. Beaumont et al. [77] observed externally tagged dace (Leuciscus leuciscus) in a glass-sided luviarium tank and compared the condition-factor (K) between tagged and untagged ish after a 10-week period, and no signiicant diference was recorded. As most studies using external tagging with electronic tags are relatively short-term, potential impacts on growth have not been of deep concern, but the studies above show negative efects on growth or body condition in Atlantic salmon juveniles, yellow perch, bluegill, and barbel, but not in cod, eel, and dace. he negative efect on growth was stronger for dorsal-mounted pannier-saddle-type tags than for single-sided tags. Social interactions Movement and habitat use is partly determined by social interactions in many ish species. Stress caused by capture, handling, and tagging may change aggression, position in dominance hierarchies, competition, parental care, shoaling, and other types of social behavior, and thus, lead to biased results in telemetry studies. Further, features such as bright colors, speciic color patterns, body size and shape, or size and shape of other morphological attributes (for instance adipose in size in reproductively mature male salmonids, degree of asymmetry) have evolved in many ishes through sexual selection either to increase attractiveness to the opposite sex or related to competition with rivals of the same sex, with the ultimate aim to maximize reproductive success. he presence of an external tag on a ish may, due to the size, shape or color of the tag, interfere with such signals. Page 15 of 23 External tags may also increase the visibility of the ish to such an extent that the predation risk is increased (see “Survival” section below). Such efects may be reduced by dying the tag to blend with ish color, thus camoulaging the tag [67]. Bright tag labels with return-information should be kept on the side of the tag towards the ish to reduce the visibility. Only a few studies have been carried out to evaluate the efects of external tagging on social interactions in ish (Fig. 2), and the existing studies have not revealed severe impacts. In a study of rainbow trout, dominance rank of individual ish only changed marginally after tagging [64]. Externally tagged dace were observed to integrate into a shoal after tagging [77]. When externally radio tagged bream (Abramis brama) were located and recaptured by seine netting, they were always part of a bream shoal, demonstrating that after tagging they had reintegrated [78]. Using ield observational methods, Cooke [79] found no evidence that externally attached radio transmitters afect parental care by rock bass (Ambloplites rupestris). Studies of social interactions may be more sensitive to subtle but chronic efects by external tagging than studies of other type tagging efects, but are diicult to carry out in a controlled way. here is clearly a need for more studies on social interactions. he lack of documented efects is not indicative of a lack of real efects, because the number of existing studies is so low. Survival Survival is not a suicient indicator of the suitability of a tagging method, but low survival is often a good indicator for a problematic method. In most telemetry studies, survival rates of externally tagged ish have been high, but with species, habitat, and methodological variations. hus, half of the studies where survival of externally tagged ish was reported found no increased mortality [compared to control ish (laboratory) or expected levels (ield)]. Mortalities reported in laboratory/mesocosm studies are rarely predation related, as relatively few such tests have been done (but see, for example, Ross and McCormick [80] who quantiied such efects), whereas, in the ield, mortalities represent a composite of disease, stress, physiological insult, and predation efects, but these impacts are often diicult to disentangle. In the laboratory, Greenstreet and Morgan [74] observed relatively high mortality of the smallest Atlantic salmon juveniles tagged with a “saddle-pack” dummy transmitter, but no mortality for larger individuals (18–20 cm). Tests of single-side and saddle type transmitters on wild bluegill and yellow perch, kept in tanks, showed up to 50 % mortality, mainly for perch, and highest with the saddle mounted tags [47]. Testing of an external attachment method, as an alternative to surgical implantation, Jepsen et al. Anim Biotelemetry (2015) 3:49 on wild blue catish kept in ponds, revealed mortality of 13 % over 6 months, possibly related to tagging. However, the authors also state that this may be attributed to elevated stress and subsequent infection associated with coninement in the hatchery pond [35]. Brown et al. [81] compared survival of externally tagged hatchery-reared Chinook salmon juveniles during simulated turbine passage (laboratory) and found no diference in mortality between tagged and control ish. A further (ield) comparison between surgically implanted (PIT-tags) and externally tagged hatchery-reared Chinook smolts during passage of hydropower stations and along river reaches showed that external tags were suitable for short-term migration studies, but not for longer periods than 10 days due to tag loss and mortality [40]. In masu salmon (Oncorhynchus masou) juveniles, kept in an outdoor tank, 83 % of externally tagged and 42 % of surgically implanted ish died within 68 days [68]. By contrast, Broadhurst et al. [21] found high mortality (and tag expulsion) in the surgically implanted group, but no mortality or tag loss in the externally tagged group in wild Macquarie perch kept in aquaria. he same result was found in a study of common carp (Cyprinus carpio), kept in concrete ponds in Africa, where all ish in the surgically implanted group died and all externally tagged ish survived [82]. Corbett et al. [23] compared external tagging with gastric implant for adult Chinook in a 50-day laboratory experiment. Only one of 10 externally tagged salmon died, whereas there was high mortality (19/20) of ish with gastric implants. In the ield, horstad et al. [28] found little mortality (1 out of 39 ish did not migrate upstream) in externally tagged sea trout (anadromous S. trutta). A similar outcome for this species was recorded by Økland et al. [26]. Likewise, in a lowland Danish river, Aarestrup and Jepsen [83] used externally attached radio tags to study wild sea-trout pre- and post-spawning movements. hey observed some mortality (<20 %) of tagged ish, but ascribed this to natural post-spawning mortality. Some tagged ish left the river after the spawning period, but 10 of 25 tagged ish were retrieved by electroishing with the tags still in place and only minor abrasions. No tag loss was observed [83]. Similar results were recorded for externally tagged Atlantic salmon in the same river [84]. However, in a similar study of sea trout spawning migration, in a smaller stream with abundant vegetation, the external tagging method had to