delta smelt tagging

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Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ujfm20 Download by: [University of California Davis] Date: 14 September 2016, At: 05:54 North American Journal of Fisheries Management ISSN: 0275-5947 (Print) 1548-8675 (Online) Journal homepage: http://www.tandfonline.com/loi/ujfm20 Feasibility of Passive Integrated Transponder and Acoustic Tagging for Endangered Adult Delta Smelt Richard M. Wilder, Jason L. Hassrick, Lenny F. Grimaldo, Marin F. D. Greenwood, Shawn Acuña, Jillian M. Burns, Donna M. Maniscalco, Patrick K. Crain & Tien-Chieh Hung To cite this article: Richard M. Wilder, Jason L. Hassrick, Lenny F. Grimaldo, Marin F. D. Greenwood, Shawn Acuña, Jillian M. Burns, Donna M. Maniscalco, Patrick K. Crain & Tien- Chieh Hung (2016) Feasibility of Passive Integrated Transponder and Acoustic Tagging for Endangered Adult Delta Smelt, North American Journal of Fisheries Management, 36:5, 1167-1177, DOI: 10.1080/02755947.2016.1198287 To link to this article: http://dx.doi.org/10.1080/02755947.2016.1198287 Published online: 13 Sep 2016. Submit your article to this journal View related articles View Crossmark data

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Page 1: Delta Smelt Tagging

Full Terms & Conditions of access and use can be found athttp://www.tandfonline.com/action/journalInformation?journalCode=ujfm20

Download by: [University of California Davis] Date: 14 September 2016, At: 05:54

North American Journal of Fisheries Management

ISSN: 0275-5947 (Print) 1548-8675 (Online) Journal homepage: http://www.tandfonline.com/loi/ujfm20

Feasibility of Passive Integrated Transponder andAcoustic Tagging for Endangered Adult Delta Smelt

Richard M. Wilder, Jason L. Hassrick, Lenny F. Grimaldo, Marin F. D.Greenwood, Shawn Acuña, Jillian M. Burns, Donna M. Maniscalco, Patrick K.Crain & Tien-Chieh Hung

To cite this article: Richard M. Wilder, Jason L. Hassrick, Lenny F. Grimaldo, Marin F. D.Greenwood, Shawn Acuña, Jillian M. Burns, Donna M. Maniscalco, Patrick K. Crain & Tien-Chieh Hung (2016) Feasibility of Passive Integrated Transponder and Acoustic Tagging forEndangered Adult Delta Smelt, North American Journal of Fisheries Management, 36:5,1167-1177, DOI: 10.1080/02755947.2016.1198287

To link to this article: http://dx.doi.org/10.1080/02755947.2016.1198287

Published online: 13 Sep 2016.

Submit your article to this journal

View related articles

View Crossmark data

Page 2: Delta Smelt Tagging

ARTICLE

Feasibility of Passive Integrated Transponder and AcousticTagging for Endangered Adult Delta Smelt

Richard M. Wilder*ICF International, 630 K Street, Suite 400, Sacramento, California 95814, USA

Jason L. HassrickICF International, 101 Lucas Valley Road, Suite 260, San Rafael, California 94903, USA

Lenny F. GrimaldoICF International, 620 Folsom Street, Suite 200, San Francisco, California 94107, USA

Marin F. D. GreenwoodICF International, 630 K Street, Suite 400, Sacramento, California 95814, USA

Shawn AcuñaMetropolitan Water District of Southern California, 1121 L Street, Suite 900, Sacramento,California 95814, USA

Jillian M. BurnsICF International, 620 Folsom Street, Suite 200, San Francisco, California 94107, USA

Donna M. ManiscalcoICF International, 75 East Santa Clara Street, San Jose, California 95113, USA

Patrick K. CrainICF International, 630 K Street, Suite 400, Sacramento, California 95814, USA

Tien-Chieh HungDepartment of Biological and Agricultural Engineering, University of California–Davis,One Shields Avenue, Davis, California 95616, USA

AbstractConservation and recovery of endangered species requires timely and defensible data to predict their responses

to management actions. In the Sacramento–San Joaquin Delta, the population of Delta Smelt Hypomesus transpa-cificus, a species of management concern, has declined to a record low. Alternative research strategies are nowsought to determine the efficacy of management actions. In this study, we assessed the feasibility of tagging culturedadult Delta Smelt as a potential surrogate for wild fish in field experiments. Preliminary experiments determinedthat anesthesia of Delta Smelt in 35 mg/L AQUI-S 20E for 4 min best facilitated tagging. The 28-d survival of DeltaSmelt (n = 39) intracoelomically injected with passive integrated transponder (PIT) tags (8.4 mm, 0.03 g) was high(95%) and did not differ from untagged control fish; tag retention was 97%. Survival of Delta Smelt with injected(n = 40) and surgically inserted (n = 40) dummy acoustic transmitters (15.0 mm, 0.22 g) was significantly lower thanPIT-tagged and control fish, with only 60% surviving tag injection and 50% surviving surgical tag insertion.

