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An acoustic sensor transmitter for in situ assessment of water quality and fish behaviour during chemical treatment of a parasite-infected river system: tag design and practical use

An acoustic sensor transmitter for in situ assessment of water quality and fish behaviour during... Background: Behaviour of potential host fish during chemical treatment against the ectoparasite Gyrodactylus salaris is a vital factor in designing treatment strategies, evaluating risk factors and establishing insights into previously failed treatments. The effectiveness of any chemical treatment may be compromised if fish either are forced to, or seek out actively, areas of the river where the water quality is less affected by the chemicals. The aim of this study was to develop and apply an acoustic fish tag for fish localization with sensors for in situ measurement of water conductivity and temperature to investigate fish behaviour before, during and after an aluminium (Al) treatment. The sensor tag allowed discrimination between water qualities, and thereby quantification of exposure to treatment water. Findings: Adult Atlantic salmon and anadromous brown trout from river Lærdalselva were tagged with external con- ductivity transmitters and followed daily by a network of passive receivers and by manual tracking 1 week ahead of treatment, during a 2-week aluminium (Al) treatment period and one week after an Al treatment. The results show no avoidance behaviour related to the Al treatment and most of the fish exhibited a behaviour during the treatment that did not differ significantly from the behaviour observed before or after the treatment. Data collected from the tags showed that the fish experienced increased conductivity during Al administration, suggesting successful exposure to treatment water. The tag gave verifiable environmental information and functioned well in the turbulent and acousti- cally demanding river environment, albeit with variable detection range. Conclusions: The conductivity and temperature tag provided novel data on fish behaviour and exposure during the Al treatment period. Results show that fish exhibit normal behaviour during this period and no avoidance response can be detected in the collected data. Keywords: Acoustic telemetry, Conductivity, Salmonids, Aluminium, Water quality, CondTag, Parasite, Gyrodactylus salaris, Atlantic salmon, Anadromous brown trout Background In Norway, introduction and secondary dispersion of the *Correspondence: knut.alfredsen@ntnu.no monogenean parasite Gyrodactylus salaris has caused Department of Civil and Environmental Engineering, Norwegian severe population decline of Atlantic salmon (Salmo University of Science and Technology (NTNU), Trondheim, Norway Full list of author information is available at the end of the article salar) in infected rivers [1, 2]. The discovery of successful © The Author(s) 2021. 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The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Alfredsen et al. Anim Biotelemetry (2021) 9:7 Page 2 of 14 elimination of G. salaris infections in salmon by exposure sea trout, both an upriver migration and more stable to aqueous labile inorganic aluminium (Al ) [3] has led holding behaviour would be expected [16]. For smaller to a scientific [4] and practical [5–7] efforts to develop a non-mature sea trout, one could expect both down and full-scale chemical treatment method for parasite elimi- upstream migration. The reach of the river studied is the nation while maintaining fish populations in infected main spawning area of the river, and the fish will mostly river systems. The eliminating effect on G. salaris of spawn in the mainstem. Based on the measured variables, labile/cationic Al in acidified waters was first described the sensor tag allows for discrimination between water by Soleng et  al. [3] and the extensive knowledge of bio- qualities such as ground water, brackish water, chemically logical effects of Al, including dose–response relation - treated water and the normal river water. For example, ships for host species Atlantic salmon and brown trout the groundwater runoff to the river Lærdalselva sus - in the acidification literature [8] defined treatment con - tains conductivity typically more than ten times that of −1 ditions (Al, pH). The method involves administering of river water (12–20 vs 150–350 µScm ). When attached Al as aluminium sulphate and acid (H SO ) for pH con- to fish, these transmitters can therefore be used to iden - 2 4 trol (target pH: 5.9–5.7) to obtain a desired concentra- tify areas in the river and estuary used by fish where the tion of Al between 25–30 and µg/l. While the causative chemical treatment for G. salaris might be suboptimal. agent responsible for G. salaris removal from the host Tracking fish before, during and after the treatment also fish is cationic/labile Al, adding aluminium sulphate and gives indication of the exposure to the chemical reagent additional sulfuric acid to decrease pH also results in a in the water and contributes to knowledge on behaviour marked water conductivity increase in the river during during the treatment. treatment [9]. Thus, the increase in water conductivity The study provides an example and ideas of how caused by the addition of ions and lowering of pH serves experimental objectives may be accommodated within as a practical proxy for measuring dose in  situ. At pre- the capabilities and limitations of contemporary digital sent little is known about the spatio-temporal response tag platforms. Detailed field observations showing the pattern of fish to the water quality changes during an Al dynamics of the fish’s exposure to the chemical reagent treatment period. Both experimental and field studies under the circumstances of a full-scale treatment sce- have demonstrated that Atlantic salmon is able to sense nario are given as well as documentation of no avoidance and avoid low pH [10] and in some cases also elevated behaviour both during and after treatment. concentrations of aluminium [11]. In other cases no avoidance has been observed for aluminium in Atlantic Methods salmon both in the laboratory [12] and for a combined Transmitter design low pH/increased aluminium in a field study [13]. An acoustic transmitter tag with a water conductivity and Fish behaviour during chemical treatment against G. temperature sensor was developed specifically for this salaris is a vital factor in designing treatment strategies, study to enable observations of individual behaviour and evaluating risk factors and establishing insights into pre- to quantify the exposure of fish to different water quali - viously failed treatments. The effectiveness of any chemi - ties during a chemical treatment. The tag was based on cal treatment may be compromised if fish either are an ultra-low power mixed-signal electronic design simi- forced to, or seek out actively, areas of the river where the lar to the acoustic tag platform described in Føre et  al. water quality is less affected. Areas of brackish water and [17], which allows physical miniaturization while secur- groundwater runoff are regarded as typical problem areas ing long operational life and flexibility with respect to in this respect. Avoidance and escape reactions from ele- sensor integration, on-board data processing and storage vated Al concentrations have been observed previously capacity. To sense water conductivity, the tag incorpo- [14]. rated a 4-pole gold-plated conductivity cell embedded in The aim of this study was to develop and apply an one of its end caps (Fig.  1) where the cell constant was acoustic fish tag, with sensors capable of simultaneously dimensioned according to the conductivity range typi- measuring temperature and conductivity of the sur- cal for the water in the river and estuary. Conductivity rounding water to investigate to what extent avoidance measurements were initiated and supervised by the on- behaviour occur before, during and after an Al treat- board microcontroller and involved activation of a driver ment. The tag was used to track Atlantic salmon (Salmo circuit that applied an alternating voltage of constant salar) and anadromous brown trout (Salmo trutta) dur- level to the outer pair of electrodes, while simultaneously ing the Al treatment of river Lærdalselva from August to sensing the corresponding voltage potential between September 2009. During this period the fish are on their the inner pair of electrodes and the total electrical cur- spawning run in the river and moves from the estuary rent flowing through the water. The microcontroller to their spawning sites [15]. For salmon and the mature measured the current and voltage signal for each cycle A lfredsen et al. Anim Biotelemetry (2021) 9:7 Page 3 of 14 Fig. 1 The conductivity and temperature acoustic transmitter tag (CondTag) with three concurrent transmitter functions. Transmitter function (i) sends S256-encoded messages on odd IDs that contain instantaneous measurements of conductivity and temperature, where the data byte is split in two 4-bit values serving as indices into a look-up table specifying predefined conductivity and temperature intervals. Transmitter function (ii) sends S256-encoded messages on even IDs that contain information reporting how many hours over the last 45 h the tag has resided in two predefined water quality categories ( WQC) defined on the basis of time averages and fluctuations in conductivity measurements. See Table 1 for a description of the WQCs. Transmitter function (iii) runs in parallel with function (i) and (ii) and emits a 20-ms acoustic “pinger” pulse every 5 s on one of three selectable tracking frequencies (72, 75 and 78 kHz), and is included to enable manual localization and tracking of the fish using manual receivers with a directional hydrophone. The inset image shows the tag with a 4-pole conductivity cell embedded in its endcap. The temperature sensor (not seen) is located on the opposite side of the endcap by employing a micropower instrumentation amplifier suitable for the anticipated conditions at the study site. and its integrated AD. Conductivity was calculated as Although the conductivity sensor allowed a maximum −1 an average over several cycles of the product of the cell measurement range of 0–2530 µScm , the sensor was −1 constant and the ratio between the measured current set to saturate at 200 µScm since the conductivity lev- and voltage. A calibrated NTC thermistor was embedded els of both normal river water and treatment water were in the tag’s end cap adjacent to the electrodes and was predicted to be very low. This gave a measurement reso - −1 used to sense ambient water temperature as well as com- lution of 0.2 µScm and laboratory tests proved that −1 pensating conductivity measurements for temperature accuracy was better than 1.4 µScm for these water dependency. The conductivity and temperature sensors types. The temperature sensor had a measurement range were calibrated with selectable gain and offset settings to of − 2.0 to 25.5 °C with resolution 0.03 °C and accuracy accommodate measurement ranges that were considered better than 0.3 °C. Alfredsen et al. Anim Biotelemetry (2021) 9:7 Page 4 of 14 Both continuous and more sporadic observations of one-byte data payload that can be sent during each trans- the fish were anticipated in the relatively long and var - mission, conductivity and temperature sensor measure- ied river system. For this reason, the tag was designed ments were compressed into two 4-bit binary codes by a and programmed as a multi-function transmitter in software algorithm that ran locally onboard the tag (see order to serve three different monitoring objectives Fig.  1). These codes served as indices into two look-up simultaneously: tables containing predefined conductivity and tempera - (i) Transmit periodic measurements of instantane- ture intervals. The approach employed data binning of ous electrical conductivity and temperature of the each variable into one of 16 different intervals with a tagged fish’s ambient water. nonlinear mapping between bin number and interval (ii) Calculate and transmit statistical information per- size. While having rather low resolution, the mapping taining to the tagged fish’s exposure to different technique allowed enhanced resolution in the parts of the water qualities over a defined time history. sensors’ measurement ranges considered likely to prevail (iii) Emit regular and frequent “pings” to permit manual during the experiment, at the expense of lower resolution acoustic bearing measurements and localization of in ranges that were considered less likely to occur. The the tagged fish using one of three separate tracking selection of intervals was done based on a priori knowl- frequencies. edge of typical conductivity and temperature ranges of normal river water during the relevant season, as well as In addition to manual tracking receivers, automatic values representative of the water quality during Al treat- monitoring receivers were used extensively for recep- ment, of groundwater effluences, and of the river estuary. tion of the telemetry data (Vemco VR100 and VR2W, Details of the coding scheme of conductivity and temper- Halifax, NS, Canada). This implied that transmitter func - ature intervals are given in Fig. 1. tion (i) and (ii) had to be based on an acoustic carrier Transmitter function (ii) was implemented to pro- frequency