Prairie Naturalist D.A. Gravenhof, M.R. Wuellner, M.J. Fincel, and C.W. Goble 2023 No. 55 77 2023 PRAIRIE NATURALIST 1:77–84 Evaluation of Two Surgery Techniques for Surgical Implantation of Acoustic Transmitters in Juvenile Chinook Salmon Oncorhynchus tshawytscha Dylan A. Gravenhof1*, Melissa R. Wuellner2, Mark J. Fincel1, Cameron W. Goble1,3 Abstract – Surgically implanting a transmitter into a fish for telemetry studies can have potential effects on the growth and survival of the tagged individuals, but results are often variable based on species, size of fish, and the surgical techniques used. This study evaluated two surgery techniques for juvenile Oncorhynchus tshawytscha Walbaum (Chinook Salmon): the traditional sutured method and a relatively novel suture-less method where the incision is left open. Four replicate tagging trials were conducted, with each trial including 100 randomly chosen Chinook Salmon (50 control; 25 for each of the two surgery methods). Study fish were anesthetized and had a Innovasea® V5 dummy transmitter surgically implanted into the body cavity. At the completion of the 29-day trials, study fish were euthanized and assessed based on wound redness and healing at the incision site. For analyses, all the fish were pooled across the four trials (n = 197) and grouped by surgery type: sutured (n = 100) and suture-less (n = 97). Two-sample independent t-tests were conducted for both wound healing and redness scores between the two surgery groups. The sutured group had better scores for both wound healing (t = −10.68, df = 150, p = <0.001) and wound redness (t = −7.60, df = 154, p = <0.001) when compared to the suture-less group. The results of this study supports the use of the traditional surgical method that uses suture material to close the incision. These results contradict some recent literature that identifies the suture-less method as being more appropriate, which suggests that the effects of tag implantation may be highly variable based on surgical method used as well as the species and size of fish being studied. Introduction Acoustic telemetry has become a widely used tool to study fish ecology, including movement, habitat use, predator-prey interactions, post-stocking survival (e.g., Hyvarinen and Rodewald 2013; Larocque et al. 2020; Leber and Blankenship 2011), and how these behaviors are influenced by the environment (Capra et al. 2017; Cooke et al. 2004). One concern that comes with using acoustic telemetry is that this technology requires a transmitter be surgically implanted into the body cavity of a fish, which may negatively influence fish physiology and alter fish behavior (Wilson et al. 2016). Many published studies have focused on the effects of tag implantation on fish growth and survival (Brown et al. 2011; Jepsen et al. 2008; Klinard et al. 2018), but results are often variable, which suggests that a tagging evaluation prior to any telemetry study is warranted. For juvenile Oncorhynchus tshawytscha Walbaum (Chinook Salmon), previous research indicates that impacts of acoustic transmitter implantation may be size dependent, with more negative impacts to growth and survival noted for smaller individuals (80–109 mm Fork Length; Brown et al. 2011). In contrast, larger adult fish have shown no long-term effects on growth or survival due to acoustic transmitter implantation (Hubbard et al. 2021). 1South Dakota Department of Game, Fish and Parks, Missouri River Fisheries Center, 20641 SD HWY 1806, Fort Pierre, South Dakota 57532, USA. 2University of Nebraska at Kearney, Department of Biology, 2401 11th Ave., Kearney, Nebraska 68849, USA. 3Alberta Environment and Protected Areas, 530-08 Street South, Lethbridge, Alberta T1J 2J8, Canada. Associate Editor: Mark Pegg, School of Natural Resources, University of Nebraska, Lincoln, NB. Prairie Naturalist D.A. Gravenhof, M.R. Wuellner, M.J. Fincel, and C.W. Goble 2023 No. 55 78 The potential negative effects on growth and post-surgery survival are likely related to both the species and size of fish under consideration. The effects of surgery and transmitter implantation have been studied in a variety of fish families including: Percidae (Hayden et al. 2014; Weinz et al. 2020); Acerpenseridae (Auer 1999; Counihan and Frost 1999); Salmonidae (Deters et al. 2010; Thorstad et al. 2005); Centrachidae (Cooke et al. 2003); and many others (Gravenhof et al. 2020; Holbrook et al. 2012). Smaller fish are often more affected by tag implantation than larger fish due to an increased tag burden on the body (Brown et al. 2011; Hubbard et al. 2021). Effects of tag