Physiological responses of Pacific halibut, <Emphasis Type="Italic">Hippoglossus stenolepis</Emphasis>, to intracoelomic implantation of electronic archival tags,with a review of tag implantation techniques employed in flatfishes

Management of Pacific halibut (Hippoglossus stenolepis), a long-lived flatfish, is complicated by possible ontogenic and sex-specific variation in migration. Archival tags promise the ability to help uncover long-term movement patterns at the individual level, if the tags can be retained and recovered from healthy fish. We examined fifteen individuals (69–90 cm fork length) for long-term physiological response to intracoelomic implantation of three types of archival tags: fully internal, internal with right angle protruding light stalk, and internal with straight protruding light stalk. Tags represented 0.05–0.16% of initial fish weights. Fish were reared at 10.8 ± 1.1°C for 59 weeks post-surgery. One fish died after 39 weeks from thermal stress unrelated to the surgical procedure. Temporal variation in behavior of tagged fish was indistinguishable from that of controls (n = 15 tagged, 5 controls). Treatment and control-group fish grew at similar rates. No tag expulsion or physiological response was evident in the individual that died at 39 weeks, but nine of eleven individuals dissected at the end of 59 weeks had developed internal responses. These responses ranged from deposition of fibrous protein and/or calcitic material on tag surfaces to partial or full tag encapsulation in either the visceral peritoneal layer (fully-internal tags) or the intestinal mesenteries (stalk-bearing tags). The responses were within the range reported for other pleuronectids implanted with tags of similar configuration and may have implications for design and interpretation of long-term tagging studies. Encapsulation may reduce the probability of tag recoveries even in the absence of tag expulsion, especially in species eviscerated at sea.     

An introduction to the practical and ethical perspectives on the need to advance and standardize the intracoelomic surgical implantation of electronic tags in fish

The intracoelomic surgical implantation of electronic tags (including radio and acoustic telemetry transmitters, passive integrated transponders and archival biologgers) is frequently used for conducting studies on fish. Electronic tagging studies provide information on the spatial ecology, behavior and survival of fish in marine and freshwater systems. However, any surgical procedure, particularly one where a laparotomy is performed and the coelomic cavity is opened, has the potential to alter the survival, behavior or condition of the animal which can impair welfare and introduce bias. Given that management, regulatory and conservation decisions are based on the assumption that fish implanted with electronic tags have similar fates and behavior relative to untagged conspecifics, it is critical to ensure that best surgical practices are being used. Also, the current lack of standardized surgical procedures and reporting of specific methodological details precludes cross-study and cross-year analyses which would further progress the field of fisheries science. This compilation of papers seeks to identify the best practices for the entire intracoelomic tagging procedure including pre- and post-operative care, anesthesia, wound closure, and use of antibiotics. Although there is a particular focus on salmonid smolts given the large body of literature available on that group, other life-stages and species of fish are discussed where there is sufficient knowledge. Additional papers explore the role of the veterinarian in fish surgeries, the need for minimal standards in the training of fish surgeons, providing a call for more complete and transparent procedures, and identifying trends in procedures and research needs. Collectively, this body of knowledge should help to improve data quality (including comparability and repeatability), enhance management and conservation strategies, and maintain the welfare status of tagged fish.     

Antibiotic use during the intracoelomic implantation of electronic tags into fish

The use of antibiotics, in particular, the use of a single dose of antibiotics during electronic tag implantation is of unproven value, and carries with it the potential for the development of antibiotic resistance in bacteria and the alteration of the immune response of the fish. Antibiotic use during electronic tag implantation must conform to relevant drug laws and regulations in the country where work is being done, including the requirements for withdrawal times before human consumption is a possibility. Currently, the choice of antibiotics (most often tetracycline or oxytetracycline) and the use of a single dose of the drug are decisions made without knowledge of the basic need for antibiotic usage and of the bacteria involved in infections that occur following electronic tag implantation. Correct perioperative use of an antibiotic is to apply the drug to the animal before surgery begins, to assure serum and tissue levels of the drug are adequate before the incision is made. However, the most common perioperative application of antibiotics during implantation of an electronic tag is to delay the administration of the drug, injecting it into the coelom after the electronic tag is inserted, just prior to closure of the incision. There is little empirical evidence that the present application of antibiotics in fish being implanted with electronic tags is of value. Improvements should first be made to surgical techniques, especially the use of aseptic techniques and sterilized instruments and electronic tags, before resorting to antibiotics.     