of 69  kHz and the S256 encoding of acoustic vide statistical records of the fish’s exposure to different messages [18]. The S256 encoding scheme only permits water qualities over a specified temporal horizon. With a 16-bit data payload for each message, which is equally tagged fish moving between locations in the complex divided between an 8-bit tag ID code and an 8-bit sensor and acoustically challenging habitat of the river, it was data value. Each transmitter tag was therefore allocated expected that signals would be beyond detection range two unique and consecutive ID codes, with odd and even of unknown extents of time during the experiment. Still, ID codes representing transmitter function (i) and (ii), it was regarded as important to be able to reconstruct respectively, with transmission alternating and repeating historical information concerning the fish’s exposure at random intervals of 40–120 s. On-board compression to different water qualities once the fish again could be techniques in terms of look-up tables and calculation of detected. All remaining data memory on-board the tag statistical moments were implemented in the tag firm - was thus allocated to a sliding time window data buffer, ware to convey useful sensor data within the limitation and an algorithm was developed to keep record of the of one byte per transmission. Transmitter function (iii), fish time of exposure to three different water quality the acoustic ping, was designed to operate concurrently categories (WQC0, WQC1 and WQC2), as defined in with function (i) and (ii), but at separate frequencies to Table  1. The data buffer was configured to cover a 45-h avoid acoustic interference with messages transmitted time history and was further divided into 15, 3-h inter- on the 69 kHz channel. The tag was thus programmed to vals (15 × 3 h = 45 h). For each 3-h interval, the algorithm emit short “ping pulses” of 20  ms duration every 5  s at calculated and stored the arithmetic mean and the vari- either 72, 75 of 78 kHz (depending on the tag ID), which ation, or number of fluctuation events occurring in the thereby permitted concurrent tracking of up to three conductivity measurements. A fluctuation event was co-located fish in the same stretch of the river while still defined to occur when two consecutive conductivity being able to receive instantaneous and statistical data on measurements happened to differ by a value greater than conductivity and temperature. a certain threshold value and was included to serve as an Transmitter function (i) was implemented to provide indicator of the variability in water quality experienced instantaneous conductivity and temperature readings by the fish. The sensor was sampled every 60 s giving 180 from the fish’s ambient water as S256-encoded messages. conductivity measurements per interval. Each interval This way data could be received at regular intervals using was then categorized into one of three different WQCs both automatic monitoring receivers (VR2W) that were based on these two variables following the criteria shown permanently deployed in specific pools of the river as in Table 1. At the time of acoustic transmission, the infor- well as manual receivers (VR100) that were in ambula- mation in the buffer was further compressed into two tory use during tracking campaigns. Due to the limited 4-bit codes, each encoding the number of hours the fish A lfredsen et al. Anim Biotelemetry (2021) 9:7 Page 5 of 14 Table 1 Definition of water quality categories (WQCs) Water quality Range of conductivity Number of conductivity fluctuation Description −1 −1 category average (µScm ) events (|κ —κ |> 5 µScm ) t t − 1 WQC0 0–25 And = 0 Normal river water, main stem WQC1 26–40 And < 4 Stabilized river water during Al treatment WQC2 0–25 And > 0 River water with groundwater influence, or other atypical variations in conductivity, or brackish water Or (estuary) 26–40 And ≥ 4 Or > 40 And Any WQCs are based on certain combinations of average conductivity and the variation between consecutive conductivity measurements, or fluctuation events, over a −1 3-h interval containing a total of 180 measurements. A fluctuation event was defined to happen when conductivity changed by more than 5 µScm in 60 s has spent in WQC0 and WQC1 over the last 45  h (see freshwater, had an acoustic source level of 146 dB @1 m Fig. 1). Time spent in WQC2 was not transmitted explic- re. 1 µPa, and an estimated battery life of more than itly but could be found implicitly by applying the formula 90 days. t = 45 – (t + t ). Details of the tag encoding WQC2 WQC0 WQC1 are shown in Fig. 1. Tagging procedure Following design, implementation and validation of Adult Atlantic salmon (N = 6, mean length 46.9  cm, SD the sensor tag prototype, a batch of 25 tags were manu- 16.1  cm) and anadromous brown trout (N = 16, mean factured by Thelma Biotel AS (Trondheim, Norway) for length 48.4  cm, SD 14.9  cm) (Table  2) from river Lærd- use in this study. The electronic tag that was designated alselva, Norway (Fig.  2) were caught by angling using as CondTag, had a cylindrical shape with 9  mm diame- sports fishing equipment at several sites along the river. ter and 43  mm length, weighed 6.3  g in air and 4.1  g in The species are both relevant as primary host (salmon) Table 2 Length, species and tag-id for the marked fish Tag-id instant Tag-id stat Species Length (cm) Tagged Tag site First obs Last obs 69 70 Anadromous brown trout 35 15.08 Oye 16.08 17.09 75 76 Anadromous brown trout 35 07.08 Rikheim 19.08 22.09 77 78 Anadromous brown trout 43 06.08 Rock 16.08 06.09 81 82 Anadromous brown trout 33 06.08 David (5.5) 16.08 22.09 83 84 Anadromous brown trout 35 15.08 Oye 16.08 09.09 85 86 Anadromous brown trout 35 07.08 Gronnebank 16.08 30.08 91 91 Anadromous brown trout 43 06.08 Rock 29.08 19.09 93 94 Anadromous brown trout 52 07.08 Rikheim 24.08 22.09 95 96 Anadromous brown trout 54 06.08 David (5.5) 29.08 29.08 143 144 Anadromous brown trout 38 15.08 Oye 16.08 22.09 145 146 Anadromous brown trout 31 07.08 Gronnebank 16.08 21.09 147 148 Anadromous brown trout 57.5 07.08 Per (5.3) 06.09 19.09 151 152 Anadromous brown trout 48.5 06.08 Rock 16.08 16.08 155 156 Anadromous brown trout 41.5 06.08 Per (5.3) 28.08 17.09 73 74 Atlantic Salmon 48 15.08 Rock 25.08 06.09 79 80 Atlantic Salmon 84 06.08 Robinson (15.7) 02.09 05.09 87 88 Atlantic Salmon 55 14.08 Grasmarki 25.08 20.09 141 142 Atlantic Salmon 53 14.08 Grasmarki 16.08 15.09 149 150 Atlantic Salmon 84 07.08 Sandebank (15) 24.08 22.09 The first tag id refers to the instantaneous measurement (transmitter function i), the second tag id refers to the statistical data (transmitter function ii). The tag date, tag site and first/last observation is also given. For tagging locations not named on Fig. 2, the distance from the estuary is given in kilometres. The fish were not weighed during marking, but using observed weight of similar size fish from the same river we estimated the tag burden of the smallest fish to be < 1.4%. The tag weighs 4.1 g in water Alfredsen et al. Anim Biotelemetry (2021) 9:7 Page 6 of 14 Fig. 2 Map of Lærdal with tracking stations marked along the river reach in red with names. Catch-and-release sites are marked with green and the Al release sites are marked with purple arrows. The numbers in the parentheses is the distance from the estuary. Inset: anadromous brown trout tagged with the conductivity tag and long-term intermediate host (trout) for the parasite temperature measurements (WTW Multiparameter G. salaris [19]. instrument). The tags were fitted with thin surgical steel After unhooking, fish were wet netted into a hold - wire and attached at two points just below the dorsal fin ing tank (volume 500 l) close to the riverbank. After by leading the ends of the wire through the fish using 23 20–30  min, fishes were netted directly from the hold - G (0.60 × 25  mm) syringes. The wire ends were secured ing tank into a pre-anaesthetic sedation tank containing on the opposite side by crimping on a small copper crimp −1 0.5  mg  l metomidate for a minimum of 2  min. Fishes with a 12-mm soft plastic disk as padding between the were then transferred to an anaesthetic bath containing crimp and the fish’s skin. −1 60  mg  l MS 222 (tricaine methanesulfonate) anaes- thetic [20]. Cessation of response to peduncle pinching Tracking setup was used as a criterion for surgical anaesthesia. Fishes The fish were followed by a stationary network of auto - reached surgical anaesthesia within 4 min and were then matic listening receivers (VEMCO VR2W, locations transferred to a tank with river water where the tagging shown in Fig.  2 and by daily manual tracking (first by was conducted. During surgery the head, gills, and most manually deploying a VEMCO VR2W at each release of the body of each fish were submerged in water. Total location and later using a portable VEMCO VR100 handling time was around 2  min per fish. Immediately directional hydrophone during August and September after tagging, the fish were transferred to a recovery tank of 2009. Manual tracking was conducted in the river with river water (80 l) with circulated flow and closely each day between the 14th of August and the 10th of monitored. Fish regained balance ability and showed September from 0800 to 2000 by following the same active swimming behaviour within 0.5–2  min of recov- route. Manual tracking was also done on the 16th and ery. After a recovery period of 5–6  min, the fish were 18th of September. This was done by walking upstream released into the river at the same site as it was angled. along the riverbank and placing both a passive receiver During recovery, tag readings were made and compared and the hydrophone of manual receiver into the river with data from a control tag permanently installed in at different sections of the pools. In pools where fish the revival tank as well as manual conductivity and were detected for more than 2 days, a passive receiver A lfredsen et al. Anim Biotelemetry (2021) 9:7 Page 7 of 14 was deployed. Once deployed in the river the passive Lærdalselva is a clearwater river and visual count- receiver was at the same location during the whole ing of salmonid spawners has been conducted from the study period. These passive receivers were offloaded early 1960s [21, 22]. The clear water made it possible to daily to check if there had been registered movement of check the status of sensor/fish that had an observed fixed tagged fish during night-time. position in the river by snorkelling. One person drift- The stationary receivers were mounted on the river ing downstream by snorkelling and one person on the bottom either using blocks of concrete or specially riverbank to register position and observations carried designed metal stands. Each site except Rikheim had out this procedure. The surveys were conducted both one receiver and range tests were performed to ensure in the upper part (Robinson–Rikheim) and in the lower coverage of the entire river width. Lærdalselva is a part (Badehølen–Bruhølen). The diver observed natural relatively small river (widths 30–60  m) and all sites behaviour in the fish encountered and fish with tags were are easily accessed on the bank. The data from the sta - seen. No dead fish were observed. tionary network and the manual tracking data were combined into a common dataset used in the analy- Other data sis. For the analysis of the fish behaviour, three phases, Two reference tags were placed at Bø and Øye together before (defined from the 16th of August to the 23rd of with the hydrophones. A continuous measurement of August), during (defined from the 26th of August to temperature was carried out during the experiment at the the 6th of September), and after (defined from the 8th same locations by connecting a Vemco Minilog II to the of September to the 15th of September) the Al treat- hydrophone stand. Water quality was monitored manu- ment, were specified to get a consistent comparison ally during the treatment period. Discharge is measured of individual fish and to avoid effects of different time at the Stuvane gauge (NVE station 73.2.0) with a time of release of the fish after tagging. A gap of 2 days is resolution of 30  min. Stuvane is located close to the defined after the start of the treatment on the 24th of Rikheim site (Fig. 2). August to allow for the treatment to cover the entire river. Similarly, a gap of 1 day is defined between the Aluminium treatment period of treatment and the start of the after period to Aluminium sulphate was added to all tributaries, as well allow the treatment chemicals to be transported out of as at several sites along the main river stem to obtain tar- the system. The different phases of the study period are get concentrations all over the river system. In addition, indicated in Fig.  3, which also shows the discharge in the main river was acidified using sulphuric acid (30%) the reach during the treatment period. Data were also to bring pH down to effective treatment levels where Al collected after the 15th of September to check move- is labile/cationic. Monitoring was done by using conduc- ment and further ensure that fish were alive. For more tivity, pH and Al fractionation (Barnes–Driscoll). As the information on the receiver network used in the experi- latter being very labour intensive, mainly the two former ment in river Lærdalselva, see Urke et al. [20]. methods were used for direct control. The pH measure - ments were used as a