*Corresponding author: [email protected] January 27, 2016; accepted May 25, 2016

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North American Journal of Fisheries Management 36:1167–1177, 2016© American Fisheries Society 2016ISSN: 0275-5947 print / 1548-8675 onlineDOI: 10.1080/02755947.2016.1198287

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Surviving fish had high tag retention (injected: 95%; surgically inserted: 100%). Although not quantified, observa-tional data suggested that the swimming ability of fish with acoustic tags was impaired. These results indicate thatcultured Delta Smelt injected with PIT tags provide resource managers with a readily available wild surrogate toexamine management actions in the delta. However, acoustic tags, which provide more detailed information onmovement patterns, must be made smaller to reduce effects on survival before they can be used successfully inDelta Smelt. Logistic regression suggested that achievement of high survival (>90%) would require a tag mass:body mass ratio below 0.02.

Efforts to protect and restore rare fish become increasinglychallenging when low population numbers prohibit the directassessment of management actions (Maxwell and Jennings2005). In California’s Sacramento–San Joaquin Delta, thefederally listed (USFWS 1993) Delta Smelt Hypomesus trans-pacificus has experienced a substantial reduction in populationsize. As a result, the beneficial outcomes of conservationefforts remain uncertain. This is of particular concern forState Water Project and Central Valley Project water opera-tions, which supply water to more than 25 million Californiansand support a multibillion dollar agricultural economy,because they are mandated to minimize the impacts to DeltaSmelt during periods when individuals are vulnerable toentrainment (Kimmerer 2008; Grimaldo et al. 2009).

New technologies and new applications of existing technolo-gies have emerged in recent years to enhance the study of fishesof special conservation concern, including environmental DNA(Jerde et al. 2011; Takahara et al. 2012; Thomsen et al. 2012a,2012b; Rees et al. 2014; Goldberg et al. 2015), hydroacoustics(Winfield et al. 2009), and underwater camera technology(Feyrer et al. 2013). These technologies are being applied toprovide nonlethal detection and estimates of distribution andabundance of rare fish and aquatic organisms. However, theirability to provide information on survival of individual fish atspecific locations is limited. In contrast, tracking studies usingdeployable microtransmitters or transponders (collectively tags)are well suited for this purpose (Voegeli et al. 2001; Heupel et al.2006; Hassrick et al. 2010; Michel et al. 2013).

The application of established tagging methods for remotedetection of Delta Smelt has been limited by their small bodysize and sensitivity to handling (Bennett 2005; Sommer et al.2011). However, the feasibility of tag implantation in culturedDelta Smelt can now be evaluated with the advent of smallertags (Deng et al. 2015) and a culture facility that annuallyproduces tens of thousands of Delta Smelt for conservationand research purposes (Lindberg et al. 2013). To date, the onlypublished, field-based study of marked, cultured Delta Smeltused external calcein and photonic marks (Castillo et al.2012). Calcein and photonic marks are relatively inexpensive(allowing for large sample sizes) but require recapture ofmarked individuals to assess survival. At the time of Castilloet al. (2012), physical marking studies were the only optionfor assessing survival because feasibility studies of PIT andacoustic tagging found significant mortality of tagged Delta

Smelt (K. Eder, California State University, Sacramento, andJ. Morinaka, California Department of Fish and Wildlife,unpublished data).

Our study assessed the feasibility of intracoelomicallyimplanting Delta Smelt with two tag types: PIT tags andinjectable Juvenile Salmon Acoustic Telemetry System(JSATS) acoustic tags (Deng et al. 2015). We monitored tag-related mortality and tag retention of tagged Delta Smelt for28 d compared with untagged controls. Our study questionswere as follows:

1. How did tag retention and tag-related survival of DeltaSmelt injected with PIT tags compare with controls?

2. How did tag retention and tag-related survival of DeltaSmelt with acoustic tags injected or surgically insertedcompare with controls?

3. How did tag retention and tag-related survival of DeltaSmelt implanted with PIT tags compare with survival ofDelta Smelt implanted with acoustic tags?

Because the anesthetic used in this study, AQUI-S 20E, hadnever been used on Delta Smelt before, we also asked thefollowing:

4. What is the optimal concentration and duration of AQUI-S20E to maximize fish survival while minimizing muscleactivity and recovery time?

METHODSThis study was conducted from January to April 2015 at the

University of California, Davis (UC Davis), Fish Conservationand Culture Laboratory in Byron, California. Cultured DeltaSmelt were obtained from the Fish Conservation and CultureLaboratory. Production and feeding regimes of Delta Smeltwere based on methods previously described by Lindberget al. (2013). Fish >70 mm FL were included in this study(mean ± SD length = 78.2 ± 4.6 mm; mass = 3.98 ± 0.87 g),which represents the upper 50th percentile of the adult sizedistribution collected in long-term field monitoring surveys(http://www.dfg.ca.gov/delta/projects.asp?ProjectID=SKT).