be abandoned due to tag loss, mortality, and observation of wounds at the tag position, most likely caused by entanglement in vegetation (N. Jepsen, unpublished). By contrast, for externally tagged tench (Tinca tinca) in a weedy lake after 1 month at liberty, nine of 15 ish were recovered with tags [85]. While some of the tags in this study were shown to have loosened, the method was judged as Page 16 of 23 successful even with ish living in a weedy environment. he “tilt-tags” employed in this study also indicated that tench exhibited the head-down feeding behaviors expected [85], suggesting normal behavior. Low mortality levels have been reported for mulloway and yellowin bream externally tagged with miniature acoustic tags in controlled studies of short (7 days) duration [43]. However, over a longer timescale and for larger silver perch with external tags, elevated mortality occurred for tagged ish (40 %) compared to control ish (10 %) after 257 days, and all surviving ish had shed their tags [22]. Hanson and Ostrand [86] tested diferent electronic tagging methods on small anadromous eulachon (haleichthys paciicus) and found high mortality (50 %) after only 5 days, of all groups, including non-tagged control ish, indicating that this species is sensitive to capture, handling, and holding (in aquaria). For yellow perch tagged with externally attached transmitters, Ross and McCormick [80] found low survival (7 %) after 86 days in a pond with low oxygen levels in summer, compared to 82 % of control ish from the same pond, suggesting a chronic impact of external tagging, combined with poor water quality. In another experiment, they found that externally tagged yellow perch, in a small pond with good water quality and a small number of predatory northern pike, exhibited 41 % survival, compared to 94 % for controls [80]. Several tagged perch were found in pike stomachs at the end of the experiment, and the authors inferred diferent susceptibility to predation to be a key cause of mortality. In the case of PSATs, it is possible to identify mortality in pelagic species because a static depth record over several days is indicative of mortality, with the tagged ish lying on the bottom, as opposed to normal changes in depth through the water column. When released from the ish, PSATs will loat to the surface, due to their positive buoyancy. Most PSATs will automatically release in response to a preset time threshold at a stable depth (typically when on the bottom) and hence data can be used to determine mortality rates [87], but may be unreliable in some species, such as basking shark, which may spend protracted periods at a stable depth. Since mortality may also occur over deep-ocean areas, a failsafe release is deployed at a speciic depth to prevent pressure damage to the PSAT, which can also be used to estimate mortality rates [87]. Mortality through predation can be identiied on occasion, due to the tag’s light sensor recording darkness (in the predator’s gut) over an extended period, and thermistor and depth log information can help to identify the predator type (e.g. persistent elevated temperatures, with temperatures characteristic of endothermic tunas and sharks, or marine mammals) [88, 89]. While such mortality estimates are possible, they were not Jepsen et al. Anim Biotelemetry (2015) 3:49 included in Musyl et al.’s detailed meta-analytical study [7], perhaps because interpretation of mortality in such instances is an inexact science. Holland and Braun [17] identiied a discussion-based reticence to report mortalities, as this could jeopardize some PSAT-based research. We consider it likely that many PSAT-recorded mortalities of large oceanic ish [e.g. 87] relect capture and handling efects more than direct efect of tagging. Indeed, many of those studies are actually directed at assessing survival of released large pelagic species from unwanted by-catch in commercial operations [e.g. 87, 90]. As smaller ishes are being tagged with miniaturized PSATs, predation is increasingly likely (large carnivores eat smaller animals), but to distinguish the efects of natural mortality from the increase due to PSAT tagging is dificult. he high mortality rates of PSAT-tagged American eel [91], attributed most likely to predation by porbeagle shark (Lamna nasus), may have been facilitated at least in part by the relatively large and buoyant tag, perhaps making the eel more conspicuous than normal. Undoubtedly, migrating eels can provide reliable food sources for top predators, but identifying the additional efect of tagging with large, positively buoyant tags in such an environment is diicult. From the published studies, it appears that direct mortality caused by external tagging is usually low, but that tagging may be contributory. Particularly, when tagging ishes of relatively small size compared to the large buoyant PSAT tags, there seem to be an extra risk of mortality due to predation. Hence, one should be cautious to draw conclusions on natural mortality levels of relatively small ishes, and causes for this mortality, based on results from PSAT tagged ish. he combined efect of capture, handling, tagging, and holding ish for observation can cause signiicant mortality, and it is diicult to separate between the efects of the tag and tagging itself, and the efects of capture and handling. It is therefore important to include untagged control ish in studies, whenever possible (laboratory/tanks/ponds), or, for instance, by comparing with less invasive tagging methods like dyemarking, coded wire tagging, or PIT-tagging in ield studies. In general, it seems that external tagging of juvenile salmonids can be done, but the experiences are not as good as they are for the surgical implant or tag injection [39] techniques. Also perciforms (including Percidae, Teraponidae, Centrarchidae) can be vulnerable to external tagging, but here the results vary among species and studies. Overall, there is large variation in survival rates among studies. In few cases, increased mortality rate can be directly linked to the tagging procedure, but usually acute mortality is caused by the combined efect of being captured, held, handled, and/or carrying the tag, whereas the carrying of the tag is manifested principally Page 17 of 23 as a chronic efect on growth, though in some cases with increased incidence of mortality, linked to disease and/or predation. Discussion A vital element of telemetry studies is that the tag should not alter animal behavior or performance, and if it does, that the efect can be measured and accounted for and thus does not interfere with the conclusions of the study [3]. Based on the information covered in this review, it is clear that while external tagging can be a valuable method to attach electronic tags to ish, substantial tag loss and adverse efects to the ish can occur. In this context, it is important to distinguish between acute and chronic impacts of external tagging on ish behavior