Training considerations for the intracoelomic implantation of electronic tags in fish with a summary of common surgical errors

Training is a fundamental part of all scientific and technical disciplines. This is particularly true for all types of surgeons. For surgical procedures, a number of skills are necessary to reduce mistakes. Trainees must learn an extensive yet standardized set of problem-solving and technical skills to handle challenges as they arise. There are currently no guidelines or consistent training methods for those intending to implant electronic tags in fish; this is surprising, considering documented cases of negative consequences of fish surgeries and information from studies having empirically tested fish surgical techniques. Learning how to do fish surgery once is insufficient for ensuring the maintenance or improvement of surgical skill. Assessment of surgical skills is rarely incorporated into training, and is needed. Evaluation provides useful feedback that guides future learning, fosters habits of self-reflection and self-remediation, and promotes access to advanced training. Veterinary professionals should be involved in aspects of training to monitor basic surgical principles. We identified attributes related to knowledge, understanding, and skill that surgeons must demonstrate prior to performing fish surgery including a “hands-on” assessment using live fish. Included is a summary of common problems encountered by fish surgeons. We conclude by presenting core competencies that should be required as well as outlining a 3-day curriculum for training surgeons to conduct intracoelomic implantation of electronic tags. This curriculum could be offered through professional fisheries societies as professional development courses.     

Effects of acoustic tagging on juvenile green sturgeon incision healing,swimming performance,and growth

Ultrasonic telemetry is a preferred method for fish-movement studies. Despite surgical tag implantation being the most common method for affixing tags, many studies lack tests addressing the assumption that tagging has no effect on fish performance or survival. The threatened, anadromous green sturgeon, Acipenser medirostris, has little documentation concerning its movements. We evaluated the effects of surgery and tag implantation in juveniles. We compared three groups: tagged fish with dummy transmitters implanted in the peritoneal cavity, sham fish that underwent surgery without tag implantation, and control fish that were handled and anesthetized but did not undergo surgery. We found no differences in growth or critical swimming velocity among groups. Photos of incisions were taken towards the beginning and at the end of the study to assess inflammation and to score each incision for closure and suture retention. Inflammation declined similarly for tagged and sham fish during the study. U_crit was not related to the extent of inflammation or to post-surgery time. All fish showed healing during the study (ca. 140 day duration) and 10 % of tagged and sham fish showed signs of inflammation by the study end. These results suggest that current ultrasonic surgical tagging methods do not significantly affect the short-term growth or swimming performance of juvenile green sturgeon. Additionally, effects of surgery can be mitigated by minimizing the number of suture entry points and by using rapid-absorbing sutures.     

Tag retention and survival of juvenile bighead carp implanted with a dummy acoustic tag at three temperatures

Bighead carp Hypophthalmichthys nobilis and silver carp Hypophthalmichthys molitrix (together, the bigheaded carps) are invasive fishes in North America that have resulted in substantial negative effects on native fish communities and aquatic ecosystems. Movement and behavior of adult bigheaded carps has been studied previously using telemetry, while similar studies with juvenile bigheaded carps have yet to be attempted. Recent technological advances in telemetry transmitters has increased the availability of tags sufficiently small enough to implant in juvenile carps. However, the effects of surgical implantation of telemetry tags on juvenile bigheaded carps have not been evaluated. We determined tag retention and survival associated with surgical implantation of acoustic telemetry tags into juvenile bighead carp (range 128–152 mm total length) at three temperatures (13, 18, and 23°C). In addition, we assessed the effect of surgically implanted transmitters on the fitness, defined as changes in weight or critical swimming speed, of carp implanted with transmitters. Survival was high among tagged fish (85%) with 47% of tags retained at the conclusion of the 45‐day study. No substantial decline in fitness of the fish was observed in tagged fish compared to untagged fish.     