We took several steps to minimize handling stress andmaintain consistency among experimental treatments. Worksurfaces were coated with 10% Stress Coat (Mars Fishcare

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North America, Chalfont, Pennsylvania) for all tagging proce-dures. After experimental manipulation, fish were kept inblack, 1.5-m-diameter, 852-L outdoor holding tanks coveredwith black mesh. Fish were held in a recirculating system withidentical holding tanks situated together so that they experi-enced the same ambient conditions and water quality. Waterflow to each tank was kept at 8 L/min to keep the turnover rateof water in each tank under 2 h. Water quality from thesettlement tank of the recirculating system was measuredtwice per week. Water quality tests included dissolved oxygen(%), pH, total ammonia nitrogen, nitrite, nitrate, salinity, andtemperature. All water leading to the tanks was pumped froma sump tank through a particle filter, then through a heat pumpfeeding into an ultraviolet sterilizer prior to entering the fishholding tanks. Water exiting the holding tanks drained to asettlement tank, which then overflowed back into the sump.Feeding, debris removal, and fish survival monitoring wereperformed daily. Moribund or diseased individuals with a lowprobability of survival were euthanized according to the UCDavis Institutional Animal Care and Use Committee regula-tion. Water temperature during the study ranged from 11.4°Cto 13.4°C, and dissolved oxygen ranged from 91.3% to 95.9%.

Anesthesia experiments.—Because we anticipated that theresults of this study could be used for future field releases ofDelta Smelt, we followed the anesthesia guidance of theCalifornia Department of Fish and Wildlife. This guidancerecommends using the anesthetic AQUI-S 20E (AquaTacticsFish Health, Kirkland, Washington) on fish to be released inthe wild when a 21-d withdrawal period cannot be met. To ourknowledge, AQUI-S 20E has never been used on Delta Smelt.Therefore, as an initial part of this study, we established thedose and duration of AQUI-S 20E necessary for successfultagging. AQUI-S 20E is in the process of being licensed bythe Food and Drug Administration, and its use is allowed onlythrough participation in the compassionate InvestigationalNew Animal Drug, Exemption 11-741 (Bowker 2015).

As part of the AQUI-S 20E evaluation, we conducted adosing experiment to determine the optimal concentration toachieve anesthesia with minimal muscle activity for tagimplantation. Three concentrations (20, 30, and 35 mg/L)were tested with 12 fish/treatment. Mean fork length was notsignificantly different among treatments (ANOVA: F2, 35 =2.52, P = 0.10). Anesthesia time (i.e., duration required toachieve little or no muscle activity) was recorded for fishimmersed in a black, 18.9-L bucket containing anesthesiabath and 0.05% Stress Coat. Recovery time (i.e., durationrequired to regain upright position with normal swimmingmotion) was recorded after a fish was returned to a bucketwith no anesthesia. Recovered fish were carefully returned toholding tanks and held for 23 d. Differences in anesthesia timeand recovery time among dose treatments were assessed usinga one-way ANOVA and post hoc Bonferroni-corrected multi-ple comparisons. Significant differences in percent survivalafter 23 d were defined as nonoverlap of bootstrapped 95%

confidence intervals, these having been generated from the2.5th and 97.5th percentiles of the percentage surviving ineach of 10,000 resamples (with replacement) of the originaldata (Brown et al. 2012).

Despite being inactive in the anesthesia bath during thedosing experiment, some individual Delta Smelt were stillactive when handled. Therefore, a second experiment wasconducted to determine the effect of increased anesthesiabath duration on fish activity and recovery time. This experi-ment held constant a 35 mg/L AQUI-S 20E dose and fixedbath duration of 3, 4, and 5 min (n = 12 fish/treatment). Meanlength was not significantly different among treatments(ANOVA: F2, 35 = 0.69, P = 0.51). The 35-mg/L dose wasselected because it previously provided the shortest time toanesthesia while providing full postanesthesia recovery andsurvival. In addition to recording recovery time and survival,counts of body muscle twitches during handling were recordedfor all treatments. Survival of recovered fish was monitoredfor only 6 d, given the low mortality (0–8% depending ontreatment) observed in the dosing experiment. All other meth-ods were identical to the dosing experiment. Statistical ana-lyses were similar to those described for the dosingexperiment except that response variables included recoverytime, body muscle twitch rate (twitches/min), and survival.