and health. External attachment of standard electronic tags can be achieved more quickly and less invasively than by surgical implantation employing suture closure, and may, particularly through dart-deployment in the ield, require no anesthesia or handling of the ish [9]. herefore, recovery and subsequent change in behavior from external tagging may be minimal and involve no immediate risk of pathogen entry to the body cavity. However, while incision and closure (by suturing) of the body wall in surgical implantation is invasive, once healed, long-term impacts are often low, while increased tissue abrasion, tag visibility to predators, and long-term elevated drag efects have the potential to generate marked chronic impacts in external telemetry tagging applications [4, 8]. his is the main reason for generally recommending surgical implants for long-term studies. Some of the subtle efects of tagging and release into the natural environment, such as predation risk, are among the best indicators of impact [92], but are increasingly diicult to evaluate under controlled conditions because of complexities in obtaining ethical/welfare committee decisions to do so. One of the few examples of studying increased predation risk resulting from external electronic tagging [80] is more than 30 years old. Control ish (handled and individually identiiable but not telemetry-tagged) cannot easily be recaptured from many natural environments, so this inhibits or biases assessment of their survival, by comparison to telemetry tagged ish, the known locations of which facilitate recapture, at least in shallow water. Also, under ield conditions, without direct observation or tag recovery, it can be diicult to distinguish telemetry tag loss from mortality of the tagged ish, and to determine the cause of mortality (whether from disease or predation, for example), in many aquatic habitats. he best options for quantifying efects may be in experiments using semi-natural closed systems that can be drained down and eiciently sampled, and where densities of predators and prey, including instrumented/ Jepsen et al. Anim Biotelemetry (2015) 3:49 treated ish, can be manipulated. However, there can be problems with obtaining animal welfare permission to establish such systems where the prime objective is to expose tagged, sham-treated, and control animals to predation risk. Animal welfare committees can perceive this as unnecessarily stressful to the experimental prey ish, but demonstration of no impact (and hence bias) under nature-like conditions for telemetry studies needs exactly this type of experiment and evidence base. Advantages and disadvantages of external tagging Advantages of external tagging include (1) the attachment can be easy and fast and requires less training than some other tagging methods; (2) the method can be used for ishes with a body shape not suitable for surgical implantation, for instance, in laterally or dorso-ventrally compressed ish with little space available in the body cavity; (3) external tag position is an advantage if sensors are used to record external variables (e.g. water temperature, light, acceleration, salinity and oxygen concentration); (4) anesthetization is not always required or desirable (e.g. for many large, marine, pelagic species, or for large freshwater ishes like sturgeon); (5) tagging ish like adult salmon, that may be used for consumption, without using anesthesia, makes it possible to release these immediately after tagging without a withdrawal period [89]. Such a period is often required to prevent human consumption of ‘narcotics’, and (6) if recovery of tags is essential, external tags can easily be identiied by ishers at recapture and there is no need for a conventional external tag to identify tagged ish (which is especially important for data storage tags that need to be returned to download stored data). Further, externally tagged ish can be more easily recaptured, because the external tags can be entangled in gillnets [93]. his may be regarded as a disadvantage, but it is sometimes an advantage if the tags need to be retrieved (e.g. data storage tags [93]). External attachment is the only option for PSATs that must be released from the ish and loat to the surface to be able to transmit data to satellites. A last advantage of external tagging is that it can be applied to female ish close to the spawning period. Using surgical implants on gravid females may be problematic due to the presence of large gonads (lack of room) and the concern that a tag may block the passage of eggs and thus interfere with spawning. he most commonly reported problems with external tags are tissue damage, tag loss and decreased swimming capacity. In summary, the disadvantages of external tagging are that (1) the tag interferes with the streamlined body shape of the ish and increases drag, disequilibrium and energy expenditure, and reduces swimming performance, (2) algae and sessile animals may grow on the tag and antenna (fouling, especially in coastal areas) and Page 18 of 23 increase the drag, which may further reduce swimming performance, (3) the tag or antenna can be entangled in aquatic vegetation, roots, between rocks or in ishing nets, (4) the visible tag may afect predation risk, competition and other interactions with conspeciics, (5) the method is not well-suited in the long term for fast-growing or non-feeding ish, (6) attachment wires may, in the long term, cause extensive damage to muscle and integument, (7) there is potential for substantial tag loss in long term studies (size/shape/species dependent), and (8) the method is not usually suitable for measuring internal, physiological variables in the long-term. In many cases researchers can test for these disadvantages in preparation for or during the study. Knowledge about the species in question, the habitat the tagged ish will be in and of the current literature on tagging efects, will aid the decision of tagging method. There is no perfect tagging method: which method to choose? here is no method for attaching electronic tags without some degree of negative impact on the ish, though in many cases the efects may be minimal and may not be detectable in comparisons with controls. he lack of a perfect tagging method and the diversity of taxa and system-speciic efects make it diicult to choose which tagging method to use. Choice of method should be based on careful evaluation of advantages and disadvantages of the diferent tagging methods, dependent on ish species, size, and life stage to be studied and the habitat, duration, and aim of the study. Information and advice to aid the decision can be found in the literature, and particularly from studies of tagging efects in the same or similar species and habitats, but in many cases pilot experiments are necessary. Our own experiences with tagging adult Atlantic salmon and brown trout with radio transmitters can serve as an example of considerations and compromises made