feedback to the dosing stations and conductivity for daily dose control. Conductivity is not strongly related to discharge in this river system and is very low naturally. Monitoring stations upstream of the dosing sites confirmed the increase in conductivity dur - ing treatment, and the pre- and post-treatment measure- ments also confirm this quite consistently. Statistical analysis The relationship between movement and discharge was tested by computing the sum of movements for each half- hour interval that matched the discharge observations and then testing the number of movements against dis- charge and change in discharge using linear regression. A movement was counted when the fish was found in differ - ent locations in two consecutive observations. Conduc- Fig. 3 Discharge over the study period measured at the Stuvane gauge (located at the Rikheim tracking station). The coloured panels tivity data were checked for normality using qq-plots and shows the periods of analysis: a prior to treatment, b treatment histograms, and since the data were skewed, a Box Cox period, c after treatment transformation was applied to the data using the package Alfredsen et al. Anim Biotelemetry (2021) 9:7 Page 8 of 14 EnvStats in R [23]. The changes in conductivity among did a similar test on individual fish using ANOVA over the periods before, during and after treatment was then all three periods and t tests on pairs of periods for each tested by first computing the averages for each fish for of the fish that had recordings over different periods. All each period and then testing this using ANOVA across analysis was done using the R software [24]. all periods and then a t test between periods, before– during, during–after and before–after. Furthermore, we Results To control the tag reading of temperature and conductiv- ity, measurements were made in the recovery tank after surgery using a calibrated instrument (WTW multipa- rameter instrument). These were then compared to assess the accuracy of the tags. The recordings confirmed good correspondence between the measurement of tempera- ture and conductivity from the tags and the instrument (Fig. 4, panel a shows temperature, panel b conductivity). This also confirmed that all tags were working at the time of release of the fish. Of the 22 tagged fish, 19 were detected either by man - ual tracking or fixed receivers during the study period as indicated in Fig.  5. We find it most likely that the three fish found during the study period were located in areas with difficult acoustic conditions and therefore dif - ficult to detect, but we cannot rule out mortality or tag Fig. 4 Comparison conductivity and temperature measured with the tag and a temperature/conductivity meter. Panel a shows water malfunction. The fish could also have moved out of the temperature and panel b shows the conductivity study area. Twelve fish were recorded throughout the Fig. 5 The figures show at which tracking locations each fish is observed over the time period as a function of the distance to the river estuary. The coloured panels show the same time periods as in Fig. 3. The graph is extended 1 week after the “AFTER” period to capture movement of fish. See Fig. 2 for more information on locations and distances along the river A lfredsen et al. Anim Biotelemetry (2021) 9:7 Page 9 of 14 experimental period in relation to fixed receiver stations in the river, and the remainder were detected one or sev- eral times during the manual tracking campaigns. A total of 32,285 detections were made during the study period, distributed with 4454 before, 14,687 during, and 13,144 in the period after the treatment. The position and movement of each individual fish are shown in Fig. 5, where the position of the fish is related to its distance from the river estuary. Relatively few move- ments were observed among the fish during the track - ing period. From the data in Fig. 5, it is evident that only three fish out of 19 (16%, tags 73, 77 and 85) show down - Fig. 6 Box plot showing the average conductivity for all fish stream movements during the period. This occurred dur - distributed on the three time periods. The conductivity interval is ing treatment for two of the fish, but both of these fish given in table (i) in Fig. 1. The p values related to the Anova test on returned to their original position after some time. The differences between the periods are shown in the graph. The thick third fish moved 900  m downstream before the treat - line represents the median, the box shows the inner quartile range ment started and stayed there. Five fish showed a distinct (IQR) and whiskers are at 1.5 * IQR upstream movement during the study period (26%, tags 69, 83, 141, 143 and 155). All upstream movements took place after the treatment period, and the longest move- raises the conductivity in the river followed by a reduc- ment was 9.6 kms. The remainder of the tagged fish (58%) tion back to the level seen in the period before treatment held position at one site during the entire period. The when the treatment is over. largest number of movements was observed in the period Further, an analysis of each individual fish between after the treatment, but no significant differences exist periods was carried out; see Fig.  5 for the periods where between the three periods. To check if discharge had an each tagged fish is observed. For the fish with observa - influence on movements, the number of movements was tions in all three periods, an ANOVA test shows that summed for each half-hour (resolution of the discharge there is a significant difference between the periods times series) and linear regression between instantane- (p < 0.001). For fish with observations for the period ous discharge and the change of discharge were carried before and during treatment, with one exception a t-test out. This shows no pattern connecting observed move - shows a significant increase in experienced conductivity ment to the observed variability of discharge over the for each individual fish during the treatment (p < 0.001 study period, movement vs. instantaneous discharge for all fish). The exception is an anadromous brown trout (r < 0.001, p > 0.05) and movement vs. changes in dis- (tag 83) in the lower part of the river that shows only a charge (r < 0.001, p > 0.05). However, the observed rises slightly increase in median conductivity from before and falls reside within normal variations in discharge and treatment to the treatment period. For fish recorded both could not be considered as floods. in the treatment period and the period after treatment, The average experienced conductivity of each fish based we see a significant reduction in conductivity for all indi - on the full set of telemetry data is shown in Fig. 6. There viduals (p < 0.05). When we compare the period before is a significant difference in conductivity experienced treatment to the period after treatment, the picture is by the fish between the treatment periods (ANOVA, mixed. Some fish are seen to return to the same level of F = 7.797, p < 0.01). Looking at the different periods, we conductivity as before the treatment, while for a few indi- see a significant increase in conductivity between the viduals we still see a significant difference in experienced period before treatment and the treatment period (t conductivity. test, t = − 3.6623, p < 0.01). We also see that the increase As an example of observed conductivity in individual in conductivity observed in the telemetry data from the fish, Fig.  7 shows three fish (tags 75, 93 and 149) located fish tags during the treatment period corresponds with at the Rikheim site 14.7  km from the estuary. These fish an increase measured in the river for the same period. were present at this site for long periods during the study, We do also see a significant reduction in conductivity and the results show individual variations that appear to between the treatment period and the period after (t test, be linked to the specific locations of the fish in the pool, t = 3.0755, p < 0.01). For the period before and period which were determined by taking cross-bearings of the after treatment there are no significant difference in the fish’s ping pulses (transmitter function iii). The tributary conductivity experienced by the fish (t test, t = − 1.3099, Nivla enters the Rikheim site from the south, and this p > 0.05). For the full period, we see that the treatment Alfredsen et al. Anim Biotelemetry (2021) 9:7 Page 10 of 14 rise in river discharge, which could be the reason for loss of reception either by the fish moving out to an area not covered by the receiver or a deterioration of the acous- tic channel. When the fish was detected again on the 2nd of September, the first message reveals that the fish had been in stable and low conductivity water (WQC0) over the entire 45-h period preceding the reception of that message, including the 17 h when reception was lost. For the second gap, the fish was out of detection range for about 20 h, from the 2nd of September 14:30 to the 3rd of September 10:30. The first message received on the 3rd of September after the gap shows that the fish had sustained 6  h of exposure to water of elevated and/or fluctuating Fig. 7 Measured conductivity intervals for the fish (tag 75: conductivity levels, and correspondingly a 39  h of expo- anadromous brown trout, 35 cm, tag 93: anadromous brown trout sure to normal river water over the last 45  h. Increasing 52 cm, tag 149: Atlantic salmon 84 cm) located at tracking location exposure to elevated and/or more unstable levels of con- Rikheim during the three analysis periods. The boxes show the same distribution as in Fig. 6. Conductivity intervals given in table (i) of ductivity can be seen in the following hours, a tendency Fig. 1 that continued towards the end of the treatment period and corresponded well with the change in general river water conductivity during the treatment. When the treat- stream discharge water of a natural higher conductivity ment ended, the tag reported an increasing prevalence level than the main river stem. The fish with tag 93 was of WQC0 (normal river water) with some lag due to the located at the entrance of the tributary for most of the 45-h sliding window buffer, as should be expected. time and this shows up as a higher level of conductivity measured by the tag when compared to the other two fish Discussion which took other positions in the pool. A number of daily In this paper, we present the design of a multi-function measurements at the Nivla outlet during the treatment acoustic sensor tag and the results from its practical use −1 period gave a median conductivity of 43 µScm (interval on adult Atlantic salmon and anadromous brown trout −1 7), and the median tag value gave 37.5 µScm (interval during a chemical Al treatment of the river Lærdalselva −1 6). The two other fish had a median value of 22.5 µScm in Norway. Movements seen in the fish both during and (interval 3) during the treatment period. after the treatment can be considered as natural migra- The statistical function of the tag provided informa - tory behaviour in Atlantic salmon and brown trout dur- tion on the time spent in different water quality catego - ing this period of the year. The effect of the Al treatment ries (WQCs) over a 45-h sliding time window, as outlined on the fish’ ambient water could be observed indirectly in the section on tag design and Fig.  1. Figure  8 shows a as an increased level of conductivity in the measure- situation where a fish (tag 81) intermittently came out ments received from the tagged fish. This demonstrates of detection range and introduced significant gaps in the utility of the sensor tag as a tool for in  situ evalua- the data received from this fish, but where the statisti - tion of the treatment process and it further confirms that cal recordings (transmitter function ii, Fig.  1) could be the fish were exposed to the active reagent during the applied to evaluate the fish’ continuous exposure to dif - treatment. The main conclusion from the movement and ferent water qualities irrespective of intermittent loss of conductivity data is therefore that the tagged fish showed contact. Each bar depicts a reception of a single statisti- no obvious signs of flight or avoidance behaviour upon cal message and shows the fraction of time where the fish exposure to the chemicals during the treatment. This is was exposed to WQC0 (normal river water—blue colour) an important observation related to the effectiveness of or the combination of WQC1 and WQC2 (treatment/ the treatment. atypical water—red colour) of the preceding 45-h period. In addition to sending regular instantaneous measure- Instantaneous values are indicated as dots on top of the ments on water conductivity and temperature, the tag plot. Panel a shows the full dataset, while panel b details was programmed to carry out an onboard analysis of a subset of the data where the fish came out of detec - an internally stored time history of conductivity meas- tion range at two occasions and caused significant gaps urements and report exposure times to different pre - in the recordings. The first gap lasted ~ 17  h, from the defined categories of water quality. This function was 1st of September 16:00 to the 2nd of September 09:00. It implemented to prevent discontinuities and gaps in should be noted that this gap coincided with a distinct the received datasets due to anticipated limitations in A