Tagging experiment.—Three tag implantation treatments andfive controls were used to assess survival and tag retention ofcultured Delta Smelt (Table 1). Based on results of the anesthesiaevaluations, fish were anesthetized for 4.5 to 5 min in a 35 mg/LAQUI-S 20E solution, randomly assigned a tag treatment andtagger, and measured for length and mass (except for completecontrols).Mean fork length was not significantly different amongtreatments (ANOVA: F6, 276 = 0.94, P = 0.46), although completecontrols were not included in the analysis. Tag implantationtreatments included PIT tag injection (n = 39), acoustic taginjection (n = 40), and acoustic tag surgical implantation (n =40). The tag implantation site for all treatments wasapproximately two-thirds of the way down the body (dorsal toventral) and 2–3 mm anterior to the distal end of the pectoral fin.The PIT tags (HPT8; Biomark, Boise, Idaho) were injectedintracoelomically using a sterilized 16-gauge-needle syringeimplanter (MK165; Biomark, Boise, Idaho). Tags weighed 0.03g in air and were 1.4 × 8.4 mm. The needle was inserted at ashallow angle (~15°) with the bevel facing the body (down). Foracoustic tag injections and surgical implantation, we useddummy tags of the smallest available JSATS tags produced bythe Pacific Northwest National Laboratory (see Deng et al. 2015;0.22 g in air, 3.4 × 15.0 mm). Each dummy tag contained a PITtag to facilitate identification. Dummy acoustic tags wereinjected using sterilized 8-gauge needles (Vita Needle,Needham, Massachusetts; see Cook et al. 2014). The needlewas inserted at a shallow angle (~15°) with approximatelyone-third to one-half of the bevel length into the body andneedle bevel facing up. Once inserted, the needle was rotated180° prior to tag injection to ensure proper insertion into the body

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(Bryson et al. 2013). Early trials found that successfulimplantation with a 90° rotation was difficult, despite thereduced extent of wounds reported for this technique by Brysonet al. (2013). The acoustic surgery treatment involved making a3–4-mm incision with a sterilized restricted-depth scalpel (15°,3 mm, Sharpoint, Reading, Pennsylvania) parallel to musclestriation to minimize trauma, followed by manual tag insertion.No glue or sutures were used to close the wound for anytreatment or control.

The controls included all levels of the handling procedureof tagged fish to identify all potential sources of direct andindirect mortality of the tagging process as follows: (1) com-plete control fish (n = 40) were moved directly from a stocktank to a treatment tank and were not otherwise handled, (2)anesthesia control fish were anesthetized and measured but nottagged (n = 41), (3) injection control fish (PIT, n = 40;acoustic, n = 37) were handled per procedures of the taginjection but a tag was not injected after the skin was perfo-rated, and (4) acoustic surgery control fish (n = 40) werehandled per procedures of the tagging surgery but a tag wasnot implanted after the incision was made.

Four taggers conducted all the tagging and fish handling.Each tagger had a minimum of 15 h of training and practicedeach tagging technique on a minimum of 50 fish before theexperiment. During the experiment, two taggers were assigneda treatment in a predetermined random order until all treat-ments were conducted once, excluding the complete control.The two taggers were then replaced by two new taggers andthe order of treatments was repeated. Tagging pairs switchedafter every round until all fish had been processed. For thecomplete control, 20 fish were moved from the stock tank tothe treatment tank at the end of rounds 20 and 40.

After tagging or control procedures had been applied, fishfrom all treatments except the complete control were placed ina recovery bucket for a minimum of 15 min or until fullyrecovered. After recovery, fish were placed in holding tanksdivided by treatment. Tank effects were assumed to be zero,consistent with other studies in which tanks were set upidentically in a recirculating system (Bolland et al. 2009).

Oxytetracycline was added prophylactically to all tanks for 4d following handling to reduce the risk of infection. In addi-tion to routine feeding and tank cleaning, we assessed swim-ming behavior and mortality of fish visible in the tank,monitored for signs of infection, and scanned tanks forexpelled tags daily for 28 d.

We compared the survival of Delta Smelt at 14 and 28 damong treatments by examining the overlap of 95% confi-dence intervals from bootstrapped data (n = 10,000 resam-ples), similar to the AQUI-S 20E concentration dosingexperiment. Tag retention data would have been analyzed inthe same way, but there ultimately were insufficient tagsexpelled to justify statistical analysis.

After 28 d, all surviving fish were euthanized with a lethaldose of buffered MS-222 (tricaine methanesulfonate; 400 mg/mL) within 1 h to avoid biasing gut fullness estimates. Fishwere identified by tag code, weighed, measured, sexed, andchecked for external or internal lesions and gut fullness.Condition factor, a quantitative index of individual fish con-dition based on the ratio of mass to length, was calculated foreach fish, with tag mass removed, as follows:

Condition factor ¼ mass� 100;000ð Þ=fork length3; (1)

where mass is measured in grams and fork length in millimeters.Condition factor was compared among treatments using a

one-way ANOVA and post hoc Bonferroni-corrected multiplecomparisons. Only fish that survived to the end of the experi-ment were included in the analysis to avoid confoundingresults with tissue decomposition of fish that died during theexperiment, despite tanks being checked daily.

External and internal lesions were evaluated qualitativelyusing guidelines from Goede and Barton (1990) to assess thecondition and health of Delta Smelt. External lesions includedcontusions, hematomas, infections, and injection or incision sitecondition. Internal lesions included contusions and evidence ofhemorrhaging. Gut fullness, a measure of stress and spaceavailable in the coelom, was visually estimated in the

TABLE 1. Experimental design of the tagging experiment. The handling for the complete control was limited to transfer by net from the stock tank to thetreatment tank.