when selecting the tagging method. In general, we commonly use surgical implantation for tagging ishes with electronic tags, but have often used external attachment, for example, for adult salmonids during the riverine upstream migration. he reason is that surgical incisions may not heal easily in ish that are in periods of high physical activity, and incisions may open up when ish are jumping and swimming in waterfalls and strong currents (own observations in Atlantic salmon, [27]). An alternative could be to tag ish with surgically implanted tags and hold them for some weeks after tagging in a pen to let the incision heal before release. However, the risk that keeping wild ish in captivity during the migration stage might afect their post-release behavior is too large [e.g. 94]. Laboratory studies in a swim speed chamber Jepsen et al. Anim Biotelemetry (2015) 3:49 have shown that even relatively large external tags (1–3 % tag to body mass ratio) do not afect the swimming performance of Atlantic salmon compared to ish with surgically implanted tags and untagged control ish [27]. However, large external tags (2–5 % tag to body mass ratio) have been shown to reduce the total migration distance of the ish in rivers with strong currents and waterfalls, and increase the duration of delay below waterfalls compared to ish tagged with smaller (0.5–1 % tag to body mass ratio) external or surgically implanted tags in both sea trout and Atlantic salmon ([27] and unpublished results). Hence, it seems that large external tags may afect burst activity and jumping ability more than sustainable swim speeds [27] as would be expected from drag vs swimming velocity relationships. A comparison between ish with small external tags and untagged ish has not been possible in these ield studies. In summary, we have concluded that both surgically implanted and external tags may negatively afect upstream-migrating salmonids in high-gradient rivers with strong lows and obstructions to passage, but that external tags overall have less negative impact than implants in such cases. We use the smallest tags possible in fast-lowing rivers, even though this reduces the duration of the study period, and when we draw conclusions from the results we have to consider that a tagged ish might migrate a shorter distance and at a slower speed than an untagged ish in some cases. he best success in studies using external tag attachment for fusiform or laterally compressed ish has often been achieved with the simplest methods; a tag lattened on the side facing the ish, ixed closely to the body on one side of the ish, usually close to the dorsal in, with two wires through the dorsal muscles. However, as an example of how it is possible to adjust and modify tagging methods to achieve better retention, Beaumont and Masters [24], Armstrong et al. [95], and Herke and Moring [48] all tagged pike externally with diferent methods for diferent purposes and perspectives. Each of the methods had speciic advantages and limitations. For researchers not entirely sure about the choice of tagging method, controlled tag efect studies will be useful to carry out. If resources are small and such studies not possible, it can still be useful to tag a few ish and observe them in the laboratory for shorter or longer time-periods. his can be cost-efective by reducing the risk of performing large ield studies that result in little or heavily biased data because of a large tag loss rate or mortality. Useful information can also be collected by recapture of some of the tagged ish towards the end of ield studies to evaluate tagging efects. his is particularly feasible in smaller freshwater systems, but recaptures by ishers in larger systems, and also in some Page 19 of 23 marine systems, can also help to evaluate the tagging methods. Fish and tag size Despite considerable emphasis on limits of tag mass to ish body mass (e.g. the so-called 2 % rule, [45]), there is no generally applicable rule for how large the tag can be in relation to ish body size [96]. he appropriate maximum relationship between tag size and ish body size is determined by the speciic study objectives, the tagging method, the species/life stage involved, and evidence from pilot studies and related insights. In some cases, tag efects are demonstrated with tags weighing less than 2 % of the body mass of the ish, and in other cases larger tags can be used without any signiicant tagging efects [96]. For potential tagging efects, tag size (volume) can be as important as tag mass. If tags must be large, it is possible to produce them so they are neutrally buoyant in water to reduce the efects of extra weight, but the larger size of the tag may increase drag and risk of entanglement in aquatic vegetation. For PSATs, which are slightly positively buoyant and are attached by a tether, two forces act on the tagged animal: the lift from the tag’s buoyancy and drag as the tag is moved through the water column. Hence, the attachment of PSATs is more challenging than of external tags that can be attached against the ish body. Nevertheless, we would also be very cautious in applying external telemetry tags for studies concentrating on measuring peak swimming performance such as in ishway trials, due to drag efects, though it should be noted that some studies have applied small external PIT tags (0.6 g, <0.5 % tag to body mass ratio), with minimal ish handling, for such evaluations with good outcomes (e.g. [97]). For small ish (<15 cm body length), the authors generally prefer to use surgical implantation instead of external attachment methods. his is because a similar sized tag can be carried inside the body cavity better than externally, because the tag is nearer the ish’s center of mass and there is no drag. However, the recent advent of radioand acoustic ‘picotags’ (<1 g in weight) now allow the tracking of smaller individuals, albeit over shorter time periods (7–21 days), and may in some instances be wellsuited for external attachment as some of the cited papers have shown. Equally, Deng et al’s [39] demonstration of an injectable acoustic tag, 0.22 g mass in air and 3.4 mm in diameter with a life of 100 days provides a long-life, rapid tagging option that may herald a new generation of picotag with low tagging impact. here is no clear tag/ish size threshold, so we recommend using as small tags as possible to safeguard against negative efects, even though this may compromise the duration of the study period. If the goal is to study ish Jepsen et al. Anim Biotelemetry (2015) 3:49 behavior over several seasons, an option is to tag new ish each season instead of studying the same ish over longer term. Several studies have shown that tag efects are less severe for smaller tags when compared to larger tag sizes (e.g. [28, 58]). For example, a larger proportion of ish with large external tags had signs of wounds at the tag attachments than those tagged with smaller tags [27]. Tag shape External tags