lfredsen et al. Anim Biotelemetry (2021) 9:7 Page 11 of 14 Fig. 8 Statistics plot for fish with tag ID 82 (anadromous brown trout, 33 cm). Panel a shows the full period and panel b a shorter period between 1st and 3rd of September. The colour of the bars indicates the number of hours the tag has been exposed to the different conductivity categories over the last 45 h, T_WQC0 is low and stable conductivity and TWQC1_2 combines the high and fluctuating categories (see Fig. 1 for more info). The dots on each panel indicate the instantaneous conductivity interval recorded by the tag when detected (table i, Fig. 1) acoustic coverage and signal quality that are caused by observations show that the fish was once again exposed the complex environment and turbulent conditions of a to water affected by the reagents at the end of the treat - river. Given that the tag could be detected again within ment period. This observation corresponds well with the time window spanned by its internal data buffer measured conductivity just downstream of the fish loca - (45  h in this case), valuable aggregated information on tion and where an incident in early September when high the prevailing water quality conditions when the fish was flow of water with low aluminium concentration from beyond detection range would be secured. The utility of the tributary Kuvella led to a period of low concentration this function was clearly demonstrated in the case of an of Al in the main river, which was seen as a reduction in −1 −1 anadromous brown trout (tag 81) that was monitored at conductivity from 24 µScm to 20 µScm measured in the site Badeholen throughout most of the study (Figs.  2 the river just downstream of the fish location. and 5), but was intermittently lost towards the end of From a technical perspective, it should be noted the treatment period creating gaps in dataset of instan- that the statistical function was implemented without taneous conductivity measurements (Fig.  8). From the including any additional components like memories or received data on exposure time to different water quality computing power to the electronic tag platform. It was categories it was nevertheless possible to conclude that exclusively implemented by writing new firmware that this fish had resided in what was categorized as normal exploited already existing hardware resources with only river water (WQC0) during those intervals. However, minor costs in battery life due to the extra processing Alfredsen et al. Anim Biotelemetry (2021) 9:7 Page 12 of 14 requirements. This demonstrates the flexibility and required to comply with the severely limited bandwidth capacity provided by contemporary digital electronic of the acoustic telemetry link. The selection of param - fish tags to carry out on-board processing and analysis eters, such as conductivity and temperature bin sizes, of sensor signals prior to transmission over the severely averaging intervals and length of the sliding time window, bandwidth-limited acoustic channel, a concept that has threshold for conductivity fluctuation events, and specifi - been utilized successfully in several subsequent telem- cation of the different water quality categories (WQCs), etry studies [17, 25–27]. Even if the recorded sensor data all have direct impact on the relevance and quality of the must undergo substantial compression and loss of detail data that may be harvested from the tags. Moreover, the before acoustic transmission, the approach features an parameters need to be selected prior to the actual study advantage over archival tags in that no recapture of the and depend on rather detailed a priori knowledge of the tag is needed to recover the data [25]. conditions that will prevail during the study. This infor - The tag also incorporated a concurrent acoustic mation may not be fully available at the time of the tag “pinger” function in order to support manual localization design and programming, particularly if the study is and tracking of the fish with directional hydrophones. novel and data background is sparse. To avoid interference with the S256-encoded acoustic Efforts were made in this study to establish the configu - messages at 69  kHz, pings were emitted every 5  s on a ration parameters as accurately as possible based on prior separate frequency. This was shown to work as intended analyses of the water chemistry of the river Lærdalselva, and proved to be a time-saving feature of considerable both in its normal state and during earlier Al treatments practical value during manual tracking campaigns where [9]. However, in hindsight, several changes in the param- multiple pools and long stretches of the river had to be eter selection could be envisioned in order to improve surveyed. The frequent pings provided rapid confirma - the performance of the tag. With the conductivity values tion of the presence or absence of fish, which would not experienced during this study, it would have been ben- be the case if the much less frequent S256 signals (up to eficial to select the conductivity intervals with a higher −1 2 min) had to be used for this purpose. The pinger func - resolution in the lower ranges (< 40 µS/cm ) at the tion was also instrumental in determining the exact expense of lower resolution in the higher ranges. No fish position of the anadromous brown trout (tag 93) at the were observed to enter either the estuary or areas with Rikheim site which reported elevated conductivity levels water of high ionic strength such as groundwater efflu - compared with two other fish residing in the same pool ents during the experiment, and the ability to detect such (Fig.  7). Localization of the anadromous brown trout at water qualities could in any case be limited to a couple −1 the outlet of the tributary Nivla, which naturally sus- of wide conductivity intervals above 40 µS/cm . Moreo- tains water of higher conductivity, warranted plausible ver, since temperature readings were of limited use in this explanation of the sensor readings and that the observa- study, a relocation of one or two bits from the tempera- tion could not be attributed to the fish taking refuge in ture field to the conductivity field of the S256 code would an unknown effluent of untreated water (e.g., groundwa - double or quadruple the resolution of the conductivity ter), and thereby compromising the efficiency of the Al intervals, respectively. This would undoubtedly make dis - treatment. crimination of normal river water from treatment water In general, the acoustic receivers worked well in the significantly clearer and such adjustments in the tag con - stream environment, but turbulence in some areas made figuration parameters would be straightforward to imple - manual tracking time-consuming and required accurate ment in similar studies in the future. positioning of the receiver to detect the transmissions. Acoustic tags have been used in river environments The simultaneous bankside tracking with the VR-100 and both for Atlantic salmon smolts [20, 28, 29] and adults approaching the fish by snorkelling confirmed that fish [30, 31], and provides a well-tested approach for tracking transmitting a signal from the same location over a long migratory fish in rivers [32]. Davidsen et  al. [26] used a period indeed were alive. A lower detection of fish tagged variation of the presented conductivity tag to track ana- in the upstream part of the study site (from Rikheim and dromous brown trout (Salmo trutta) during the CFT upstream) was observed during the experiment. Snorkel- Legumin treatment of the river Vefsna to eradicate G. ling confirmed that fish was alive, but heavy riffles and air salaris. They found no avoidance behaviour and no sur - entrainment made detection more difficult. No dead fish vival, which indicate a successful rotenone treatment. were observed in any of the snorkelling surveys. Similar to the findings of Davidsen et al. [26], there were One of the main challenges of the tag design pre- no avoidance behaviour in the Atlantic salmon and ana- sented in this study relates to the selection of appropriate dromous brown trout tagged in the study presented here, parameters for processing and analyses, as well as achiev- but in contrast no mortality was recorded which is an ing sufficient compression of the sensor data, which is advantage of the Al treatment method. In another study, A lfredsen et al. Anim Biotelemetry (2021) 9:7 Page 13 of 14 Mitamura et al. [27] used a tag based on the design pre- be accommodated within the processing capabilities of sented here to measure salinity during seaward migration contemporary digital acoustic tag platforms. of Atlantic salmon in a fjord in Norway. They utilized Acknowledgements both the conventional tracking method and the storage The authors are grateful for the assistance given by T. Grimelid, Ljøsne Hatch- feature of the tag to record the salinity, and found that the ery and R.A. Golf, The Norwegian Nature Inspectorate (SNO). The reported work was financed by the Norwegian Environment Agency. The authors thank statistical data stored on the tag both provided a longer H.R. Astrup and O. Wendelboe for their hospitality during the field work. record of data and insight into fish using low salinity areas also in the outer fjord which would be difficult to Authors’ contributions AaG and JAA designed the acoustic tag based on specifications given by HAU obtain with a conventional tag and tracking setup. and TK. HAU, TK, AGH and JAA designed the experiment. All authors partici- As mentioned above, the data from the tagging experi- pated in the field work. MK, KTA, JAA, HAU and TK performed data preparation ment in river Lærdalselva show no obvious response in and analysis. KTA wrote the manuscript with input from all other authors. All authors read and approved the final manuscript. the fish during the release of Al and acid to remove G. salaris. This is important for the success of the procedure Funding since only a few fish avoiding treatment could ensure the The project was funded by the Norwegian Environmental Agency. survival of the parasite and thereby reintroduce it to the Availability of data and materials fish population. A variation in the level of conductivity The datasets used and/or analysed during the current study are available from is observed in individual fish which indicate that they the corresponding author on reasonable request. are exposed to different sources of water, which under - Ethics approval and consent to participate line the importance of administering the treatment solu- Approval for the tagging experiment was granted by the Norwegian Animal tion to tributaries and other areas where water influx is Research Authority (ID 1292). observed. During the study period all detected fish sur - Consent for publication vived the experiment. This show that the Al treatment Not applicable. [5, 6] for G. salaris can be carried out without killing the Competing interests host fish populations, which was a key factor in the devel - The authors declare that they have no competing interests. opment of the method. The operation to eradicate the parasite from Lærdal was ultimately considered a success Author details Department of Civil and Environmental Engineering, Norwegian University since the control of fish in the river showed no parasite in of Science and Technology (NTNU), Trondheim, Norway. INAQ AS, Trondheim, the following years, and the river was declared free of G. 3 Norway. Faculty of Biosciences and Aquaculture, Nord University, Bodø, Nor- 4 5 salaris in the fall of 2017. way. Norwegian Institute of Water Research, Oslo, Norway. Thelma Biotel AS, Trondheim, Norway. Department of Engineering Cybernetics, Norwegian University of Science and Technology (NTNU), Trondheim, Norway. Conclusion Received: 20 November 2020 Accepted: 27 January 2021 This paper describes the development of a multi-function acoustic transmitter tag equipped with sensors for in situ measurement of water quality in terms of conductivity References and temperature. The tag transmits instantaneous meas - 1. Forseth T, Barlaup BT, Finstad B, Fiske P, Gjøsæter H, Falkegård M, Hindar urements of water quality, while it also features onboard A, Mo T, Rikhardsen A, Thorstad EB, Vøllestad LA, Wennevik V. The major processing of measurement data to obtain statistical threats to Atlantic salmon in Norway. ICES J Mar Sci. 2017;74(6):1496–513. https ://doi.org/10.1093/icesj ms/fsx02 0. information on the fish’s exposure to different water qual - 2. Johnsen BO, Jensen A. The Gyrodactylus story in Norway. Aquaculture. ities over time. The latter function provides the means to 1991;98:289–302. evaluate the water quality experienced by the fish when it 3. Soleng A, Poleo ABS, Alstad NEW, Bakke TA. Aqueous aluminium eliminates G. salaris (Platyhelminthes, Monogenea) infections in Atlantic has been out of detection range. Simultaneously, the tag salmon. Parasitology. 1999;119:19–25. emits tracking signals (pings) on a separate frequency to 4. Poleo ABS, Schjolden J, Hansen H, Bakke TA, Mo TA, Rosseland B, Lydersen facilitate efficient presence detection and fish localiza - E. The effect of various metals on G. salaris (Platyhelminthes, Monogenea) infections in Atlantic salmon (Salmo salar). Parasitology. 2003;128:1–9. tion. The tag was applied to provide data on the behav - 5. 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The study AG (2005) Experimental elimination of Gyrodactylus salaries in River provides an example of how experimental objectives may Alfredsen et al. Anim Biotelemetry (2021) 9:7 Page 14 of 14 Batnfjordselva, Northwestern Norway, with aluminium. North Inst Water 21. Finstad A, Einum S, Saettem L, Hellen B. Spatial distribution of Atlantic Res Rep 5015:30 salmon (Salmo salar) breeders: among- and within-river variation and 8. Kroglund F, Rosseland B, Teien H, Salbu B, Kristensen T, Finstad B. Water predicted consequences for offspring habitat availability. Can J Fish quality limits for Atlantic salmon (Salmo salar L.) exposed to short term Aquat Sci. 2010;67(12):1993–2001. https ://doi.org/10.1139/F10-122. reductions in pH and increased aluminum simulating episodes. Hydrol 22. Sattem L (2016) Anadromous spawning population in the river Earth Syst Sci. 2008;12:491–507. Lærdalselva, Lærdal Municipality in Sogn og Fjordane County 2016 (In 9. 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Riverine and fjord migration of wild and hatchery reared Atlantic salmon smolts. Fish Manage Ecol. 2013;20:544–52. https ://doi.org/10.1111/fme.12042 . Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : fast, convenient online submission thorough peer review by experienced researchers in your field rapid publication on acceptance support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Animal Biotelemetry Springer Journals