implantation likely differ among species due to differences in morphological characteristics. For example, Gravenhof et al. (2020) found surgically implanting transmitters into the ventral side of adult Dorosoma cepedianum Lesueur (Gizzard Shad) to be more difficult than some other species because it required prolonged surgery duration and cutting two-three rib bones to access the abdominal ca vity of the fish. How the incisions for tag implantation are closed may be another factor that influences healing and ultimately the survival of fish. The most common incision closure method uses monofilament suture material to close the wound and promote quicker healing and higher tag retention rates (Wagner and Cooke 2005). Adherence to recommended incision closure methods can minimize complications and fish discomfort and promote quicker healing (Mulcachy 2003). Some drawbacks of this recommended technique include increased inflammation, delayed wound healing, and tearing of the skin (Schoonyan et al. 2017; Wagner et al. 2000) due to its invasive nature. One alternative approach, the suture-less method, is a relatively novel technique that follows similar protocols for incision and tag insertion but does not require a suture to close the wound, rather the wound is left open. Various studies using the suture-less method have observed quicker healing rates, reduced inflammation, and improved tag retention when compared to the “traditional” sutured method (Huysman et al. 2020; Kelican et al. 2021). However, studies investigating the suture-less method are limited, with most published literature focusing on Oncorhynchus mykiss Walbaum (Rainbow Trout) and Salmo trutta Linnaeus (Brown Trout), and with adult fish rather than growing juvenile fish (Huysman et al. 2020; Kelican et al. 2021; Kientz et al. 2021). Understanding the appropriate methods for surgical implantation of transmitters and the potential effects of implantation is crucial for ensuring that fish with an implanted transmitter both survive and behave similarly to untagged individuals when conducting a study that utilizes acoustic telemetry. Movements and habitat use of juvenile Chinook Salmon are commonly studied using acoustic telemetry (Anglea et al. 2004; Hinke et al. 2005; Mc- Michael et al. 2006). Thus, understanding the effects and efficacy of different implantation methods can inform future studies of this species across their range. This study evaluated two surgical techniques (traditional sutured method and novel suture-less method) to inform which method may be appropriate for tagging juvenile Chinook Salmon. Methods Egg collection and fish rearing The juvenile Chinook Salmon used in this study originated as eggs collected by the South Dakota Department of Game, Fish and Parks (SDGFP) at Whitlock Bay Spawning Station on Lake Oahe, South Dakota in October 2019 and 2020. After egg collection, eggs were fertilized and water hardened before being transported to Cleghorn Springs State Fish Hatchery in Rapid City, South Dakota. At the hatchery, the eggs were incubated and hatched into a flow-through system for rearing to the juvenile smolt stage. The flow-through rearing system at the hatchery consisted of 6-m diameter circular tanks with cement bottoms and Prairie Naturalist D.A. Gravenhof, M.R. Wuellner, M.J. Fincel, and C.W. Goble 2023 No. 55 79 stainless-steel walls with a water depth of ~0.86 m. The well water for this system has an average temperature of 11 °C, total hardness (CaCO3) of 360 mg/L, a pH of 7.6, and a total dissolved solids level of 390 mg/L (South Dakota Department of Game, Fish and Parks, Ft. Pierre, SD, 2022 unpubl. data). The juvenile Chinook Salmon were fed 3-mm BioVita Fry extruded feed (Bio-Oregon, Longview, Washington, USA) at feeding rates determined using the hatchery constant method (Butterbaugh and Willoughby 1967). The juvenile salmon were reared at a density of approximately 1 1.36 kg/m3. Trial design and surgery protocols Four replicate trials were completed for this project: two in 2020 and two in 2021. For each trial, 100 juvenile Chinook Salmon were randomly selected for inclusion in the trial (50 control; 25 for each of two surgery methods). Due to budgetary constraints, only 50 dummy transmitters were available for this study, and as such, a sample size of 50 tagged individuals was deemed sufficient for each trial. The study fish were first anesthetized using tricaine methane sulfonate (MS-222) to stage-4 anesthesia (i.e., loss of equilibrium, reflexes, and muscle tone with a slow but steady opercular rate; Summerfelt and Smith 1990). All