Tag retention and mortality of adult Atlantic salmon Salmo salar gastrically tagged with different sized telemetry transmitters

A batch of 1 sea winter pre‐spawning adult Salmo salar from the Bush river in Northern Ireland, U.K., were gastrically tagged with large (13 mm diameter) and small (9 mm diameter) dummy acoustic telemetry tags alongside untagged control fish. Survival differed between control and tagged fish and the estimated probability of survival by the end of the study for control fish with no tag was 0·94, small tags was 0·90 and large tags was 0·72. Tag loss through regurgitation was slightly higher for fish tagged with larger tags than for fish tagged with smaller tags and the estimated probability of tag loss for fish with a small tag was 0·10 and for large tags was 0·14.     

The novel use of pop‐off satellite tags (PSATs) to investigate the migratory behaviour of European sea bass Dicentrarchus labrax

A total of 12 adult European sea bass Dicentrarchus labrax were tagged with pop‐off satellite archival tags (PSAT) in Irish coastal waters and in offshore waters in the north‐east Celtic Sea between 2015 and 2016. Archived data were successfully recovered from five of the 12 tags deployed, three from fish released in inshore Irish waters and two from fish released offshore in the eastern Celtic Sea. All three fish tagged in inshore waters were found to undertake migrations into the open ocean coinciding with the spawning period. These fish also exhibited fidelity to inshore sites post‐migration, returning to the same general location (within c. 73 km, which is roughly the predicted mean accuracy of the method) of their original release site. Although the number of tracks obtained here was limited, some degree of aggregation between inshore and offshore tagged fish in the eastern Celtic Sea was noted during the expected spawning period suggesting PSATs can provide new information on specific spawning locations of European sea bass.     

Evaluation of PIT‐tagging in cyprinids

Laboratory and field experiments were used to investigate how different marking procedures, with 23 mm PIT (passive integrated transponders) – tags, affected mortality, body condition and tag expulsion in small roach Rutilus rutilus and rudd Scardinus erythrophthalmus (117 to 163 mm total length). In a laboratory experiment mortality was low (≤ 6%) and only occurred among fishes that had their incision closed with sutures. The latter also had a specific growth rate that tended to be lower than the fish tagged without sutures. The different marking procedures did not adversely affect the body condition of fishes either in the laboratory experiment (after 37 days) or in the field experiment (up to 369 days). No tag expulsions were observed among laboratory fishes PIT‐tagged without sutures. Marking without the use of sutures to close the incision, appears to be the most appropriate PIT tagging procedure for small cyprinids.     

Trends in the reporting of tagging procedures for fish telemetry studies that have used surgical implantation of transmitters: a call for more complete reporting

The intracoelomic surgical implantation of telemetry transmitters in fish is becoming the “standard” tagging approach for most field telemetry studies. Subsequently, efforts must be made to ensure the welfare of the fish are maintained and that fish do not experience significant mortality or sublethal impairments in health, behavior or physiology as a result of surgical procedures. Therefore, it is essential to adequately report information relating to all aspects of the surgical procedure to enable the reader to make an accurate interpretation of study results. We conducted a quantitative literature review aimed at characterizing trends in data reporting by examining a sample of fish telemetry studies published in peer-reviewed outlets during the last 20 years. We used a repeatability score, based on 16 predetermined criteria, to evaluate the reporting of surgical procedures in telemetry studies. The majority of studies failed to report basic information relating to the surgical procedures used. Repeatability scores were highly variable between studies and ranged from 0–93.8%. No single study provided complete information (mean repeatability score = 50.7%) and repeatability showed no trend over time. Some study information was consistently well reported (e.g. tag size and dimensions, the type of anaesthetic used and the location of incision). In contrast, the type of suture knots, duration or level of anaesthesia and precautions taken to minimize infection were consistently left out of the methods section of most telemetry studies. Our review was confounded by the large proportion of studies that cited other sources for their surgical methods, many of which themselves lacked complete information. We recommend that future electronic tagging studies that involve intracoelomic implantation include the minimum reporting standards presented in this paper. Increasing the detail of reporting will improve the quality of data presented, minimize welfare and ethical concerns and allow transparency for study repeatability.     