Treatment AnesthesiaLength or massmeasurement Tag type Skin perforation Tag insertion

Complete control No No None None NoneAnesthesia control Yes Yes None None NonePIT tag injection control Yes Yes None Injection NonePIT tag injection Yes Yes PIT Injection InjectionAcoustic tag injection control Yes Yes None Injection NoneAcoustic tag injection Yes Yes Acoustic Injection InjectionAcoustic tag surgery control Yes Yes None Incision NoneAcoustic tag surgery Yes Yes Acoustic Incision Manual

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translucent intestines and recorded in three categories: full,partial, and empty. The proportions of fish with external lesions,internal lesions, and the three different categories of gut fullnesswere compared among treatments using the same bootstrappingprocedure that was used to compare the proportion of fishsurviving in each treatment. Only fish that survived to the endof the experiment were included in the analysis.

Following the recommendation of Archdeacon et al.(2009), the probability of survival of tagged Delta Smelt as acontinuous function of fish size was estimated using logisticregression. In order to combine data from PIT and acoustic tagtreatments, fish size was expressed as tag burden (tag massdivided by body mass). The logistic regression’s formula is

Yi ¼ eðβ0þβ1XiÞ= 1þ eðβ0þβ1XiÞh i

; (2)

where Yi = the probability of survival of fish i on day 28, β0 = theregression intercept, β1 = the regression slope, and Xi = the inde-pendent variable (tag burden) of fish i (Archdeacon et al. 2009).

RESULTS

Anesthesia ExperimentsFor the dosing experiment, time to anesthesia was significantly

different among treatments (ANOVA: F2, 34 = 13.99, P < 0.0001);pairwise comparisons revealed that mean time to anesthesia wassignificantly longer for the 20 mg/L treatment than the 30 and 35mg/L treatments (Bonferroni t-test = 2.53,P< 0.05), butmean timeto anesthesia did not differ between 30 and 35mg/L concentrations(Table 2). Mean recovery time showed an increasing trend from4.59 ± 2.65 min (mean ± SD) in the 20 mg/L dose to 6.01 ± 1.94min in the 35 mg/L dose, but differences in means were notsignificant (ANOVA: F2, 35 = 1.64, P = 0.21). Survival over 23 dafter anesthesia was high (92–100%) in all treatments and was notsignificantly different based on overlapping bootstrapped 95%confidence intervals from 10,000 resamples of the original data.One mortality occurred at 5 d in the 20 mg/L treatment and nomortalities occurred in the 30 or 35 mg/L treatments.

For the anesthesia duration experiment, the rate of bodymuscle twitches was inversely related to anesthesia duration,but differences among 3-, 4-, and 5-min treatments were notsignificant because of high variation within treatments

(ANOVA: F2, 35 = 2.80, P = 0.075; Table 3). Mean recoverytime did not differ among treatments (ANOVA: F2, 35 = 1.85,P = 0.17). Survival over the 6 d after anesthesia was high(92–100%) among treatments and was not significantly dif-ferent based on overlapping bootstrapped 95% confidenceintervals from 10,000 resamples of the original data. Onemortality occurred after 6 d in the 4-min treatment.

Tagging ExperimentSurvival of Delta Smelt in the PIT tag injection treatment

(95% after 14 and 28 d) was significantly higher than survivalin both acoustic tag injection (63% after 14 d; 50% after 28 d)and acoustic tag surgery (60% after 14 and 28 d) treatments,based on nonoverlapping bootstrapped 95% confidence inter-vals from 10,000 resamples of the original data (Figures 1, 2).However, 14-d and 28-d survival did not significantly differbetween acoustic tag injection and acoustic tag surgery treat-ments. Delta Smelt implanted with acoustic tags exhibitedimpaired swimming ability throughout the 28-d experiment,with fish generally moving very slowly or remaining station-ary on the tank bottom, whereas PIT-tagged fish swam vigor-ously and similarly to control fish.

There was no significant difference in survival between thePIT tag injection control (100% after 14 and 28 d) and PIT taginjection treatments (95% after 14 and 28 d; Figures 1, 2).There was no significant difference in 14-d survival betweenthe acoustic tag injection control (89%) and acoustic taginjection treatments (63%), but 28-d survival of fish in theacoustic injection tag treatment (50%) was significantly lowerthan survival in the acoustic tag injection control (89%). The14- and 28-d survival in the acoustic tag surgery control (98%for both) was significantly higher than in the acoustic tagsurgery treatment (60% after 14 and 28 d; Figure 2).Survival in the PIT tag injection control and acoustic tagsurgery control was not different from survival in the anesthe-sia control (100% after 14 and 28 d), although survival in theacoustic tag injection control was significantly lower thansurvival in the anesthesia control after both 14 and 28 d.There was no difference in survival between the completecontrol (98% after 14 and 28 d) and anesthesia control.

There were 3 of 119 tags that were shed over the 28-dperiod; one was shed from a fish in the PIT tag injection

TABLE 2. Summary of the AQUI-S 20E dosing experiment. Anesthesia andrecovery times are presented as the mean (SD in parentheses). Survival wasmonitored for 23 d.