are often attached with stainless steel wires or nylon ilaments through the muscle at the dorsal in, with the tag resting at the skin below the in. Tags with a lat shape facing the body are better suited for such external attachment than cylindrical tags because they interfere less with a streamlined body shape, rest closer to the ish, and are, therefore, less likely to loosen and cause long-term negative impacts. However, due to the components of acoustic tags, they are usually produced with a cylindrical shape and are, therefore, less suitable for external tagging than radio transmitters and archival tags, which are available in both cylindrical and lat shapes. An exception to this may be for sturgeon, which seems to have better tag retention for cylindrical tags than lat tags when using external attachment, likely because of their concave body shape beneath the bone plates (scutes) [31]. The way forward he large variation in results, even from the same tags attached to the same species and size of ish, makes it diicult to generalize tagging advice, and the best advice is to test the speciic method as thoroughly as possible before using it in the ield. here is a need for more tag efect studies (including externally mounted electronic tags) in both ield and laboratory environments, particularly studies including control groups of untagged ish, studies evaluating efects of diferent tag/ish sizes, and studies with larger sample sizes. Also, inclusion of sham tagged groups could be useful to separate possible efects of the tagging process from the efects of carrying a tag. In studies of surgical implanting, sham-tagged control groups are often included, but this has not been the case in external tagging studies. Although potentially relevant, subtle efects like social interactions and predation are the least studied impacts. Studies of predation risk related to tagging may be among the best bioassays of impact (e.g. [98]) and are important to evaluate how well tagged ish represent natural mortality in diferent ecosystems. here is, however, still a need for studies of tag loss, swimming performance, and growth for many species, as well as studies that can be used to reine tagging methods. Page 20 of 23 For large PSATs, published tagging efect studies have demonstrated particular problems related to tag loss, reduced swim capacity, and likely increased predation. However, there is still a paucity of tag efect studies related to the use of PSATs and a large need for studies quantifying tagging efects and studies that can be used to reine tagging methods and reduce possible efects. In all tagging experiences, it is crucial that the experimental ish are captured (if wild) and handled in the most careful way. Most experienced ish researchers agree that acquiring the right ish, at the right time, in the right condition, is often the most challenging part of a telemetry study, especially when using wild ish. here is much focus in the literature and by ethical committees on tag efects, but often the combined efects of capture and handling may be even more important for the welfare of the ish and the outcome of the study than tagging itself. We would, therefore, like to emphasize the particular need for more studies on efects of capture and handling, by comparison to tagging, on subsequent performance in the short and longer term. Authors’ contributions All authors contributed to the collection of the literature and drafting of the manuscript. All authors read and approved the final manuscript. Author details 1 Section for Freshwater Fisheries and Ecology, Technical University of Denmark, 8600 Silkeborg, Denmark. 2 Norwegian Institute for Nature Research (NINA), 7485 Trondheim, Norway. 3 School of Biological and Biomedical Sciences, Durham University, South Road, Durham DH1 3LE, UK. Acknowledgements NJ was funded by Fiskeplejen (the Danish Rod License), and EBT and TBH were funded by the Norwegian Institute for Nature Research (NINA). Compliance with ethical guidelines Competing interests The authors declare that they have no competing interests. Received: 3 June 2015 Accepted: 17 September 2015 References 1. Shepherd B. Transmitter attachment and fish behaviour. Underw Telem Newsl. 1973;3(1):8–11. 2. Lucas MC, Baras E. Migration of freshwater fishes. Oxford: Blackwell; 2001. 3. Cooke SJ, Hinch SG, Lucas MC, Lutcavage M. Biotelemetry and biologging. In: Zale AV, Parrish DL, Sutton TM, editors. Fisheries techniques. 3rd ed. Bethesda: American Fisheries Society; 2012. p. 819–60. 4. Thorstad EB, Rikardsen AH, Alp A, Økland F. The use of electronic tags in fish research—an overview of fish telemetry methods. Turkish J Fish Aquat Sci. 2013;13:881–96. 5. Bridger CJ, Booth RK. The effects of biotelemetry transmitter presence and attachment procedures on fish physiology and behavior. Rev Fish Sci. 2003;11:13–34. 6. Lucas MC, Baras E. Methods for studying the spatial behaviour of freshwater fishes in the natural environment. Fish Fish. 2000;1:283–316. Jepsen et al. Anim Biotelemetry (2015) 3:49 7. Musyl MK, Domeier ML, Nasby-Lucas N, Brill RW, McNaughton LM, Swimmer JY, Lutcavage MS, Wilson SG, Galuardi B, Liddle JB. Performance of pop-up satellite archival tags. Mar Ecol Prog Ser. 2011;433:1–28. 8. Jepsen N, Koed A, Thorstad E, Baras E. Surgical implantation of transmitters in fish: how much have we learnt? Hydrobiologia. 2002;483:239–48. 9. Cooke SJ, Woodley CM, Eppard MB, Brown RS, Nielsen JL. Advancing the surgical implantation of electronic tags in fish: a gap analysis and research agenda based on a review of trends in intraceoelomic tagging effects studies. Rev Fish Biol Fish. 2011;21:127–51. 10. Baras E. A bibliography on underwater telemetry. Can Rep Fish Aquat Sci. 1991;1819:1–55. 11. Drenner SM, Clark TD, Whitney CK, Martins EG, Cooke SJ, Hinch SG. A synthesis of tagging studies examining the behaviour and survival of anadromous salmonids in marine environments. PLoS One. 2012;7:e31311. 12. Thorsteinsson V. Tagging methods for stock assessment and research in fisheries. Report of concerted action FAIR CT.96.1394 (CATAG). Reykjavik. Marine Research Institute Technical Report; 2002 (79), p. 179. 13. Henderson HF, Hasler AD, Chipman GG. An ultrasonic transmitter for use in studies of movements of fishes. Trans Am Fish Soc. 1966;95:350–6. 14. McCleave JD, Horrall RM. Ultrasonic tracking of homing cutthroat trout (Salmo clarki) in Yellowstone Lake. J Fish Res Board Can. 1970;27:715–30. 15. Carr WES, Chaney TB. Harness for an attachment of an ultrasonic transmitter to the red dru, Sciaenops ocellata. Fish Bull. 1977;74:998–1000. 16. Ichihara T, Soma M, Yoshida K, Suzuki K. An ultrasonic device in biotelemetry and its application to tracking a yellowtail. Bull Far Seas Fish Res Lab. 1972;7:27–48. 17. Holland KN, Braun MJ. Proceedings of “Tying One On”—a workshop on tag attachment techniques for large marine animals. School of Ocean and Earth Science and Technology 03-02, Joint Institute for Marine and Atmospheric Research Contribution 03-349, University of HawaiiManoa. 