study fish then received a unique fin clip to distinguish between control and treatment groups. All fish in the control group were then immediately returned to their rearing tanks for recovery. The fish selected for surgery were divided into two groups: sutured and suture-less surgery methods. Fish in both groups received an incision parallel to the ventral line of the fish that was approximately 5 mm long. Incisions were made using a size #15 disposable, sterile scalpel (Cynamed®). Fish then had an Innovasea® V5 dummy transmitter (0.65 g weight in air, 12.7 mm length, and 4.3 x 5.73 mm diameter) inserted into the body cavity toward the anterior part of the fish. Fish in the suture-less group were immediately released into recovery tanks following tag insertion, while fish in the sutured group had their incision secured with one suture using a tapered point needle (RB-1) and absorbable monofilament suture material (Securos Surgical® 5-0 Securocryl; Poliglecaprone 25). The fish were held temporarily in recovery tanks until they were able to regain equilibrium, before being returned to the rearing tanks. Surgical evaluation For each trial, fish were monitored for 29 d (excluding trial 3, which was only conducted for 20 d due to time constraints). While unlikely, a delayed suture hypersensitivity reaction may have been missed in the trial 3 group with a shorter duration. At the completion of the trial, fish were collected from the rearing tank and euthanized using a lethal dose of MS-222. Fish were identified by treatment group based on the presence of fin clips. Digital images were captured of the incision site and used to assess wound healing and redness (Fig. 1). Wound healing and redness were assessed based on a scoring scale designed by Huysman et al. (2020) as an adaptation of a method designed by Paukert et al. (2001; Table 1). Each image was scored by two blind readers, and the mean score between readers was used for overall analyses. Fish were also dissected to determine if the dummy transmitter had been retained in the body cavity through the end of the trial. Over the course of the four trials, three study fish died due to circumstances unrelated to the study (i.e., accidentally stepping on a tagged fish within the rearing tank), and these fish were ex cluded from analyses. All the surgery fish included in the study (n = 197) were pooled across the four trials and grouped by surgery type: sutured (n = 100) and suture-less (n = 97). A Jarque-Bera goodness-of-fit test was used to determine whether the sample data followed a normal distribution. Two-sample independent t-tests assuming unequal variances were conducted in Prairie Naturalist D.A. Gravenhof, M.R. Wuellner, M.J. Fincel, and C.W. Goble 2023 No. 55 80 Microsoft Excel® for both the wound healing and wound redness scores, to test for potential differences between the sutured and suture-less surgery groups. Additionally, a two-sample z-test for proportions was conducted in Microsoft Excel® to test for a potential difference in tag retention proportions between the sutured and suture-less surgery groups. Statistical significance was determined at α = 0.05 Results The juvenile Chinook Salmon randomly selected for inclusion in the trials had a wide range in size (90–181 mm in total length (TL) and 7–87 g in weight) but mean TL (139 mm; standard error [SE] = 1 mm) and mean weight (29 g; SE = 0.7 g) were comparable across trials. This range of weights provided tag burdens (ratio of tag weight to body weight of the fish) that ranged from 0.7–9.3%, but mean tag burden was 2.6% (SE = 0.1%). Tag retention for the sutured group was significantly greater than the suture-less group across the four trials (100 v 86%; z = 3.88, p <0.001). Results from the Jarque-Bera goodness-of-fit test indicated that the data were normally distributed for both the wound healing (X2 = 38.94, df = 2, p = <0.001) and wound redness (X2 = 16.17, df = 2, p = <0.001) scores. The mean wound healing score for the sutured group was 0.28 (SE = 0.04) but was 1.10 (SE = 0.07) for the suture-less group (Fig. 2); differences between the two groups were statistically significant (t = −10.68, df = 150, p = <0.001). Similarly, the mean wound redness score for the sutured group was 0.21 (SE = 0.04) but was 0.81 (SE = 0.07) for the suture-less treatment (Fig. 2), and both were statistically different from one another (t = −7.60, df = 154, p = <0.001). Discussion We found significantly higher tag retention rates and better wound healing and redness scores for the sutured method compared to the suture-less method. This