Anesthesiadose (mg/L) n

Anesthesiatime in minutes

Recovery timein minutes

Survival(%)

20 12 4.53 (1.77) 4.59 (2.65) 9230 12 2.70 (1.00) 4.89 (1.27) 10035 12 1.96 (0.50) 6.02 (1.94) 100

TABLE 3. Summary of the anesthesia duration experiment using a 35 mg/LAQUI-S 20E dose. Body muscle activity and recovery time data are presentedas the mean (SD in parentheses). Survival was recorded for 6 d.

Anesthesiaduration inminutes n

Body muscleactivity

(twitches/min)

Recoverytime inminutes

Survival(%)

3 12 8.8 (5.1) 11.81 (2.81) 1004 12 6.4 (5.5) 9.76 (2.92) 925 12 4.2 (3.3) 11.29 (2.38) 100

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treatment, and two were shed from fish in the acoustic taginjection treatment. No tags were shed from the acoustic tagsurgery treatment.

Mean condition factor ranged from 0.72 ± 0.08 (mean ± SD) inthe acoustic tag injection treatment to 0.80 ± 0.10 in the anesthe-sia control, but there was no significant difference in conditionfactor among treatments (ANOVA: F7, 269 = 1.65, P = 0.12)(Figure 3).

External lesions in Delta Smelt were most prevalent in theacoustic tag injection control (27%) and least prevalent in thePIT tag injection treatment (0%). There were several pairwisedifferences, defined as nonoverlapping bootstrapped 95% con-fidence intervals from 10,000 resamples of the original data, inexternal lesion prevalence among treatments (Figure 4),although none were intuitive or predicted. There were nosignificant differences among treatments in internal lesionprevalence.

Gut fullness results are presented here individually,although they are autocorrelated and should not be consideredindependent of each other. Regardless, they collectively pro-vide information related to the effects of tag treatments onDelta Smelt feeding. The acoustic tag surgery treatment had asignificantly greater proportion of fish with empty guts (25%)than the acoustic tag surgery control (3%) and the anesthesiacontrol (0%), with all other treatments and controls intermedi-ate (Figure 4). The acoustic tag surgery treatment (25%) andPIT tag injection control (25%) had a greater prevalence of

partially full guts than the acoustic tag surgery control (3%),with all other treatments and controls intermediate. The acous-tic tag surgery control (95%) had a significantly greater pro-portion of fish with full guts than the complete control (72%),PIT tag injection control (70%), acoustic tag injection treat-ment (63%), and acoustic tag surgery treatment (50%). Theacoustic tag surgery treatment also had a lower prevalence offull guts than the anesthesia control (85%), acoustic tag injec-tion control (82%), and PIT tag injection treatment (75%).

The probability of survival of tagged Delta Smelt was sig-nificantly inversely related to tag burden (β1 = –55.81 ± 13.39[mean ± SE]; Wald χ2 = 17.37, P < 0.0001; Figure 5). Over therange of tag burdens encountered in this study, the logisticregression predicted survival to vary from 96% with a tagburden of 0.6% to just below 20% with a tag burden of 8.7%.

DISCUSSIONThis study demonstrates that cultured adult Delta Smelt can

be successfully implanted with PIT tags. The 95% survivalrate of Delta Smelt injected with PIT tags was indistinguish-able from controls and was similar to survival rates describedfor other small fishes with low tag burdens (Bolland et al.2009). A previous unpublished experiment evaluating tageffects in Delta Smelt found 57% survival of small individualsinjected with 0.07-g PIT tags, resulting in an approximate 2%tag burden; the same unpublished experiment also found 84%

FIGURE 1. Daily survival of Delta Smelt in tagging treatments and controls.

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survival, with an approximate 1% tag burden, of larger indi-viduals (Morinaka, unpublished data). A separate unpublishedexperiment using slightly larger (0.11 g) PIT tags and surgicalimplantation found 66% survival with approximately 2.8% tagburden and 78% survival with approximately 1.6% tag burden(Eder, unpublished data). The higher survival with PIT tags inthe present study likely reflects a relatively small tag burden(average = 0.8%) and the small size of the tag itself, whichprobably had reduced direct effects (i.e., tissue or organdamage) and indirect effects (e.g., food ingestion and swim-ming behavior) on the Delta Smelt.

Survival of Delta Smelt implanted with acoustic tags viainjection needle or surgery was substantially lower than in

those implanted with PIT tags. The acoustic tag controlsexhibited relatively high survival after 28 d, suggesting thatthe approximate 4–8% tag burden in fish implanted withacoustic tags contributed to lower survival than in fish injectedwith PIT tags. Maintaining a probability of survival above90% in tagged Delta Smelt would require tag burdens of 2%or less (Figure 5).