The effects of surgically implanted acoustic transmitters on laboratory growth, survival and tag retention in hatchery yearling Chinook salmon

Telemetry has proven an effective means for studying the movement of fishes, however, biases associated with tagged animals requires careful scrutiny if accurate conclusions are to be made from field studies. The objective of this study was to evaluate growth, survival, and tag retention in hatchery yearling Chinook salmon (Oncorhynchus tshawytscha) juveniles with intracoelomic surgically implanted acoustic transmitters representing 2.6 to 5.6% of body weight. The first trial consisted of three treatments; passive integrated transponder (PIT) tag-only (25 fish), acoustic-tag+PIT-tag (25 fish), and sham-surgery+PIT-tag (25 fish). There were no significant differences in relative growth rate (% change in weight day^?1) among treatments over the 221 day trial. Survival in the acoustic-tag treatment (80%) was not significantly different from the PIT-tag-only and sham treatments (92 and 88% respectively). The second trial consisted of three treatments; PIT-tag-only (22 fish), acoustic-tag+PIT-tag with absorbable sutures (12 fish) and acoustic-tag+PIT-tag with non-absorbable sutures (12 fish). There were no significant differences in relative growth rate among treatments over the 160 day trial. Survival in the second trial was 100%. Fish with absorbable sutures healed sooner and with less inflammation compared to fish with non-absorbable sutures. Tag retention was 100% in both trials. The results of this study suggest that acoustic transmitters of less than 5.6% body weight can be effectively used in 1-year old Chinook salmon.     

The effect of ultrasonic tags on the growth rates of Atlantic salmon, Salmo salar L., parr of varying size just prior to smolting

The attachment of dummy, ultrasonic, acoustic tags, of the Stirling Mk. VI design, to pre-smolt Atlantic salmon parr significantly affected fish growth rates. Fish less than 160 mm in length lost weight and showed no change in length. Fish over 160 mm in length put on weight, though at a rate significantly lower than that of untagged controls. For fish between 160 and 180mm in length, the increase in length was significantly smaller in tagged fish than in untagged controls. Over 180 mm in length, no difference could be detected in the length gains of tagged and untagged fish.
Smaller tagged fish gave up maintaining station and showed signs of distress at an earlier stage in the experiment than larger tagged fish. Tag-related mortality was inversely related to fish size. All but two of the control fish survived the experiment and continued to maintain station throughout.
The results suggest that the minimum length of Atlantic salmon parr on which this design of acoustic tag could be employed is 160 mm, and that caution is needed in the interpretation of track lengths longer than l0 daysof parr in the size range 160–180 mm.     

The veterinarian’s role in surgical implantation of electronic tags in fish

The current role of veterinarians participating in the intracoelomic surgical implantation of electronic tags in fisheries research projects with researchers is limited, but could be expanded. Veterinary training is broadly applicable to conducting surgeries on any species, and there are increasing numbers of veterinarians with fish-specific experience. A few of the roles veterinarians can play include advising on surgical instrument selection and acquisition, interfacing with Institutional Animal Care and Use Committees, devising strategies for anesthesia, providing direction on disinfection and sterilization, complying with regulatory requirements, providing individualized surgery instruction, and occasionally performing field surgeries. Veterinarians and fish researchers bring different strengths and deficits to bear in a fish surgery project, and it is helpful to recognize these for successful collaborations. Engaging veterinary consultation for electronic tag implantation surgeries in fish can be a mutually beneficial experience for the researcher and the veterinarian, with dividends in data quality and welfare of the research subjects.     