2003. http://www.soest.hawaii.edu/PFRP/soest_jimar_rpts/ holland_braun.pdf. 18. Hays GC, Bradshaw CJA, James MC, Lovell P, Sims DW. Why do Argos satellite tags deployed on marine animals stop transmitting? J Exp Mar Biol Ecol. 2007;349:52–60. 19. Økland F, Thorstad EB, Westerberg H, Aarestrup K, Metcalfe J. Development and testing of attachment methods for pop-up satellite archival transmitters in European eel. Anim Biotel. 2013;1:3. 20. Broadhurst BT, Ebner BC, Clear RC. Radio-tagging flexible-bodied fish: temporary confinement enhances radio-tag retention. Mar Freshw Res. 2009;60:356–60. 21. Broadhurst BT, Ebner BC, Clear RC. Effects of radio-tagging on two-yearold, endangered Macquarie perch (Macquaria australasica: Percichthyidae). Mar Freshw Res. 2009;60:341–5. 22. O’Connor JP, Koehn JD, Nicol SJ, O’Mahony DJ, McKenzie JA. Retention of radio tags in golden perch (Macquaria ambigua), silver perch (Bidyanus bidyanus) and carp (Cyprinus carpio). Mar Freshw Res. 2009;60:334–40. 23. Corbett SC, Moser ML, Dittman AH. Experimental evaluation of adult spring Chinook salmon radio-tagged during the late stages of spawning migration. N Am J Fish Manage. 2012;32:853–8. 24. Beaumont WRC, Masters JEG. A method for the attachment of miniature radio tags to pike Esox lucius. Fish Manag Ecol. 2003;10:407–9. 25. McCubbing DJF, Bayliss BD, Locke VM. Spawning migration of radio tagged landlocked Arctic Charr, Salvelinus alpinus L. in Ennerdale lake, the English Lake District. Hydrobiologia. 1998;371(372):173–80. 26. Økland F, Jensen AJ, Johnsen BO. Winter habitat and seaward migration of a Norwegian brown trout population. In: Baras E, Philippart J-C, editors. Underwater biotelemetry. Proceedings of the first conference and workshop on fish telemetry in Europe: April 4–6, 1995; Liege. Belgium: University of Liege; 1996. p. 161–71. 27. Thorstad EB, Økland F, Finstad B. Effects of telemetry transmitters on swimming performance of adult Atlantic salmon. J Fish Biol. 2000;57:531–5. 28. Thorstad EB, Foldvik A, Lo H, Bjørnå T, Stensli JH. Effects of handling adult sea trout (Salmo trutta) in a fishway and tagging with external radio transmitters. Boreal Env Res. 2014;19:408–16. Page 21 of 23 29. Collins MR, Cooke DW, Smith TIJ. Telemetry of shortnose and Atlantic sturgeons in the southeastern USA. In: Eiler JH, Alcorn DJ, Neuman MR, editors. Proceedings of the 15th international symposium on biotelemetry. May 9–14, 1999; Juneau. Wageningen: International Society on Biotelemetry; 2000, p. 145–53. 30. Collins MR, Cooke DW, Smith TIJ, Post WC, Russ DC, Walling DC. Evaluation of four methods of transmitter attachment on shortnose sturgeon, Acipenser brevirostrum. J Appl Ichthyol. 2002;18:491–4. 31. Sutton TM, Volkman ET, Pangle KL, Rajchel DA. Effects of absorbable suture strand diameter on retention of external radio transmitters by juvenile lake sturgeon. N Am J Fish Manage. 2004;24:1404–8. 32. Sutton TM, Benson AC. Influence of external transmitter shape and size on tag retention and growth of juvenile lake sturgeon. Trans Am Fish Soc. 2003;132:1257–63. 33. Counihan TD, Frost CN. Influence of externally attached transmitters on the swimming performance of juvenile white sturgeon. Trans Am Fish Soc. 1999;128:965–70. 34. Holbrook SC, Byars WD, Lamprecht SD, Leitner JK. Retention and physiological effects of surgically implanted telemetry transmitters in blue catfish. N Am J Fish Manage. 2012;32(2):276–81. 35. Bodine KA, Fleming P. Evaluation of an alternative technique for attaching external transmitters to blue catfish. N Am J Fish Manage. 2013;33:950–5. 36. Mitamura H, Mitsunaga Y, Arai N, Viputhanumas T. Comparison of two methods of attaching telemetry transmitters to the Mekong giant catfish, Pangasianodon gigas. Zool Sci. 2006;23:235–8. 37. Baras E, Westerloppe L. Transintestinal expulsion of surgically implanted tags in African catfishes of different size and age. Trans Am Fish Soc. 1999;128:737–46. 38. Cottrill RA, Økland F, Aarestrup K, Jepsen N, Koed A, Hunter KJ, Butterworth KG, McKinley RS. Evaluation of three telemetry transmitter attachment methods for female silver-phase American eels (Anguilla rostrata Lesueur). J Great Lakes Res. 2006;32:502–11. 39. Deng ZD, Carlson TJ, Li H, Xiao J, Myjak MJ, Lu J, Martinez JJ, Woodley CM, Weiland MA, Eppard MB. An injectable acoustic transmitter for juvenile salmon. Sci Rep. 2015;5:#8111. doi:10.1038/srep08111. 40. Brown RS, Deng ZD, Cook KV, Pflugrath BD, Li X, Fu T, Martinez JJ, Li H, Trumbo BA, Ahmann ML, Seaburg AG. A field evaluation of an external and neutrally buoyant acoustic transmitter for juvenile salmon: Implications for estimating hydroturbine passage survival. PLoS One. 2013;8(10):e77744. 41. Deng ZD, Martinez JJ, Colotelo AH, Abel TK, LeBarge AP, Brown RS, Pflugrath BD, Mueller RP, Carlson TJ, Seaburg AG, Johnson RL, Ahmann ML. Development of external and neutrally buoyant acoustic transmitters for juvenile salmon turbine passage evaluation. Fish Res. 2012;113:95–105. 42. Bégout Anras ML, Bodaly RA, McNicol R. Use of an acoustic beam actograph to assess the effects of external tagging procedure on lake whitefish swimming activity. Trans Am Fish Soc. 1998;127:329–35. 43. Pursche AR, Walsh CT, Taylor MD. Evaluation of a novel external tag-mount for acoustic tracking of small fish. Fish Manag Ecol. 2014;21:169–72. 44. Brown R, Eiler JH. Performance of Yukon River inconnu tagged with external and internal radio transmitters. In: Eiler JH, Alcorn DJ, Neuman MR, editors. Proceedings of the 15th international symposium on biotelemetry, May 9–14, 1999; Juneau. Wageningen: International Society on Biotelemetry; 2000, p. 145–53. 45. Winter JD. Underwater biotelemetry. In: Nielsen LA, Johnson DL, editors. Fisheries techniques. Bethesda: American Fisheries Society; 1983. p. 371–95. 46. Young AH, Tytler P, Holliday FGT, MacFarlane A. A small sonic tag for measurement of locomotor behavior in fish. J Fish Biol. 1972;4:57–65. 47. Weimer EJ, Duehr JP, Brown ML. Comparison of two external transmitter types on two sizes of bluegills and yellow perch. N Am J Fish Manage. 2006;26:670–5. 48. Herke SW, Moring JR. “Soft” harness for external attachment of large radio transmitters to northern pike (Esox lucius). Fish Res. 1999;39:305–12. 49. Arnold GP, Holford BH. The physical effects of an acoustic tag on the swimming performance of plaice and cod. J Cons Explor Mer. 1978;38:189–200. Jepsen et al. Anim Biotelemetry (2015) 3:49 50. Righton D, Kjesbu OS, Metcalfe J. A field and experimental evaluation of the effect of data storage tags on the growth of cod. J Fish Biol. 2006;68:385–400. 51. Hunter E, Buckley AA, Stewart C, Metcalfe JD. Migratory behaviour of the thornback ray Raja clavata, in the southern North Sea. J Mar Biol Ass UK. 2005;85:1095–105. 52. Jadot C. Comparison of two tagging techniques for Sarpa salpa: external attachment and intraperitoneal implantation. Oceanol Acta. 2003;26:497–501. 