The availability of controlled studies examining taggingeffects in other osmerids is limited. Clément et al. (2012)found 85% 14-d survival of Rainbow Smelt Osmerus mordaxtagged with 23-mm, 0.6-g PIT tags. These fish ranged from<155 mm to >180 mm FL, suggesting a tag burden of approxi-mately 1–2%. These results are generally consistent with thosein the present study. Juvenile salmonids appear to be lesssensitive to tag implantation than Delta Smelt. An approxi-mate 6–8% tag burden threshold has been observed for mini-mizing tagging effects in juvenile Atlantic Salmon Salmosalar (Lacroix et al. 2004), Coho Salmon Oncorhynchuskisutch (Chittenden et al. 2009), Chinook Salmon O. tsha-wytscha (Brown et al. 2010), and Sockeye Salmon O. nerka(Collins et al. 2013). Delta Smelt have a smaller coelom and amore slender body than salmonids, which likely contribute totheir greater tag sensitivity.

The probability of mortality from the acoustic tag injectionprocess in our study may have been increased by the relativelylarge perforation made by the 8-gauge needle. Bryson et al.(2013) found that a 90° rotation after a bevel-up insertionreduced the wound extent compared with rotating 180°,which suggests that minimizing needle rotation and movementwithin the body could mitigate some of the damage caused bythe large needle used for acoustic tag injections. On the other

FIGURE 2. Bootstrapped mean survival estimates (error bars show 95%confidence intervals) based on 10,000 resamples of the original data foradult Delta Smelt at 14 d and 28 d. Significant differences among treatmentsare denoted by different letters, determined by nonoverlapping confidenceintervals. Treatments were as follows: complete control (CC), anesthesiacontrol (AC), PIT tag injection control (PIC), PIT tag injection (PI), acoustictag injection control (AIC), acoustic tag injection (AI), acoustic tag surgerycontrol (ASC), and acoustic tag surgery (AS).

FIGURE 3. Final condition factor for fish that survived to the end of the studywith their tag still implanted, where applicable. The values are given as themean ± 1 SD. The treatment codes are defined in Figure 2. The sample sizevaried by treatment (CC: n = 39; AC: n = 41; PIC: n = 40; PI: n = 36; AIC: n =33; AI: n = 19; ASC: n = 38; AS: n = 24).

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hand, acoustic tag injection controls had relatively high survi-val (89%), again suggesting that tag burden (or tag insertion)was the main factor contributing to the lower survival after 28d in fish injected with acoustic tags.

Injection and surgical implantation of acoustic tags affectedDelta Smelt movement and survival in a way that could haveimportant implications for field trials. The mortality of fish withsurgically implanted acoustic tags was relatively high (n = 14)during the 6 d following tagging, but there were only two

additional mortalities in the subsequent 22 d of the experiment(Figure 1). This suggests that, if acoustic tags were surgicallyimplanted in Delta Smelt and individuals were held for at least6 d, mortality of fish surviving past 6 d would be relatively low,although sublethal effects (e.g., observed reduced swimmingability) must also be considered. In contrast, aside from thefirst day on which five mortalities occurred, acoustic tag injec-tion mortality rates were relatively constant throughout theexperiment, possibly because of chronic negative effects from

FIGURE 4. Necropsy visual comparisons of lesions (left panels) and gut fullness (right panels) across tagging treatments. The values are the 50th percentile(error bars show 95% confidence intervals) of bootstrapped estimates based on 10,000 resamples of the original data. Differing letters denote significantdifferences among treatments with nonoverlapping confidence intervals. Treatment codes are defined in Figure 2; sample sizes are listed in Figure 3. Althoughdata in the three right panels are not independent of one another, they are shown separately in the figure to facilitate visual interpretation.

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tag injection. Studies comparing injection and surgical implan-tation of tags in other fishes have also found a greater mortalityof fish with tag injection, likely as a result of internal organdamage from the needle (Baras et al. 1999, 2000; Archdeaconet al. 2009). However, we found that there was no difference inthe prevalence of internal lesions (mainly evidence of hemor-rhaging) between fish that survived to the end of the experimentwith acoustic tag injections and surgeries (Figure 4).

The implantation of acoustic tags by injection or surgeryresulted in significantly higher mortality rates after 28 d than inthe controls. The 50–60% survival rates render the JSATS tagstested in the present study unsuitable for field studies of DeltaSmelt response to management actions. There was some evi-dence that feeding was impaired in both acoustic tag treatments,as measured by gut fullness in the fish at the end of the experi-ment (Figure 4), possibly because the relatively large tagsincreased stress levels or occupied space that would have other-wise been available for food.We did not observe a correspondingdecline in condition factor (Figure 3), but these fishwere not foodlimited, and because they were adults, growth rate was likely tobe slow (and therefore may not have been expected to changemuch over the course of this short experiment).

Survival for the acoustic tag surgery control after 28 d wassimilar to the anesthesia control, suggesting that Delta Smeltare resilient to handling and surgical techniques. We did not

include a control for tag insertion due to the difficulty ofremoving a tag without harm to the fish, so we were unableto determine whether it was the act of tag insertion or the tagburden itself that resulted in lower survival. Survival in theacoustic tag injection control was somewhat lower than survi-val in the acoustic tag surgery control, suggesting that theremay have been an effect of the needle on survival, as sup-ported by the higher prevalence of internal lesions (Figure 4).