An acoustic sensor transmitter for in situ assessment of water quality and fish behaviour during chemical treatment of a parasite-infected river system: tag design and practical use

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10.1186/s40317-021-00230-6
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Abstract

Background: Behaviour of potential host fish during chemical treatment against the ectoparasite Gyrodactylus salaris is a vital factor in designing treatment strategies, evaluating risk factors and establishing insights into previously failed treatments. The effectiveness of any chemical treatment may be compromised if fish either are forced to, or seek out actively, areas of the river where the water quality is less affected by the chemicals. The aim of this study was to develop and apply an acoustic fish tag for fish localization with sensors for in situ measurement of water conductivity and temperature to investigate fish behaviour before, during and after an aluminium (Al) treatment. The sensor tag allowed discrimination between water qualities, and thereby quantification of exposure to treatment water. Findings: Adult Atlantic salmon and anadromous brown trout from river Lærdalselva were tagged with external con- ductivity transmitters and followed daily by a network of passive receivers and by manual tracking 1 week ahead of treatment, during a 2-week aluminium (Al) treatment period and one week after an Al treatment. The results show no avoidance behaviour related to the Al treatment and most of the fish exhibited a behaviour during the treatment that did not differ significantly from the behaviour observed before or after the treatment. Data collected from the tags showed that the fish experienced increased conductivity during Al administration, suggesting successful exposure to treatment water. The tag gave verifiable environmental information and functioned well in the turbulent and acousti- cally demanding river environment, albeit with variable detection range. Conclusions: The conductivity and temperature tag provided novel data on fish behaviour and exposure during the Al treatment period. Results show that fish exhibit normal behaviour during this period and no avoidance response can be detected in the collected data. Keywords: Acoustic telemetry, Conductivity, Salmonids, Aluminium, Water quality, CondTag, Parasite, Gyrodactylus salaris, Atlantic salmon, Anadromous brown trout Background In Norway, introduction and secondary dispersion of the *Correspondence: knut.alfredsen@ntnu.no monogenean parasite Gyrodactylus salaris has caused Department of Civil and Environmental Engineering, Norwegian severe population decline of Atlantic salmon (Salmo University of Science and Technology (NTNU), Trondheim, Norway Full list of author information is available at the end of the article salar) in infected rivers [1, 2]. The discovery of successful © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Alfredsen et al. Anim Biotelemetry (2021) 9:7 Page 2 of 14 elimination of G. salaris infections in salmon by exposure sea trout, both an upriver migration and more stable to aqueous labile inorganic aluminium (Al ) [3] has led holding behaviour would be expected [16]. For smaller to a scientific [4] and practical [5–7] efforts to develop a non-mature sea trout, one could expect both down and full-scale chemical treatment method for parasite elimi- upstream migration. The reach of the river studied is the nation while maintaining fish populations in infected main spawning area of the river, and the fish will mostly river systems. The eliminating effect on G. salaris of spawn in the mainstem. Based on the measured variables, labile/cationic Al in acidified waters was first described the sensor tag allows for discrimination between water by Soleng et  al. [3] and the extensive knowledge of bio- qualities such as ground water, brackish water, chemically logical effects of Al, including dose–response relation - treated water and the normal river water. For example, ships for host species Atlantic salmon and brown trout the groundwater runoff to the river Lærdalselva sus - in the acidification literature [8] defined treatment con - tains conductivity typically more than ten times that of −1 ditions (Al, pH). The method involves administering of river water (12–20 vs 150–350 µScm ). When attached Al as aluminium sulphate and acid (H SO ) for pH con- to fish, these transmitters can therefore be used to iden - 2 4 trol (target pH: 5.9–5.7) to obtain a desired concentra- tify areas in the river and estuary used by fish where the tion of Al between 25–30 and µg/l. While the causative chemical treatment for G. salaris might be suboptimal. agent responsible for G. salaris removal from the host Tracking fish before, during and after the treatment also fish is cationic/labile Al, adding aluminium sulphate and gives indication of the exposure to the chemical reagent additional sulfuric acid to decrease pH also results in a in the water and contributes to knowledge on behaviour marked water conductivity increase in the river during during the treatment. treatment [9]. Thus, the increase in water conductivity The study provides an example and ideas of how caused by the addition of ions and lowering of pH serves experimental objectives may be accommodated within as a practical proxy for measuring dose in  situ. At pre- the capabilities and limitations of contemporary digital sent little is known about the spatio-temporal response tag platforms. Detailed field observations showing the pattern of fish to the water quality changes during an Al dynamics of the fish’s exposure to the chemical reagent treatment period. Both experimental and field studies under the circumstances of a full-scale treatment sce- have demonstrated that Atlantic salmon is able to sense nario are given as well as documentation of no avoidance and avoid low pH [10] and in some cases also elevated behaviour both during and after treatment. concentrations of aluminium [11]. In other cases no avoidance has been observed for aluminium in Atlantic Methods salmon both in the laboratory [12] and for a combined Transmitter design low pH/increased aluminium in a field study [13]. An acoustic transmitter tag with a water conductivity and Fish behaviour during chemical treatment against G. temperature sensor was developed specifically for this salaris is a vital factor in designing treatment strategies, study to enable observations of individual behaviour and evaluating risk factors and establishing insights into pre- to quantify the exposure of fish to different water quali - viously failed treatments. The effectiveness of any chemi - ties during a chemical treatment. The tag was based on cal treatment may be compromised if fish either are an ultra-low power mixed-signal electronic design simi- forced to, or seek out actively, areas of the river where the lar to the acoustic tag platform described in Føre et  al. water quality is less affected. Areas of brackish water and [17], which allows physical miniaturization while secur- groundwater runoff are regarded as typical problem areas ing long operational life and flexibility with respect to in this respect. Avoidance and escape reactions from ele- sensor integration, on-board data processing and storage vated Al concentrations have been observed previously capacity. To sense water conductivity, the tag incorpo- [14]. rated a 4-pole gold-plated conductivity cell embedded in The aim of this study was to develop and apply an one of its end caps (Fig.  1) where the cell constant was acoustic fish tag, with sensors capable of simultaneously dimensioned according to the conductivity range typi- measuring temperature and conductivity of the sur- cal for the water in the river and estuary. Conductivity rounding water to investigate to what extent avoidance measurements were initiated and supervised by the on- behaviour occur before, during and after an Al treat- board microcontroller and involved activation of a driver ment. The tag was used to track Atlantic salmon (Salmo circuit that applied an alternating voltage of constant salar) and anadromous brown trout (Salmo trutta) dur- level to the outer pair of electrodes, while simultaneously ing the Al treatment of river Lærdalselva from August to sensing the corresponding voltage potential between September 2009. During this period the fish are on their the inner pair of electrodes and the total electrical cur- spawning run in the river and moves from the estuary rent flowing through the water. The microcontroller to their spawning sites [15]. For salmon and the mature measured the current and voltage signal for each cycle A lfredsen et al. Anim Biotelemetry (2021) 9:7 Page 3 of 14 Fig. 1 The conductivity and temperature acoustic transmitter tag (CondTag) with three concurrent transmitter functions. Transmitter function (i) sends S256-encoded messages on odd IDs that contain instantaneous measurements of conductivity and temperature, where the data byte is split in two 4-bit values serving as indices into a look-up table specifying predefined conductivity and temperature intervals. Transmitter function (ii) sends S256-encoded messages on even IDs that contain information reporting how many hours over the last 45 h the tag has resided in two predefined water quality categories ( WQC) defined on the basis of time averages and fluctuations in conductivity measurements. See Table 1 for a description of the WQCs. Transmitter function (iii) runs in parallel with function (i) and (ii) and emits a 20-ms acoustic “pinger” pulse every 5 s on one of three selectable tracking frequencies (72, 75 and 78 kHz), and is included to enable manual localization and tracking of the fish using manual receivers with a directional hydrophone. The inset image shows the tag with a 4-pole conductivity cell embedded in its endcap. The temperature sensor (not seen) is located on the opposite side of the endcap by employing a micropower instrumentation amplifier suitable for the anticipated conditions at the study site. and its integrated AD. Conductivity was calculated as Although the conductivity sensor allowed a maximum −1 an average over several cycles of the product of the cell measurement range of 0–2530 µScm , the sensor was −1 constant and the ratio between the measured current set to saturate at 200 µScm since the conductivity lev- and voltage. A calibrated NTC thermistor was embedded els of both normal river water and treatment water were in the tag’s end cap adjacent to the electrodes and was predicted to be very low. This gave a measurement reso - −1 used to sense ambient water temperature as well as com- lution of 0.2 µScm and laboratory tests proved that −1 pensating conductivity measurements for temperature accuracy was better than 1.4 µScm for these water dependency. The conductivity and temperature sensors types. The temperature sensor had a measurement range were calibrated with selectable gain and offset settings to of − 2.0 to 25.5 °C with resolution 0.03 °C and accuracy accommodate measurement ranges that were considered better than 0.3 °C. Alfredsen et al. Anim Biotelemetry (2021) 9:7 Page 4 of 14 Both continuous and more sporadic observations of one-byte data payload that can be sent during each trans- the fish were anticipated in the relatively long and var - mission, conductivity and temperature sensor measure- ied river system. For this reason, the tag was designed ments were compressed into two 4-bit binary codes by a and programmed as a multi-function transmitter in software algorithm that ran locally onboard the tag (see order to serve three different monitoring objectives Fig.  1). These codes served as indices into two look-up simultaneously: tables containing predefined conductivity and tempera - (i) Transmit periodic measurements of instantane- ture intervals. The approach employed data binning of ous electrical conductivity and temperature of the each variable into one of 16 different intervals with a tagged fish’s ambient water. nonlinear mapping between bin number and interval (ii) Calculate and transmit statistical information