53. Bégout Anras ML, Covès D, Dutto G, Laffargue P, Lagardère F. Tagging juvenile seabass and sole with telemetry transmitters: medium-term effects on growth. ICES J Mar Sci. 2003;60:1328–34. 54. Jellyman D, Tsukamoto K. Swimming depths of offshore migrating longfin eels Anguilla dieffenbachii. Mar Ecol Prog Ser. 2005;286:261–7. 55. Grusha DS, Patterson MR. Quantification of drag and lift imposed by pop-up satellite archival tags and estimation of the metabolic cost to cownose rays (Rhinoptera bonasus). Fish Bull. 2005;103:63–70. 56. Thorstad EB, Økland F, Heggberget TG. Are long term negative effects from external tags underestimated? Fouling of an externally attached telemetry transmitter. J Fish Biol. 2001;59:1092–4. 57. Gaertner D, Hallier JP. Tag shedding by tropical tunas in the Indian Ocean and other factors affecting the shedding rate. Fish Res. 2015;163:98–105. 58. Witt MJ, Doherty PD, Godley BJ, Graham RT, Hawkes LA, Henderson SM. Basking shark satellite tagging project: insights into basking shark (Cetorhinus maximus) movement, distribution and behaviour using satellite telemetry (Phase 1, July 2014). Scottish Natural Heritage Commissioned Report No. 752. 59. Schauer J, Hissmann K, Fricke H. A method for deployment of externally attached sonic fish tags from a manned submersible and their effects on coelacanths. Mar Biol. 1997;128:359–62. 60. Thorstad EB, Hay CJ, Næsje TF, Økland F. Movements and habitat use of three cichlid species in the Zambezi River, Namibia. Ecol Freshw Fish. 2001;10:238–46. 61. Thorstad EB, Hay CJ, Næsje TF, Chanda B, Økland F. Movements and habitat utilization of nembwe, Serranochromis robustus (Günther, 1864), in the Upper Zambezi River. Afr Zool. 2005;40:253–9. 62. Steinhausen MF, Andersen NG, Steffensen JF. The effect of external dummy transmitters on oxygen consumption and performance of swimming Atlantic cod. J Fish Biol. 2006;69:951–6. 63. Lewis AE, Muntz WRA. The effects of external ultrasonic tagging on the swimming performance of rainbow trout, Salmo gairdneri Richardson. J Fish Biol. 1984;25:577–85. 64. Mellas EJ, Haynes JM. Swimming performance and behavior of rainbow trout (Salmo gairdneri) and white perch (Morone americana): effects of attaching telemetry transmitters. Can J Fish Aquat Sci. 1985;42:488–93. 65. Peake S, McKinley RS, Scruton DA, Moccia R. Influence of transmitter attachment procedures on swimming performance of wild and hatchery-reared Atlantic salmon smolts. Trans Am Fish Soc. 1997;126:707–14. 66. McCleave JD, Stred KA. Effect of dummy telemetry transmitters on stamina of Atlantic salmon (Salmo salar) smolts. J Fish Res Board Can. 1975;32:559–63. 67. Janak JM, Brown RS, Colotelo AH, Pflugrath BD, Stephenson JR. The effects of neutrally buoyant, externally attached transmitters on swimming performance and predator avoidance of juvenile Chinook salmon. Trans Am Fish Soc. 2012;141:1424–32. 68. Makiguchi Y, Ueda H. Effects of external and surgically implanted dummy radio transmitters on mortality, swimming performance and physiological status of juvenile masu salmon Oncorhynchus masou. J Fish Biol. 2009;74:304–11. 69. Burgerhout E, Manabe R, Brittijn SA, Aoyama J, Tsukamoto K, van den Thillart GEEJM. Dramatic effect of pop-up satellite tags on eel swimming. Naturwissenschaften. 2011;98:631–4. 70. Methling C, Tudorache C, Skov PV, Steffensen JF. Pop up satellite tags impair swimming performance and energetics of the European eel (Anguilla anguilla). PLoS One. 2011;6(6):e20797. 71. Tudorache C, Burgerhout E, Brittijn S, van den Thillart G. The effect of drag and attachment site of tags on swimming eels: experimental quantification and evaluation tool. PLoS One. 2014;9:e112280. Page 22 of 23 72. Gray RH, Haynes JM. Spawning migration of adult chinook salmon (Oncorhynchus tshawytscha) carrying external and internal radio transmitters. J Fish Res Board Can. 1979;36:1060–4. 73. Sundström LF, Gruber SH. Effects of capture and transmitter attachments on the swimming speed of large juvenile lemon sharks in the wild. J Fish Biol. 2002;61:834–8. 74. Greenstreet SPR, Morgan RIG. The effect of ultrasonic tags on the growth rates of Atlantic salmon, Salmo salar L., parr of varying size just prior to smolting. J Fish Biol. 1989;35:301–9. 75. Baras E. Time and space utilisation modes and strategies in the common barbel, Barbus barbus (L.). Cahiers d’Ethologie. 1992;12:125–442. 76. Eveson JP, Welch DW. Evaluation of techniques for attaching archival tags to salmon: influence on growth and survival. In: Moore A, Russell I, editors. Advances in fish telemetry. Proceedings of the 3rd conference on fish telemetry in Europe. CEFAS, Lowestoft. 2000, p. 29–35. 77. Beaumont WRC, Clough S, Ladle M, Welton JS. A method for the attachment of miniature radio tags to small fish. Fish Manag Ecol. 1996;3:201–7. 78. Caffrey JM, Conneely JJ, Connolly B. Radio telemetric determination of bream (Abramis brama L.) movements in Irish canals. In: Baras E, Philippart JC, editors. Underwater biotelemetry. Proceedings of the first conference and workshop on fish telemetry in Europe 1996. University of Liege, 1996, p. 59–65. 79. Cooke SJ. Externally attached radio transmitters do not affect the parental care behavior of rock bass. J Fish Biol. 2003;62:965–70. 80. Ross MJ, McCormick JH. Effects of external radio transmitters on fish. Prog Fish Cult. 1981;43:67–72. 81. Brown RS, Pflugrath BD, Carlson TJ, Deng ZD. The effect of an externally attached neutrally buoyant transmitter on mortal injury during simulated hydroturbine passage. J Renew Sustain Energ. 2012;4:e013107. 82. Økland F, Hay CJ, Næsje TF, Nickandor N, Thorstad EB. Learning from unsuccessful radio tagging of common carp in a Namibian reservoir. J Fish Biol. 2003;62:735–9. 83. Aarestrup K, Jepsen N. Spawning migration of sea trout (Salmo trutta L.) in a Danish river. Hydrobiologia. 1998;371(372):275–81. 84. Aarestrup K, Jepsen N, Rasmussen G, Økland F, Thorstad B, Holdensgaard G. Prespawning migratory behaviour and spawning success of sea-ranched Atlantic salmon (Salmo salar L.) in the River Gudenaa, Denmark. Fish Manag Ecol. 2000;7:387–400. 85. Perrow MR, Jowitt AJD, Johnson SR. Factors affecting the habitat selection of tench in a shallow eutrophic lake. J Fish Biol. 1996;48:859–70. 86. Hanson KC, Ostrand KG. Evaluation of transmitter application techniques for use in research of adult eulachon. N Am J Fish Manage. 2013;33:1119–24. 87. Moyes CD, Fragoso N, Brill RW, Musyl MK. Predicting post release survival in large pelagic fish. Trans Am Fish Soc. 2006;135:1389–97. 88. Kerstetter DW, Polovina JJ, Graves JE. Evidence of shark predation and scavenging on fishes equipped with pop-up satellite archival tags. Fish Bull. 2004;102:750–6. 89. Wahlberg M, Westerberg H, Aarestrup K, Feunteun E, Gargan P, Righton D. Evidence of marine mammal predation of the European eel (Anguilla anguilla L.) on its marine migration. Deep-Sea Res. 2014;86:32–8. 