contradicts some recent literature that has reported positive results of using a novel suture-less surgery technique (Huysman et al. 2020; Kelican et al. 2021). This difference in results could be explained by considering the life stage of study individuals. Previous published studies, such as Huysman et al. (2020) and Kelican et al. (2021), used adult fish when testing the Figure 1. Digital images of dummy tagged juvenile Chinook Salmon showing various stages of healing with assigned wound healing and redness score for each using the scoring criteria outlined in Table 1. (Photos by Dylan A. Gravenhof). Sutured method Wound healing = 0; Wound redness = 0 Suture-less method Wound healing = 2; Wound redness = 2 Prairie Naturalist D.A. Gravenhof, M.R. Wuellner, M.J. Fincel, and C.W. Goble 2023 No. 55 81 suture-less method, but our study used smaller, juvenile individuals. This difference could suggest that the utility of the suture-less method varies based on the size and life stage of study individuals. Our results support the use of a traditional surgical procedure that uses suture material to close the incision site post-operation (Adams et al. 1998; Anglea et al. 2004; Deters et al. 2010). However, these results were somewhat surprising given the sutured method did require longer handling times and more invasive procedures. The mean surgery duration (time from when the incision was made to the time the fish was released to the recovery tank) was 69 s for the sutured method and 17 s for the suture-less method. Our results suggest that even with a handling time approximately four times longer with the traditional sutured method, the pros of a properly closed incision outweigh the potential cons of a prolonged handling time. Some steps can be taken to mitigate any potential effects of the more invasive procedure including the use of different needle types, needle sizes, and suture material (Wagner et al. 2010). The smallest and least invasive needle should be used to easily penetrate the skin while minimizing cutting of the tissue (Von Fraunhofer and Chu 1997). Additionally, for most fish, including Chinook Salmon, absorbable monofilament is the recommended material in order to minimize tissue inflammation (Deters et al. 2010). By utilizing the appropriate surgical materials, our results suggest that the sutured method promotes better and quicker wound healing which may minimize any potential adverse effects of slightly increased handling times. Tag retention rates are also an important factor to consider when selecting a surgery method. Acoustic transmitters are often costly, and sample sizes of tagged individuals are often smaller than comparable studies utilizing cheaper technology (Sequeira et al. 2019). Our Table 1. Scoring criteria developed by Huysman et al. (2020) for wound redness and wound healing used to determine the surgery method promoting quickest and best healing rates. Wound healing Wound redness 0 Complete closure No redness present 1 Closure of < 50% Redness localized to incision/suture site 2 No closure Redness extended beyond incision/suture site Figure 2. Mean wound healing (A) and wound redness (B) scores for juvenile Chinook Salmon 20–29 days post-surgery using the scoring criteria outlined in Table 1. Prairie Naturalist D.A. Gravenhof, M.R. Wuellner, M.J. Fincel, and C.W. Goble 2023 No. 55 82 results did identify a significant difference in tag retentions between the two methods, which could be particularly concerning as any number of expelled transmitters has the potential to be a costly loss and negatively impact the overall results of an acoustic telemetry study. Of the two surgery methods compared in this study, the sutured technique provided the best tag retention rates, promoted the quickest wound healing, and reduced wound redness/ inflammation. One limitation of this study was relatively small sample sizes, but the results do align with what many consider the “traditional” method for surgically tagging juvenile salmonids. However, these results also contradict recent published literature that suggest sutureless surgery as a newer, better approach. These conflicting results suggest that consideration should be given to tagging protocols before starting a telemetry study. Tagging protocols may differ based on species and life stage of the fish and the type/size of the transmitter. A “onesize- fits-all” approach may not be appropriate when it comes to choosing a surgical method. Future studies should consider replicating this study with larger sample sizes, multiple species, and both juvenile and