per- size. While having rather low resolution, the mapping taining to the tagged fish’s exposure to different technique allowed enhanced resolution in the parts of the water qualities over a defined time history. sensors’ measurement ranges considered likely to prevail (iii) Emit regular and frequent “pings” to permit manual during the experiment, at the expense of lower resolution acoustic bearing measurements and localization of in ranges that were considered less likely to occur. The the tagged fish using one of three separate tracking selection of intervals was done based on a priori knowl- frequencies. edge of typical conductivity and temperature ranges of normal river water during the relevant season, as well as In addition to manual tracking receivers, automatic values representative of the water quality during Al treat- monitoring receivers were used extensively for recep- ment, of groundwater effluences, and of the river estuary. tion of the telemetry data (Vemco VR100 and VR2W, Details of the coding scheme of conductivity and temper- Halifax, NS, Canada). This implied that transmitter func - ature intervals are given in Fig. 1. tion (i) and (ii) had to be based on an acoustic carrier Transmitter function (ii) was implemented to pro- frequency of 69  kHz and the S256 encoding of acoustic vide statistical records of the fish’s exposure to different messages [18]. The S256 encoding scheme only permits water qualities over a specified temporal horizon. With a 16-bit data payload for each message, which is equally tagged fish moving between locations in the complex divided between an 8-bit tag ID code and an 8-bit sensor and acoustically challenging habitat of the river, it was data value. Each transmitter tag was therefore allocated expected that signals would be beyond detection range two unique and consecutive ID codes, with odd and even of unknown extents of time during the experiment. Still, ID codes representing transmitter function (i) and (ii), it was regarded as important to be able to reconstruct respectively, with transmission alternating and repeating historical information concerning the fish’s exposure at random intervals of 40–120 s. On-board compression to different water qualities once the fish again could be techniques in terms of look-up tables and calculation of detected. All remaining data memory on-board the tag statistical moments were implemented in the tag firm - was thus allocated to a sliding time window data buffer, ware to convey useful sensor data within the limitation and an algorithm was developed to keep record of the of one byte per transmission. Transmitter function (iii), fish time of exposure to three different water quality the acoustic ping, was designed to operate concurrently categories (WQC0, WQC1 and WQC2), as defined in with function (i) and (ii), but at separate frequencies to Table  1. The data buffer was configured to cover a 45-h avoid acoustic interference with messages transmitted time history and was further divided into 15, 3-h inter- on the 69 kHz channel. The tag was thus programmed to vals (15 × 3 h = 45 h). For each 3-h interval, the algorithm emit short “ping pulses” of 20  ms duration every 5  s at calculated and stored the arithmetic mean and the vari- either 72, 75 of 78 kHz (depending on the tag ID), which ation, or number of fluctuation events occurring in the thereby permitted concurrent tracking of up to three conductivity measurements. A fluctuation event was co-located fish in the same stretch of the river while still defined to occur when two consecutive conductivity being able to receive instantaneous and statistical data on measurements happened to differ by a value greater than conductivity and temperature. a certain threshold value and was included to serve as an Transmitter function (i) was implemented to provide indicator of the variability in water quality experienced instantaneous conductivity and temperature readings by the fish. The sensor was sampled every 60 s giving 180 from the fish’s ambient water as S256-encoded messages. conductivity measurements per interval. Each interval This way data could be received at regular intervals using was then categorized into one of three different WQCs both automatic monitoring receivers (VR2W) that were based on these two variables following the criteria shown permanently deployed in specific pools of the river as in Table 1. At the time of acoustic transmission, the infor- well as manual receivers (VR100) that were in ambula- mation in the buffer was further compressed into two tory use during tracking campaigns. Due to the limited 4-bit codes, each encoding the number of hours the fish A lfredsen et al. Anim Biotelemetry (2021) 9:7 Page 5 of 14 Table 1 Definition of water quality categories (WQCs) Water quality Range of conductivity Number of conductivity fluctuation Description −1 −1 category average (µScm ) events (|κ —κ |> 5 µScm ) t t − 1 WQC0 0–25 And = 0 Normal river water, main stem WQC1 26–40 And < 4 Stabilized river water during Al treatment WQC2 0–25 And > 0 River water with groundwater influence, or other atypical variations in conductivity, or brackish water Or (estuary) 26–40 And ≥ 4 Or > 40 And Any WQCs are based on certain combinations of average conductivity and the variation between consecutive conductivity measurements, or fluctuation events, over a −1 3-h interval containing a total of 180 measurements. A fluctuation event was defined to happen when conductivity changed by more than 5 µScm in 60 s has spent in WQC0 and WQC1 over the last 45  h (see freshwater, had an acoustic source level of 146 dB @1 m Fig. 1). Time spent in WQC2 was not transmitted explic- re. 1 µPa, and an estimated battery life of more than itly but could be found implicitly by applying the formula 90 days. t = 45 – (t + t ). Details of the tag encoding WQC2 WQC0 WQC1 are shown in Fig. 1. Tagging procedure Following design, implementation and validation of Adult Atlantic salmon (N = 6, mean length 46.9  cm, SD the sensor tag prototype, a batch of 25 tags were manu- 16.1  cm) and anadromous brown trout (N = 16, mean factured by Thelma Biotel AS (Trondheim, Norway) for length 48.4  cm, SD 14.9  cm) (Table  2) from river Lærd- use in this study. The electronic tag that was designated alselva, Norway (Fig.  2) were caught by angling using as CondTag, had a cylindrical shape with 9  mm diame- sports fishing equipment at several sites along the river. ter and 43  mm length, weighed 6.3  g in air and 4.1  g in The species are both relevant as primary host (salmon) Table 2 Length, species and tag-id for the marked fish Tag-id instant Tag-id stat Species Length (cm) Tagged Tag site First obs Last obs 69 70 Anadromous brown trout 35 15.08 Oye 16.08 17.09 75 76 Anadromous brown trout 35 07.08 Rikheim 19.08 22.09 77 78 Anadromous brown trout 43 06.08 Rock 16.08 06.09 81 82 Anadromous brown trout 33 06.08 David (5.5) 16.08 22.09 83 84 Anadromous brown trout 35 15.08 Oye 16.08 09.09 85 86 Anadromous brown trout 35 07.08 Gronnebank 16.08 30.08 91 91 Anadromous brown trout 43 06.08 Rock 29.08 19.09 93 94 Anadromous brown trout 52 07.08 Rikheim 24.08 22.09 95 96 Anadromous brown trout 54 06.08 David (5.5) 29.08 29.08 143 144 Anadromous brown trout 38 15.08 Oye 16.08 22.09 145 146 Anadromous brown trout 31 07.08 Gronnebank 16.08 21.09 147 148 Anadromous brown trout 57.5 07.08 Per (5.3) 06.09 19.09 151 152 Anadromous brown trout 48.5 06.08 Rock 16.08 16.08 155 156 Anadromous brown trout 41.5 06.08 Per (5.3) 28.08 17.09 73 74 Atlantic Salmon 48 15.08 Rock 25.08 06.09 79 80 Atlantic Salmon 84 06.08 Robinson (15.7) 02.09 05.09 87 88 Atlantic Salmon 55 14.08 Grasmarki 25.08 20.09 141 142 Atlantic Salmon 53 14.08 Grasmarki 16.08 15.09 149 150 Atlantic Salmon 84 07.08 Sandebank (15) 24.08 22.09 The first tag id refers to the instantaneous measurement (transmitter function i), the second tag id refers to the statistical data (transmitter function ii). The tag date, tag site and first/last observation is also given. For tagging locations not named on Fig. 2, the distance from the estuary is given in kilometres. The fish were not weighed during marking, but using observed weight of similar size fish from the same river we estimated the tag burden of the smallest fish to be < 1.4%. The tag weighs 4.1 g in water Alfredsen et al. Anim Biotelemetry (2021) 9:7 Page 6 of 14 Fig. 2 Map of Lærdal with tracking stations marked along the river reach in red with names. Catch-and-release sites are marked with green and the Al release sites are marked with purple arrows. The numbers in the parentheses is the distance from the estuary. Inset: anadromous brown trout tagged with the conductivity tag and long-term intermediate host (trout) for the parasite temperature measurements (WTW Multiparameter G. salaris [19]. instrument). The tags were fitted with thin surgical steel After unhooking, fish were wet netted into a hold - wire and attached at two points just below the dorsal fin ing tank (volume 500 l) close to the riverbank. After by leading the ends of the wire through the fish using 23 20–30  min, fishes were netted directly from the hold - G (0.60 × 25  mm) syringes. The wire ends were secured ing tank into a pre-anaesthetic sedation tank containing on the opposite side by crimping on a small copper crimp −1 0.5  mg  l metomidate for a minimum of 2  min. Fishes with a 12-mm soft plastic disk as padding between the were then transferred to an anaesthetic bath containing crimp and the fish’s skin. −1 60  mg  l MS 222 (tricaine methanesulfonate) anaes- thetic [20]. Cessation of response to peduncle pinching Tracking setup was used as a criterion for surgical anaesthesia. Fishes The fish were followed by a stationary network of auto - reached surgical anaesthesia within 4 min and were then matic listening receivers (VEMCO VR2W, locations transferred to a tank with river water where the tagging shown in Fig.  2 and by daily manual tracking (first by was conducted. During surgery the head, gills, and most manually deploying a VEMCO VR2W at each release of the body of each fish were submerged in water. Total location and later using a portable VEMCO VR100 handling time was around 2  min per fish. Immediately directional hydrophone during August and September after tagging, the fish were transferred to a recovery tank of 2009. Manual tracking was conducted in the river with river water (80 l) with circulated flow and closely each day between the 14th of August and the 10th of monitored. Fish regained balance ability and showed September from 0800 to 2000 by following the same active swimming behaviour within 0.5–2  min of recov- route. Manual tracking was also done on the 16th and ery. After a recovery period of 5–6  min, the fish were 18th of September. This was done by walking upstream released into the river at the same site as it was angled. along the riverbank and placing both a passive receiver During recovery, tag readings were made and compared and the hydrophone of manual receiver into the river with data from a control tag permanently installed in at different sections of the pools. In pools where fish the revival tank as well as manual conductivity and were detected for more than 2 days, a passive receiver A lfredsen et al. Anim Biotelemetry (2021) 9:7 Page 7 of 14 was deployed. Once deployed in the river the passive Lærdalselva is a clearwater river and visual count- receiver was at the same location during the whole ing of salmonid spawners has been conducted from the study period. These passive receivers were offloaded early 1960s [21, 22]. The clear water made it possible to daily to check if there had been registered movement of check the status of sensor/fish that had an observed fixed tagged fish during night-time. position in the river by snorkelling. One person drift- The stationary receivers were mounted on the river ing downstream by snorkelling and one person on the bottom either using blocks of concrete or specially riverbank to register position and observations carried designed metal stands. Each site except Rikheim had out this procedure. The surveys were conducted both one receiver and range tests were performed to ensure in the upper part (Robinson–Rikheim) and in the lower coverage of the entire river width. Lærdalselva is a part (Badehølen–Bruhølen). The diver observed natural relatively small river (widths 30–60  m) and all sites behaviour in the fish encountered and fish with tags were are easily accessed on the bank. The data from the sta - seen. No dead fish were observed. tionary network and the manual tracking data were combined into a common dataset used in the analy- Other data sis. For the analysis of the fish behaviour, three phases, Two reference tags were placed at Bø and Øye together before (defined from the 16th of August to the 23rd of with the hydrophones. A continuous measurement of August), during (defined from the 26th of August to temperature was carried out during the experiment at the the 6th of September), and after (defined from the 8th same locations by connecting a Vemco Minilog II to the of September to the 15th of September) the Al treat- hydrophone stand. Water quality was monitored manu- ment, were specified to get a consistent comparison ally during the treatment period. Discharge is measured of individual fish and to avoid effects of different time at the Stuvane gauge (NVE station 73.2.0) with a time of release of the fish after tagging. A gap of 2 days is resolution of 30  min. Stuvane is