Suitability of surgically implanted 8-mm passive integrated transponder tags for small-bodied fishes

Innovative tools that benefit conservation are critical as freshwater fishes are lost at unprecedented rates. Mark-recapture methods can characterize population demographics and life-history traits of diverse fishes, but suitable techniques for tagging for individual recognition of small-bodied fishes are rare. Passive integrated transponder (PIT) tag technology may facilitate the tagging of small fishes and early life stages of larger species. However, relatively little research has evaluated the suitability of these small (8.4 × 1.4 mm) tags for many groups of small fishes. Tag loss (retention and survival) and growth of individuals implanted with PIT tags relative to control and sham treatments were compared for eight fishes of differing morphologies. Additionally, the utility of cyanoacrylate to improve tag retention was tested on a subset of taxa. Fish of each species were equally divided and randomly assigned to one of three treatment groups (handled [control], surgical incision [sham], or surgical incision and PIT tag implantation [PIT]). During the 42-d study period, mortalities and expelled tags were counted daily and growth was measured weekly. Researchers can generally expect little tag loss and uncompromised growth rates for a variety of small-bodied fishes; however, initial fish length was related to the magnitude of physiological effects for some taxa (i.e., blacknose dace Rhinichthys atratulus, johnny darter Etheostoma nigrum, juvenile white sucker Catostomus commersonii). Relatively poor survival (<80%) was observed for two benthic species: johnny darter and blacknose dace, often when incision wounds became inflamed before healing. Prevalent tag loss for johnny darter, tadpole madtom Noturus gyrinus, and a dorsal-laterally compressed cyprinid can be reduced by closing the wounds with cyanoacrylate, but with substantially increased mortality rates. This research demonstrates the broad applicability of PIT tagging technology for ecological studies of small-bodied fishes and alleviates many concerns when surgically implanting tags into several fishes.     

Results of satellite tagging of Atlantic bluefin tuna, <Emphasis Type="Italic">Thunnus thynnus</Emphasis>, off the coast of Ireland

Pop-up satellite archival tags were attached to six Atlantic bluefin tuna (Thunnus thynnus) off the west coast of Ireland in autumn 2003 and 2004. The satellite tags measured pressure, ambient temperature and light for the term of deployment. Radio pop-up satellite endpoint positions, light and sea surface temperature estimations of geolocation indicate that two fish tagged minutes apart off the coast of County Donegal, migrated to the eastern and western Atlantic Ocean over the following 8 months. The two fish were 5218 km apart at the termination of the experiment. After tagging in September and popping up the following March and April, one fish had traveled to the western Atlantic while the other was located in the waters off the southwest coast of Portugal. A third fish tagged off the coast of County Donegal in October 2004 moved into the Mediterranean Sea and was caught by a fishing vessel southeast of Malta on 11 June 2005. The results link bluefin tuna feeding on European foraging grounds with known eastern breeding regions and western Atlantic waters.     

Surgical implantation of radio tags in three eel species (Anguilla spp.) in South Africa

Studies have reported poor survival of surgically tagged freshwater fishes in warm African waters. This study aimed to assess the applicability of using radio telemetry (and surgical implantation of tags) for Anguilla spp. Nineteen yellow eels (Anguilla bengalensis, A. marmorata and A. mossambica) were surgically implanted with radio tags between October 2018 and January 2019 in the Thukela River, South Africa. Most eels were alive 6 months after tagging, and recaptured eels displayed advanced or complete healing at the incision site. Therefore, this method appears suitable for African freshwater eels.     

A non‐invasive method to assess the impact of electronic tag insertion on stress levels in fishes

The present study investigated, for the first time, a non‐invasive technique for monitoring cortisol levels in fishes that had been implanted with electronic transmitters. This technique involved the measurement of cortisol released into the water by individual fish. Carp Cyprinus carpio and roach Rutilus rutilus that had been tagged with miniature dummy acoustic transmitters responded to the surgical implantation of the tags with an immediate (1 to 4 h) increase in cortisol concentrations in the water. These amounts of cortisol were higher than in 'handled only' and 'handled and anaesthetized' groups. Estimated cortisol release rates for both species correlated well with the direct measurements in the water. In both species, water cortisol concentration and cortisol release rates returned to pre‐stress levels within 12 h of tag‐insertion, and remained low for the remainder of the experiment. The calculation of cortisol release rates highlighted a difference of a factor of about four between peak release rates in carp and roach. There was no evident long‐term cortisol stress response to the presence of a tag in the body cavity in either species.     