Behavioral impairment was only evident in fish implantedwith larger acoustic tags. These fish exhibited slower swimspeeds and frequently pitched, rolled, or remained stationarynear the tank bottom throughout the 28-d experiment. Werecommend additional behavioral experiments with PIT- andacoustic-tagged fish to quantify the extent to which tags alterswimming performance (e.g., burst speeds and sustainedswimming) and predator avoidance (Brown et al. 2010;Collins et al. 2013; Walker et al. 2016).

Minimizing handling time is critical when working withspecies that are sensitive to handling. Aside from the acoustictag surgery treatment (mean ± SD = 1.01 ± 0.27 min), meanhandling times for each treatment in the tagging experiment inthis study were less than a minute, which can be largelyattributed to eliminating suturing from the procedure. Themajority of time in salmonid tagging efforts involving surgeryis spent suturing to improve tag retention and facilitate wound

FIGURE 5. Relationship between tag burden (tag mass/body mass) and survival probability for Delta Smelt implanted with PIT and acoustic tags. Symbolsindicate survival (1) or mortality (0) of individual fish (a small amount of noise was added to reduce overlap). Lines indicate the continuous relationship fromlogistic regression of these data.

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healing (Wagner et al. 2011). The loss of just three tags acrossall tagging treatments in our study (n = 119) suggests that thetime savings from the reduced handling did not have anassociated cost in a higher rate of tag loss. The results fromthe AQUI-S 20E dosing and duration experiments indicatethat a 35 mg/L dose and 4 min in anesthesia is adequate forfuture Delta Smelt tagging studies. While subsequent recoverywas somewhat prolonged relative to lower AQUI-S 20E doses,survival was not reduced. We considered this a worthwhilecompromise given that the primary goals of effective AQUI-S20E use were reduced time to heavy anesthesia with minimalfish movement during tag implantation, together with highpostanesthesia survival.

Management RelevanceCultured Delta Smelt implanted with tags may serve as a

useful tool for studying the effectiveness of managementactions, including those related to State Water Project andCentral Valley Project operations. For example, cultured DeltaSmelt implanted with tags could be used as wild-fish surrogatesfor examination of survival related to the effects of wateroperation management actions (see Castillo et al. 2012), forwhich survival estimates are critical for estimating population-level entrainment effects (Kimmerer 2008). These data may, inturn, contribute to the development and refinement of simula-tion models, as has been done for salmonids in the Sacramento–San Joaquin Delta (Zeug et al. 2012). However, additionalstudies are needed to further develop and evaluate taggingmethods. For example, behavioral experiments using culturedfish should be conducted prior to any field studies involvingreleases of fish into native habitats to understand how tags mayaffect mobility and survival (Collins et al. 2013).

This study demonstrates that PIT tags have considerablepotential for use in tracking studies of Delta Smelt in the wild.For example, PIT tags could be considered for specific appli-cations, such as the measurement of fish loss rates at waterdiversions (e.g., Clark et al. 2009; Castillo et al. 2012), habitatuse, and effectiveness of habitat restoration projects.

Ultimately, the optimal solution for the evaluation of DeltaSmelt management actions would be successful implementa-tion of acoustic tagging because the detection range of PITtags is generally limited to less than a meter (Burnett et al.2013). Acoustic tagging of Delta Smelt would facilitate avariety of tracking studies throughout the Sacramento–SanJoaquin Delta that would aid conservation and recovery effortsfor the species. Potential study topics include the estimation oftransit times in delta channels under different water projectoperations, quantification of restored habitat use, and identifi-cation of areas with intense rates of predation. Our studysuggests that acoustic tags must be made smaller to reducethe effects on Delta Smelt survival. On the basis of our logisticregression analysis, we recommend a tag burden of ~2% orlower (Figure 5). This would necessitate acoustic tags that areless than half the mass of the JSATS tags tested in the present

study. To this end, investment in tagging research and devel-opment of smaller tags is encouraged.

ACKNOWLEDGMENTSFunding for this research was provided by the State and

Federal Contractors Water Agency Science Program Grant#15-09. D. Fullerton and S. Fong provided critical guidanceand study support. We thank G. Tigan and all the staff atthe UC Davis Fish Culture and Conservation Laboratory forlogistical support and assistance during our study. We alsothank G. Castillo, J. Miranda, K. Clark, M. Weiland,C. Woodley, K. Eder, and J. Morinaka for sharing theirknowledge and providing insightful comments, suggestions,data, and equipment. We thank B. Fujimura and T. Sommerfor helpful comments on earlier drafts and the editor,associate editor, and two anonymous reviewers for com-ments on the submitted manuscript. We also thankK. Cowin and J. Reyes for their assistance with laboratoryexperiments and manuscript preparation, respectively. Thisstudy was conducted in accordance with UC DavisInstitutional Animal Care and Use Committee Protocol18608.

ORCIDRichard M. Wilder http://orcid.org/0000-0003-1244-

4824

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