located close to the defined after the start of the treatment on the 24th of Rikheim site (Fig. 2). August to allow for the treatment to cover the entire river. Similarly, a gap of 1 day is defined between the Aluminium treatment period of treatment and the start of the after period to Aluminium sulphate was added to all tributaries, as well allow the treatment chemicals to be transported out of as at several sites along the main river stem to obtain tar- the system. The different phases of the study period are get concentrations all over the river system. In addition, indicated in Fig.  3, which also shows the discharge in the main river was acidified using sulphuric acid (30%) the reach during the treatment period. Data were also to bring pH down to effective treatment levels where Al collected after the 15th of September to check move- is labile/cationic. Monitoring was done by using conduc- ment and further ensure that fish were alive. For more tivity, pH and Al fractionation (Barnes–Driscoll). As the information on the receiver network used in the experi- latter being very labour intensive, mainly the two former ment in river Lærdalselva, see Urke et al. [20]. methods were used for direct control. The pH measure - ments were used as a feedback to the dosing stations and conductivity for daily dose control. Conductivity is not strongly related to discharge in this river system and is very low naturally. Monitoring stations upstream of the dosing sites confirmed the increase in conductivity dur - ing treatment, and the pre- and post-treatment measure- ments also confirm this quite consistently. Statistical analysis The relationship between movement and discharge was tested by computing the sum of movements for each half- hour interval that matched the discharge observations and then testing the number of movements against dis- charge and change in discharge using linear regression. A movement was counted when the fish was found in differ - ent locations in two consecutive observations. Conduc- Fig. 3 Discharge over the study period measured at the Stuvane gauge (located at the Rikheim tracking station). The coloured panels tivity data were checked for normality using qq-plots and shows the periods of analysis: a prior to treatment, b treatment histograms, and since the data were skewed, a Box Cox period, c after treatment transformation was applied to the data using the package Alfredsen et al. Anim Biotelemetry (2021) 9:7 Page 8 of 14 EnvStats in R [23]. The changes in conductivity among did a similar test on individual fish using ANOVA over the periods before, during and after treatment was then all three periods and t tests on pairs of periods for each tested by first computing the averages for each fish for of the fish that had recordings over different periods. All each period and then testing this using ANOVA across analysis was done using the R software [24]. all periods and then a t test between periods, before– during, during–after and before–after. Furthermore, we Results To control the tag reading of temperature and conductiv- ity, measurements were made in the recovery tank after surgery using a calibrated instrument (WTW multipa- rameter instrument). These were then compared to assess the accuracy of the tags. The recordings confirmed good correspondence between the measurement of tempera- ture and conductivity from the tags and the instrument (Fig. 4, panel a shows temperature, panel b conductivity). This also confirmed that all tags were working at the time of release of the fish. Of the 22 tagged fish, 19 were detected either by man - ual tracking or fixed receivers during the study period as indicated in Fig.  5. We find it most likely that the three fish found during the study period were located in areas with difficult acoustic conditions and therefore dif - ficult to detect, but we cannot rule out mortality or tag Fig. 4 Comparison conductivity and temperature measured with the tag and a temperature/conductivity meter. Panel a shows water malfunction. The fish could also have moved out of the temperature and panel b shows the conductivity study area. Twelve fish were recorded throughout the Fig. 5 The figures show at which tracking locations each fish is observed over the time period as a function of the distance to the river estuary. The coloured panels show the same time periods as in Fig. 3. The graph is extended 1 week after the “AFTER” period to capture movement of fish. See Fig. 2 for more information on locations and distances along the river A lfredsen et al. Anim Biotelemetry (2021) 9:7 Page 9 of 14 experimental period in relation to fixed receiver stations in the river, and the remainder were detected one or sev- eral times during the manual tracking campaigns. A total of 32,285 detections were made during the study period, distributed with 4454 before, 14,687 during, and 13,144 in the period after the treatment. The position and movement of each individual fish are shown in Fig. 5, where the position of the fish is related to its distance from the river estuary. Relatively few move- ments were observed among the fish during the track - ing period. From the data in Fig. 5, it is evident that only three fish out of 19 (16%, tags 73, 77 and 85) show down - Fig. 6 Box plot showing the average conductivity for all fish stream movements during the period. This occurred dur - distributed on the three time periods. The conductivity interval is ing treatment for two of the fish, but both of these fish given in table (i) in Fig. 1. The p values related to the Anova test on returned to their original position after some time. The differences between the periods are shown in the graph. The thick third fish moved 900  m downstream before the treat - line represents the median, the box shows the inner quartile range ment started and stayed there. Five fish showed a distinct (IQR) and whiskers are at 1.5 * IQR upstream movement during the study period (26%, tags 69, 83, 141, 143 and 155). All upstream movements took place after the treatment period, and the longest move- raises the conductivity in the river followed by a reduc- ment was 9.6 kms. The remainder of the tagged fish (58%) tion back to the level seen in the period before treatment held position at one site during the entire period. The when the treatment is over. largest number of movements was observed in the period Further, an analysis of each individual fish between after the treatment, but no significant differences exist periods was carried out; see Fig.  5 for the periods where between the three periods. To check if discharge had an each tagged fish is observed. For the fish with observa - influence on movements, the number of movements was tions in all three periods, an ANOVA test shows that summed for each half-hour (resolution of the discharge there is a significant difference between the periods times series) and linear regression between instantane- (p < 0.001). For fish with observations for the period ous discharge and the change of discharge were carried before and during treatment, with one exception a t-test out. This shows no pattern connecting observed move - shows a significant increase in experienced conductivity ment to the observed variability of discharge over the for each individual fish during the treatment (p < 0.001 study period, movement vs. instantaneous discharge for all fish). The exception is an anadromous brown trout (r < 0.001, p > 0.05) and movement vs. changes in dis- (tag 83) in the lower part of the river that shows only a charge (r < 0.001, p > 0.05). However, the observed rises slightly increase in median conductivity from before and falls reside within normal variations in discharge and treatment to the treatment period. For fish recorded both could not be considered as floods. in the treatment period and the period after treatment, The average experienced conductivity of each fish based we see a significant reduction in conductivity for all indi - on the full set of telemetry data is shown in Fig. 6. There viduals (p < 0.05). When we compare the period before is a significant difference in conductivity experienced treatment to the period after treatment, the picture is by the fish between the treatment periods (ANOVA, mixed. Some fish are seen to return to the same level of F = 7.797, p < 0.01). Looking at the different periods, we conductivity as before the treatment, while for a few indi- see a significant increase in conductivity between the viduals we still see a significant difference in experienced period before treatment and the treatment period (t conductivity. test, t = − 3.6623, p < 0.01). We also see that the increase As an example of observed conductivity in individual in conductivity observed in the telemetry data from the fish, Fig.  7 shows three fish (tags 75, 93 and 149) located fish tags during the treatment period corresponds with at the Rikheim site 14.7  km from the estuary. These fish an increase measured in the river for the same period. were present at this site for long periods during the study, We do also see a significant reduction in conductivity and the results show individual variations that appear to between the treatment period and the period after (t test, be linked to the specific locations of the fish in the pool, t = 3.0755, p < 0.01). For the period before and period which were determined by taking cross-bearings of the after treatment there are no significant difference in the fish’s ping pulses (transmitter function iii). The tributary conductivity experienced by the fish (t test, t = − 1.3099, Nivla enters the Rikheim site from the south, and this p > 0.05). For the full period, we see that the treatment Alfredsen et al. Anim Biotelemetry (2021) 9:7 Page 10 of 14 rise in river discharge, which could be the reason for loss of reception either by the fish moving out to an area not covered by the receiver or a deterioration of the acous- tic channel. When the fish was detected again on the 2nd of September, the first message reveals that the fish had been in stable and low conductivity water (WQC0) over the entire 45-h period preceding the reception of that message, including the 17 h when reception was lost. For the second gap, the fish was out of detection range for about 20 h, from the 2nd of September 14:30 to the 3rd of September 10:30. The first message received on the 3rd of September after the gap shows that the fish had sustained 6  h of exposure to water of elevated and/or fluctuating Fig. 7 Measured conductivity intervals for the fish (tag 75: conductivity levels, and correspondingly a 39  h of expo- anadromous brown trout, 35 cm, tag 93: anadromous brown trout sure to normal river water over the last 45  h. Increasing 52 cm, tag 149: Atlantic salmon 84 cm) located at tracking location exposure to elevated and/or more unstable levels of con- Rikheim during the three analysis periods. The boxes show the same distribution as in Fig. 6. Conductivity intervals given in table (i) of ductivity can be seen in the following hours, a tendency Fig. 1 that continued towards the end of the treatment period and corresponded well with the change in general river water conductivity during the treatment. When the treat- stream discharge water of a natural higher conductivity ment ended, the tag reported an increasing prevalence level than the main river stem. The fish with tag 93 was of WQC0 (normal river water) with some lag due to the located at the entrance of the tributary for most of the 45-h sliding window buffer, as should be expected. time and this shows up as a higher level of conductivity measured by the tag when compared to the other two fish Discussion which took other positions in the pool. A number of daily In this paper, we present the design of a multi-function measurements at the Nivla outlet during the treatment acoustic sensor tag and the results from its practical use −1 period gave a median conductivity of 43 µScm (interval on adult Atlantic salmon and anadromous brown trout −1 7), and the median tag value gave 37.5 µScm (interval during a chemical Al treatment of the river Lærdalselva −1 6). The two other fish had a median value of 22.5 µScm in Norway. Movements seen in the fish both during and (interval 3) during the treatment period. after the treatment can be considered as natural migra- The statistical function of the tag provided informa - tory behaviour in Atlantic salmon and brown trout dur- tion on the time spent in different water quality catego - ing this period of the year. The effect of the Al treatment ries (WQCs) over a 45-h sliding time window, as outlined on the fish’ ambient water could be observed indirectly in the section on tag design and Fig.  1. Figure  8 shows a as an increased level of conductivity in the measure- situation where a fish (tag 81) intermittently came out ments received from the tagged fish. This demonstrates of detection range and introduced significant gaps in the utility of the sensor tag as a tool for in  situ evalua- the data received from this fish, but where the statisti - tion of the treatment process and it further confirms that cal recordings (transmitter function ii, Fig.  1) could be the fish were exposed to the active reagent during the applied to evaluate the fish’ continuous exposure to dif - treatment. The main conclusion from the movement and ferent water qualities irrespective of intermittent loss of conductivity data is therefore that the tagged fish showed contact. Each bar depicts a