Carlin tag recoveries as an indicator of predation on salmon smolts by goosanders and red-breasted mergansers

Between 1984 and 1990 a total 221 Carlin tags used to mark salmon Salmo salar smolts in the River North Esk, NE Scotland, were recovered from the stomachs of goosanders Mergus merganser and red-breasted mergansers M. serrator . Both Carlin-tagging and adipose-clipping affected the predation of salmon smolts by sawbill ducks. The mean (± S.D.) sizes of tagged smolts taken by both species were similar (117 ± 3 mm) and significantly smaller than the mean sizes of smolts in the river, possibly due to a reduction in the swimming performance of small smolts bearing tags. Large adipose-clipped smolts (±mean smolt size) were predated significantly more than unclipped smolts, but no such difference was observed for small smolts (相似文献   

Comparison between PIT and radio telemetry to evaluate winter habitat use and activity patterns of juvenile Atlantic salmon and brown trout

Winter habitat use and activity patterns of juvenile Atlantic salmon and brown trout were analysed in a comparative study between Passive Integrated Transponder (PIT) technology, radio telemetry and underwater observation by snorkelling. Two study periods were conducted in Stoney River, Newfoundland, Canada. During Study period I, 49 juvenile Atlantic salmon (fork length: 11.0–18.0 cm) and 7 brown trout (11.0–17.3 cm) were tagged with PIT tags and/or radio transmitters in late winter of 2004. During Study period II, 18 juvenile Atlantic salmon (fork length: 12.0–18.4 cm) and 23 brown trout (10.9–20.8 cm) were tagged and tracked twice a day at 10:00 h and 22:00 h on five consecutive days in late winter of 2005. From the 56 fish released during Study period I, on average 19.6 ± 6.0% of the PIT tagged fish and 99.3 ± 2.2% of the radio tagged fish were relocated during any given survey. Over the Study period II, 39% of fish emigrated from the study site. PIT technology had an efficiency of 39.2 ± 14.1% to detect the remaining fish. In contrast, radio telemetry relocated on average 96.9 ± 6.5% of the tagged fish whereas by snorkelling on average only 4.1 ± 5.6% of the tagged fish were observed. PIT telemetry may however be more efficient in smaller, less heterogeneous streams. The advantage of PIT technology over radio telemetry is clearly that it is relatively less costly permitting higher numbers of individuals to be tagged and there is no limit in the operational life of the transponder. In winter, juvenile salmonids preferred low flow velocity and no preferences were observed for any specific water depth over the range of available water depths. Fish selected preferentially boulder habitat over other substrates in the environment. Habitat utilisation did not differ between day and night. The use of winter preference indices may be important for future habitat modelling.     

A Field Evaluation of an External and Neutrally Buoyant Acoustic Transmitter for Juvenile Salmon: Implications for Estimating Hydroturbine Passage Survival

Turbine-passed fish are exposed to rapid decreases in pressure which can cause barotrauma. The presence of an implanted telemetry tag increases the likelihood of injury or death from exposure to pressure changes, thus potentially biasing studies evaluating survival of turbine-passed fish. Therefore, a neutrally buoyant externally attached tag was developed to eliminate this bias in turbine passage studies. This new tag was designed not to add excess mass in water or take up space in the coelom, having an effective tag burden of zero with the goal of reducing pressure related biases to turbine survival studies. To determine if this new tag affects fish performance or susceptibility to predation, it was evaluated in the field relative to internally implanted acoustic transmitters (JSATS; Juvenile Salmon Acoustic Telemetry System) used widely for survival studies of juvenile salmonids. Survival and travel time through the study reach was compared between fish with either tag type in an area of high predation in the Snake and Columbia rivers, Washington. An additional group of fish affixed with neutrally-buoyant dummy external tags were implanted with passive integrated transponder (PIT) tags and recovered further downstream to assess external tag retention and injury. There were no significant differences in survival to the first detection site, 12 river kilometers (rkm) downstream of release. Travel times were also similar between groups. Conversely, externally-tagged fish had reduced survival (or elevated tag loss) to the second detection site, 65 rkm downstream. In addition, the retention study revealed that tag loss was first observed in fish recaptured approximately 9 days after release. Results suggest that this new tag may be viable for short term (<8 days) single-dam turbine-passage studies and under these situations, may alleviate the turbine passage-related bias encountered when using internal tags, however further research is needed to confirm this.