adult fish. Our study saw conflicting results with previous studies that used different species and life stages, which suggests that more investigation could be warranted. Additionally, comparing the suture-less method in sham versus actual tag implantation surgeries could also provide insight into proper tagging techniques. Acknowledgements The authors thank the staff at Cleghorn Springs State Fish Hatchery for their assistance in rearing the fish for this study and the logistical help in monitoring the study fish during the trials. The authors also thank the various biologists and technicians from the Ft. Pierre Regional Office of SDGFP for their assistance in conducting surgeries on the tagged fish. Funding for this project was provided by Federal Aid in Sportfish Restoration. Literature Cited Adams, N.S., D.W. Rondorf, S.D. Evans, and J. E. Kelly. 1998. Effects of surgically and gastrically implanted radio transmitters on growth and feeding behavior of juvenile Chinook Salmon. Transactions of the American Fisheries Society 127:128–136. Anglea, S.M., D.R. Geist, R.S. Brown, and K.A. Deters. 2004. Effects of acoustic transmitters on swimming performance and predator avoidance of juvenile Chinook Salmon. North American Journal of Fisheries Management 24:162–170. Auer, N.A. 1999. Population characteristics and movements of lake sturgeon in the Sturgeon River and Lake Superior. Journal of Great Lakes Research 25(2):282–293. Brown, R.S., R.A. Harnish, K.M. Carter, J.W. Boyd, K.A. Deters, and M.B. Eppard. 2011. An evaluation of the maximum tag burden for implantation of acoustic transmitters in juvenile Chinook Salmon. North American Journal of Fisheries Management 30(2):499–505. Butterbaugh, G.L., and H. Willoughby. 1967. A feeding guide for Brook, Brown, and Rainbow trout. Progessive Fish-Culturist 29:210–215. Capra, H., L. Plichard, J. Berge, H. Pella, M. Ovidio, E. McNeil, and N. Lamouroux. 2017. Fish habitat selection in a large hydropeaking river: Strong individual and temporal variations revealed by telemetry. Science of the Total Environment 578:109–120. Cooke, S.J., B.D.S. Graeb, C.D. Suski, and K.G. Ostrand. 2003. Effects of suture material on incision healing, growth, and survival of juvenile Largemouth Bass implanted with miniature radio transmitters: Case study of a novice and experienced fish surgeon. Journal of Fish Biology 62:1366–1380. Cooke, S.J., C.M. Blunt, and J.F. Schreer. 2004. Understanding fish behavior, distribution, and survival in thermal effluents using fixed telemetry arrays: A case study of Smallmouth Bass in a discharge canal during winter. Environmental Management 33:140–150. Prairie Naturalist D.A. Gravenhof, M.R. Wuellner, M.J. Fincel, and C.W. Goble 2023 No. 55 83 Counihan, T.D., and C.N. Frost. 1999. Influence of externally attached transmitters on the swimming performance of juvenile White Sturgeon. Transactions of the American Fisheries Society 128:965–970. Deters, K.A., R.S. Brown, K.M. Carter, J.W. Bond, M.B. Eppard, and A.G. Seaburg. 2010. Performance assessment of suture type, water temperature, and surgeon skill in juvenile Chinook Salmon surgically implanted with acoustic transmitters. Transactions of the American Fisheries Society 139:888–889. Gravenhof, D.A., H.A. Morey, C.W. Goble, M.J. Fincel, and J.L. Davis. 2020. Short term survival and tag retention of Gizzard Shad implanted with dummy transmitters. Journal of Fisheries Sciences 14(2):1–7. Hayden, T.A., C.M. Holbrook, D.G. Fielder, C.S. Vandergoot, R.A. Bergstedt, J.M. Dettmers, C.C. Krueger, and S.J. Cooke. 2014. Acoustic telemetry reveals large-scale migration patterns of Walleye in Lake Huron. PLoS One 9(12):1–19. Hinke, J.T., G.M. Watters, G.W. Boehlert, and P. Zedonis. 2005. Ocean habitat use in autumn by Chinook Salmon in coastal waters of Oregon and California. Marine Ecology Progress Series 285:181–192. Holbrook, S.C., W.D. Byars, S.D. Lamprecht, and J.K. Leitner. 2012. Retention and physiological effects of surgically implanted telemetry transmitters in Blue Catfish. North American Journal of Fisheries Management 32(2):276–281. Hubbard, J.A.G., B.E. Hickie, J. Bowman, L.E. Hrenchuk, P.J. Blanchfield, and M.D. Rennie. 2021. No long-term effect of intracoelomic acoustic transmitter implantation on survival, growth, and body condition of a long-lived stenotherm in the wild. Canadian Journal of Fisheries and Aquatic Sciences 78(2):173–183. Huysman, N., S. White, J. Kientz, J.M. Voorhees, and M.E. Barnes. 2020. Suture-less implantation of acoustic transmitters in two salmonids. International Journal o f Sciences 9(3):60–64. Hyvarinen, P., and P. Rodewald. 