90. Kerstetter DW, Graves JE. Survival of white marlin (Tetrapturus albididus) released from commercial pelagic longline gear in the western North Atlantic. Fish Bull. 2006;104:434–44. 91. Beguer-Pon M, Benechetrit J, Castonguay M, Aarestrup K, Campana SE, Stokesbury MJW, Dodson JJ. Shark predation on migrating adult American eels (Anguilla rostrata) in the Gulf of St. Lawrence. PLoS One. 2012;7:e46830. 92. Wargo Rub AM, Jepsen N, Liedtke TL, Moser ML, Weber EPS. Surgical tagging and telemetry methods in fisheries research: promoting veterinary and research collaboration. Am J Vet Res. 2014;75:402–16. 93. Rikardsen AH, Thorstad EB. External attachment of data storage tags increases probability of being recaptured in nets compared to internal tagging. J Fish Biol. 2006;68:963–8. 94. Donaldson MR, Hinch SG, Patterson DA, et al. The consequences of angling, beach seining, and confinement on the physiology, postrelease behaviour and survival of adult sockeye salmon during upriver migration. Fish Res (Amsterdam). 2011;108:133–41. Jepsen et al. Anim Biotelemetry (2015) 3:49 95. Armstrong JD, Lucas MC, Priede IG, DeVera L. An acoustic telemetry system for monitoring the heart rate of pike, Esox lucius L., and other fish in their natural environment. J Exp Biol. 1989;143:549–52. 96. Jepsen N, Schreck C, Clement S, Thorstad E. A brief discussion of the 2 % tag/bodymass rule. In: Spedicato MT, Marmulla G, Lembo G, editors. Aquatic telemetry: advances and applications. FAO—COISPA, Rome. 2005, p. 255–9. 97. Castro-Santos T, Haro A, Walk S. A passive integrated transponder (PIT) tag system for monitoring fishways. Fish Res. 1996;28:253–61. 98. Jepsen N, Christoffersen M, Munksgaard T. The level of predation used as indicator of tagging/handling effects. Fish Man Ecol. 2008;15:365–8. 99. Almeida PR, Quintella BR, Dias NM. Movement of radio-tagged anadromous sea lamprey during the spawning migration in the River Mondego (Portugal). Hydrobiologia. 2002;83:1–8. 100. Speed CW, O’Shea OR, Meekan MG. Transmitter attachment and release methods for short-term shark and stingray tracking on coral reefs. Mar Biol. 2013;160:1041–50. 101. West GJ, Stevens JD. Archival tagging of school shark, Galeorhinus galeus, in Australia: initial results. Env Biol Fish. 2001;60:283–98. 102. Blaylock RA. Effects of external biotelemetry transmitters on behaviour of the cownose ray Rhinoptera bonasus (Mitchill 1815). J Exp Mar Biol Ecol. 1990;141:213–20. 103. Corcoran MJ, Wetherbee BM, Shivji MS, Potenski MD, Chapman DD, Harvey GM. Supplemental feeding for ecotourism reverses diel activity and alters movement patterns and spatial distribution of the southern stingray, Dasyatis americana. PLoS One. 2013;8(3):e59235. 104. Moser ML, Ross SW. Habitat use and movements of shortnose and Atlantic sturgeons in the lower Cape Fear River, North Carolina. Trans Am Fish Soc. 1995;124:225–34. 105. Crook DA. A method for externally attaching radio transmitters to minimize dermal irritation. J Fish Biol. 2004;64:258–61. 106. Økland F, Thorstad EB, Hay CJ, Næsje TF, Chanda B. Patterns of movement and habitat use by tigerfish (Hydrocynus vittatus) in the Upper Zambezi River (Namibia). Ecol Freshw Fish. 2005;14:79–86. 107. Facey DE, McCleave JD, Doyon GE. Responses of Atlantic salmon parr to output of pulsed ultrasonic transmitters. Trans Am Fish Soc. 1977;106:489–96. 108. Solomon DJ. Migration of smolts of Atlantic salmon (Salmo salar L.) and sea trout (Salmo trutta L.) in a chalkstream. Environ Biol Fish. 1978;2:223–9. 109. Johnstone ADF, Walker AF, Urquhart GG, Thorne AA. Acoustic tracking of sea trout smolts, Salmo trutta L., on the west coast of Scotland. In: Baras E, Philippart JC, editors. Underwater biotelemetry. Proceedings of the first conference and workshop on fish telemetry in Europe, University of Liège; 1996, pp 59–65. Page 23 of 23 110. Holliday FGT, Tytler P, Young AH. Activity levels of trout (Salmo trutta) in Airthrey Loch, Stirling, and Loch Leven, Kinross. Proc R Soc Edinb (B). 1973;74:315–31. 111. Priede IG, Young AH. The ultrasonic telemetry of cardiac rhythms of wild brown trout (Salmo trutta L.) as an indicator of bio-energetics and behaviour. J Fish Biol. 1977;10:299–318. 112. Oswald RL. The use of telemetry to study light synchronization with feeding and gill ventilation rates in Salmo trutta. J Fish Biol. 1978;13:729–39. 113. Dombeck MP. Movement and behaviour of the muskellunge determined by radio-telemetry. Department of natural resources. Technical bulletin 113. Madison, Wisconsin, Department of Natural Resources; 1979. 114. Claireaux G, Lefrançois C. A method for the external attachment of acoustic tags on roundfish. Hydrobiologia. 1998;371(372):113–6. 115. Caldwell IR, Correia M, Palma J, Vincent ACJ. Advances in tagging syngnathids, with the effects of dummy tags on behaviour of Hippocampus guttulatus. J Fish Biol. 2011;78:1769–85. 116. Matthews KR, Quinn TP, Miller BS. Use of ultrasonic transmitters to track demersal rockfish movements on shallow rocky reefs. Am Fish Soc Symp. 1990;7:375–9. 117. Chamberlain A. Effects of tagging on equilibrium and feeding. Underw Telem Newsl. 1979;9(1):1–3. 118. Lefrançois C, Odion M, Claireaux G. An experimental and theoretical analysis of the effect of added weight on the energetics and hydrostatic function of the swimbladder of European sea bass (Dicentrarchus labrax). Mar Biol. 2001;139:13–7. 119. Khan MT, Khan TA, Wilson ME. Habitat use and movement of river blackfish (Gadopsis marmoratus R.) in a highly modified Victorian stream using radio telemetry. Ecol Freshw Fish. 2004;13:285–93. 120. Ralston SL, Horn MH. High tide movements of the temperate-zone herbivorous fish Cebidichthys violaceus (Girard) as determined by ultrasonic telemetry. J Exp Mar Biol Ecol. 1986;98:35–50. 121. Campbell HA, Bishop CM, Davies DA, Egginton S. Recording long-term heart rate in Paranotothenia angustata using an electronic datalogger. J Fish Biol. 2005;67:1150–6. 122. Holland KN, Brill RW, Chang RKC. Horizontal and vertical movements of yellowfin and bigeye tuna associated with fish aggregating devices. Fish Bull. 1990;88:493–507. 123. Lutcavage ME, Brill RW, Skomal GB, Chase BC, Howey PW. Results of pop-up satellite tagging of spawning size class fish in the Gulf of Maine: do North Atlantic Bluefin tuna spawn in the mid-Atlantic? Can J Fish Aquat Sci. 1999;56:173–7. 124. Connolly RM, Melville AJ, Preston KM. Patterns of movement and habitat use by leafy seadragons tracked ultrasonically. J Fish Biol. 2002;61:684–95. 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Jepsen, N., Thorstad, E.B., Havn, T. & Lucas, M.C. (2015) The use of external electronic tags on fish: an evaluation of tag retention and tagging effects. Animal Biotelemetry 3:49 DOI 10.1186/s40317-015-0086-z.

Jepsen, N., Thorstad, E.B., Havn, T. & Lucas, M.C. (2015) The use of external electronic tags on fish: an evaluation of tag retention and tagging effects. Animal Biotelemetry 3:49 DOI 10.1186/s40317-015-0086-z.

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