2013. Enriched rearing improves survival of hatchery-reared Atlantic Salmon smolts during migration in the River Tornionjoki. Canadian Journal of Fisheries and Aquatic Sciences 70(9):1386–1395. Jepsen, N., J.S. Mikkelsen, and A. Koed. 2008. Effects of tag and suture type on survival and growth of Brown Trout with surgically implanted telemetry tags in the wild. Journal of Fish Biology 72(3):594–602. Kelican, A.N., N. Huysman, L.A. Van Rysselberge, J.M. Voorhees, and M.E. Barnes. 2021. Assessment of a novel surgical technique for acoustic transmitter insertion. Open Journal of Veterinary Medicine 11:247–257. Kientz, J., N. Huysman, and M.E. Barnes. 2021. A comparison of cyanoacrylate to sutures for wound closure following acoustic transmitter insertion in Rainbow Trout. Aquaculture and Fisheries 6(5):513–518. Klinard, N.V., E.A. Halfyard, A.T. Fisk, T.J. Stewart, and T.B. Johnson. 2018. Effects of surgically implanted acoustic tags on body condition, growth, and survival in a small, laterally compressed forage fish. Transactions of the American Fisheries Society 147(4):749–757. Larocque, S.M., T.B. Johnson, and A.T. Fisk. 2020. Survival and migration patterns of naturally and hatchery-reared Atlantic Salmon (Salmo salar) smolts in a Lake Ontario tributary using acoustic telemetry. Freshwater Biology 65(5):835–848. Leber, K.M., and H.L. Blankenship. 2011. How advances in tagging technology improved progress in a new science: marine stock enhancement. Bethesda, Maryland, USA: American Fisheries Society Symposion 76:1–12. McMichael, G., G.E. Johnson, J. Vucelick, G. Ploskey, and T. Carlson. 2006. Use of acoustic telemetry to assess habitat use of juvenile Chinook Salmon and Steelhead at the mouth of the Columbia River. PNNL-15575. Richland, Washington, USA: Pacific Northwest National Laboratory. Mulcachy, D.M. 2003. Surgical implantation of transmitters into fish. Institute for Laboratory Animal Research Journal 44:295–306. Paukert, C.P., P.J. Chavala, B.L. Heikes, and M.L. Brown. 2001. Effects of implanted transmitter size and surgery on survival, growth, and wound healing of Bluegill. Transactions of the American Fisheries Society 125:707–714. Prairie Naturalist D.A. Gravenhof, M.R. Wuellner, M.J. Fincel, and C.W. Goble 2023 No. 55 84 Sequeira, A.M.M., M.R. Heupel, M.A. Lea, V.M. Eguiluz, C.M. Duarte, M.G. Meekan, M. Thums, H.J. Calich, R.H. Carmichael, D.P. Costa, L.C. Ferreira, J. Fernandez-Gracia, R. Harcourt, A.L. Harrison, I. Jonsen, C.R. McMahon, D.W. Sims, R.P. Wilson, and G.C. Hays. 2019. The importance of sample size in marine megafauna tagging studies. Ecological Applications 29(6):1344–1360. Schoonyan, A., R.T. Kraus, M.D. Faust, C.S. Vandergoot, S.J. Cooke, H.A. Cook, T.A. Hayden, and C.C. Kreuger. 2017. Estimating incision healing rate for surgically implanted acoustic transmitter from recaptured fish. Animal Biotelemetry 5(1):1–8. Summerfelt, R.C., and L.S. Smith. 1990. Anesthesia, surgery, and related techniques. Pp. 213–272, In C.B. Schreck, and P.B. Moyle (Eds.) Methods for Fish Biology. Bethesda, MD, USA: American Fisheries Society. Thorstad, E.B., F. Okland, and B. Finstad. 2005. Effects of telemetry transmitters on swimming performance of adult Atlantic Salmon. Journal of Fish Biology 57(2):531–535. Von Fraunhofer, J.A., and C.C. Chu. 1997. Surgical needles. Pp. 25–38, In Chu, C.C., J.A. Fraunhofer, and H.P. Greisler (Eds.) Wound closure biomaterials and devices. CRC Press: Boca Raton, FL, USA. Wagner, G.N., E.D. Stevens, and P. Byrne. 2000. Effects of suture pattern on surgical wound healing in Rainbow Trout. Transactions of the American Fisheries Society 129:1196–1205. Wagner, G.N., and S.J. Cooke. 2005. Methodological approaches and opinions of researchers involved in the surgical implantation of telemetry transmitters in fish. Journal of Aquatic Animal Health 17:160–169. Wagner, G.N., S.J. Cooke, R.S. Brown, and K.A. Deters. 2010. Incision closure and surgery. Pp. 53–68 In R.S. Brown, S.J. Cooke, G.N. Wagner, and M.B. Eppard (Eds.) Methods for surgical implantation of acoustic transmitters in juvenile salmonids. U.S. Army Corps of Engineers, Portland District. Weinz, A.A., J.K. Matley, N.V. Klinard, A.T. Fisk, and S.F. Colborne. 2020. Identification of predation events in wild fish using novel acoustic transmitters. Animal Biotelemetry 8(28):1–14. Wilson, A.D.M, T.A. Hayden, C.S. Vandergroot, R.T. Kraus, J.M. Dettmers, S.J. Cooke, and C.C. Krueger. 2016. Do intracoelomic telemetry transmitters alter the post-release behavior of migratory fish? Ecology of Freshwater Fish 26(2):292–300.