reception of a single statisti- no obvious signs of flight or avoidance behaviour upon cal message and shows the fraction of time where the fish exposure to the chemicals during the treatment. This is was exposed to WQC0 (normal river water—blue colour) an important observation related to the effectiveness of or the combination of WQC1 and WQC2 (treatment/ the treatment. atypical water—red colour) of the preceding 45-h period. In addition to sending regular instantaneous measure- Instantaneous values are indicated as dots on top of the ments on water conductivity and temperature, the tag plot. Panel a shows the full dataset, while panel b details was programmed to carry out an onboard analysis of a subset of the data where the fish came out of detec - an internally stored time history of conductivity meas- tion range at two occasions and caused significant gaps urements and report exposure times to different pre - in the recordings. The first gap lasted ~ 17  h, from the defined categories of water quality. This function was 1st of September 16:00 to the 2nd of September 09:00. It implemented to prevent discontinuities and gaps in should be noted that this gap coincided with a distinct the received datasets due to anticipated limitations in A lfredsen et al. Anim Biotelemetry (2021) 9:7 Page 11 of 14 Fig. 8 Statistics plot for fish with tag ID 82 (anadromous brown trout, 33 cm). Panel a shows the full period and panel b a shorter period between 1st and 3rd of September. The colour of the bars indicates the number of hours the tag has been exposed to the different conductivity categories over the last 45 h, T_WQC0 is low and stable conductivity and TWQC1_2 combines the high and fluctuating categories (see Fig. 1 for more info). The dots on each panel indicate the instantaneous conductivity interval recorded by the tag when detected (table i, Fig. 1) acoustic coverage and signal quality that are caused by observations show that the fish was once again exposed the complex environment and turbulent conditions of a to water affected by the reagents at the end of the treat - river. Given that the tag could be detected again within ment period. This observation corresponds well with the time window spanned by its internal data buffer measured conductivity just downstream of the fish loca - (45  h in this case), valuable aggregated information on tion and where an incident in early September when high the prevailing water quality conditions when the fish was flow of water with low aluminium concentration from beyond detection range would be secured. The utility of the tributary Kuvella led to a period of low concentration this function was clearly demonstrated in the case of an of Al in the main river, which was seen as a reduction in −1 −1 anadromous brown trout (tag 81) that was monitored at conductivity from 24 µScm to 20 µScm measured in the site Badeholen throughout most of the study (Figs.  2 the river just downstream of the fish location. and 5), but was intermittently lost towards the end of From a technical perspective, it should be noted the treatment period creating gaps in dataset of instan- that the statistical function was implemented without taneous conductivity measurements (Fig.  8). From the including any additional components like memories or received data on exposure time to different water quality computing power to the electronic tag platform. It was categories it was nevertheless possible to conclude that exclusively implemented by writing new firmware that this fish had resided in what was categorized as normal exploited already existing hardware resources with only river water (WQC0) during those intervals. However, minor costs in battery life due to the extra processing Alfredsen et al. Anim Biotelemetry (2021) 9:7 Page 12 of 14 requirements. This demonstrates the flexibility and required to comply with the severely limited bandwidth capacity provided by contemporary digital electronic of the acoustic telemetry link. The selection of param - fish tags to carry out on-board processing and analysis eters, such as conductivity and temperature bin sizes, of sensor signals prior to transmission over the severely averaging intervals and length of the sliding time window, bandwidth-limited acoustic channel, a concept that has threshold for conductivity fluctuation events, and specifi - been utilized successfully in several subsequent telem- cation of the different water quality categories (WQCs), etry studies [17, 25–27]. Even if the recorded sensor data all have direct impact on the relevance and quality of the must undergo substantial compression and loss of detail data that may be harvested from the tags. Moreover, the before acoustic transmission, the approach features an parameters need to be selected prior to the actual study advantage over archival tags in that no recapture of the and depend on rather detailed a priori knowledge of the tag is needed to recover the data [25]. conditions that will prevail during the study. This infor - The tag also incorporated a concurrent acoustic mation may not be fully available at the time of the tag “pinger” function in order to support manual localization design and programming, particularly if the study is and tracking of the fish with directional hydrophones. novel and data background is sparse. To avoid interference with the S256-encoded acoustic Efforts were made in this study to establish the configu - messages at 69  kHz, pings were emitted every 5  s on a ration parameters as accurately as possible based on prior separate frequency. This was shown to work as intended analyses of the water chemistry of the river Lærdalselva, and proved to be a time-saving feature of considerable both in its normal state and during earlier Al treatments practical value during manual tracking campaigns where [9]. However, in hindsight, several changes in the param- multiple pools and long stretches of the river had to be eter selection could be envisioned in order to improve surveyed. The frequent pings provided rapid confirma - the performance of the tag. With the conductivity values tion of the presence or absence of fish, which would not experienced during this study, it would have been ben- be the case if the much less frequent S256 signals (up to eficial to select the conductivity intervals with a higher −1 2 min) had to be used for this purpose. The pinger func - resolution in the lower ranges (< 40 µS/cm ) at the tion was also instrumental in determining the exact expense of lower resolution in the higher ranges. No fish position of the anadromous brown trout (tag 93) at the were observed to enter either the estuary or areas with Rikheim site which reported elevated conductivity levels water of high ionic strength such as groundwater efflu - compared with two other fish residing in the same pool ents during the experiment, and the ability to detect such (Fig.  7). Localization of the anadromous brown trout at water qualities could in any case be limited to a couple −1 the outlet of the tributary Nivla, which naturally sus- of wide conductivity intervals above 40 µS/cm . Moreo- tains water of higher conductivity, warranted plausible ver, since temperature readings were of limited use in this explanation of the sensor readings and that the observa- study, a relocation of one or two bits from the tempera- tion could not be attributed to the fish taking refuge in ture field to the conductivity field of the S256 code would an unknown effluent of untreated water (e.g., groundwa - double or quadruple the resolution of the conductivity ter), and thereby compromising the efficiency of the Al intervals, respectively. This would undoubtedly make dis - treatment. crimination of normal river water from treatment water In general, the acoustic receivers worked well in the significantly clearer and such adjustments in the tag con - stream environment, but turbulence in some areas made figuration parameters would be straightforward to imple - manual tracking time-consuming and required accurate ment in similar studies in the future. positioning of the receiver to detect the transmissions. Acoustic tags have been used in river environments The simultaneous bankside tracking with the VR-100 and both for Atlantic salmon smolts [20, 28, 29] and adults approaching the fish by snorkelling confirmed that fish [30, 31], and provides a well-tested approach for tracking transmitting a signal from the same location over a long migratory fish in rivers [32]. Davidsen et  al. [26] used a period indeed were alive. A lower detection of fish tagged variation of the presented conductivity tag to track ana- in the upstream part of the study site (from Rikheim and dromous brown trout (Salmo trutta) during the CFT upstream) was observed during the experiment. Snorkel- Legumin treatment of the river Vefsna to eradicate G. ling confirmed that fish was alive, but heavy riffles and air salaris. They found no avoidance behaviour and no sur - entrainment made detection more difficult. No dead fish vival, which indicate a successful rotenone treatment. were observed in any of the snorkelling surveys. Similar to the findings of Davidsen et al. [26], there were One of the main challenges of the tag design pre- no avoidance behaviour in the Atlantic salmon and ana- sented in this study relates to the selection of appropriate dromous brown trout tagged in the study presented here, parameters for processing and analyses, as well as achiev- but in contrast no mortality was recorded which is an ing sufficient compression of the sensor data, which is advantage of the Al treatment method. In another study, A lfredsen et al. Anim Biotelemetry (2021) 9:7 Page 13 of 14 Mitamura et al. [27] used a tag based on the design pre- be accommodated within the processing capabilities of sented here to measure salinity during seaward migration contemporary digital acoustic tag platforms. of Atlantic salmon in a fjord in Norway. They utilized Acknowledgements both the conventional tracking method and the storage The authors are grateful for the assistance given by T. Grimelid, Ljøsne Hatch- feature of the tag to record the salinity, and found that the ery and R.A. Golf, The Norwegian Nature Inspectorate (SNO). The reported work was financed by the Norwegian Environment Agency. The authors thank statistical data stored on the tag both provided a longer H.R. Astrup and O. Wendelboe for their hospitality during the field work. record of data and insight into fish using low salinity areas also in the outer fjord which would be difficult to Authors’ contributions AaG and JAA designed the acoustic tag based on specifications given by HAU obtain with a conventional tag and tracking setup. and TK. HAU, TK, AGH and JAA designed the experiment. All authors partici- As mentioned above, the data from the tagging experi- pated in the field work. MK, KTA, JAA, HAU and TK performed data preparation ment in river Lærdalselva show no obvious response in and analysis. KTA wrote the manuscript with input from all other authors. All authors read and approved the final manuscript. the fish during the release of Al and acid to remove G. salaris. This is important for the success of the procedure Funding since only a few fish avoiding treatment could ensure the The project was funded by the Norwegian Environmental Agency. survival of the parasite and thereby reintroduce it to the Availability of data and materials fish population. A variation in the level of conductivity The datasets used and/or analysed during the current study are available from is observed in individual fish which indicate that they the corresponding author on reasonable request. are exposed to different sources of water, which under - Ethics approval and consent to participate line the importance of administering the treatment solu- Approval for the tagging experiment was granted by the Norwegian Animal tion to tributaries and other areas where water influx is Research Authority (ID 1292). observed. During the study period all detected fish sur - Consent for publication vived the experiment. This show that the Al treatment Not applicable. [5, 6] for G. salaris can be carried out without killing the Competing interests host fish populations, which was a key factor in the devel - The authors declare that they have no competing interests. opment of the method. The operation to eradicate the parasite from Lærdal was ultimately considered a success Author details Department of Civil and Environmental Engineering, Norwegian University since the control of fish in the river showed no parasite in of Science and Technology (NTNU), Trondheim, Norway. INAQ AS, Trondheim, the following years, and the river was declared free of G. 3 Norway. Faculty of Biosciences and Aquaculture, Nord University, Bodø, Nor- 4 5 salaris in the fall of 2017. way. Norwegian Institute of Water Research, Oslo, Norway. Thelma Biotel AS, Trondheim, Norway. Department of Engineering Cybernetics, Norwegian University of Science and Technology (NTNU), Trondheim, Norway. Conclusion Received: 20 November 2020 Accepted: 27 January 2021 This paper describes the development of a multi-function acoustic transmitter tag equipped with sensors for in situ measurement of water quality in terms of conductivity References and temperature. The tag transmits instantaneous meas - 1. Forseth T, Barlaup BT, Finstad B, Fiske P, Gjøsæter H, Falkegård M, Hindar urements of water quality, while it also features onboard A, Mo T, Rikhardsen A, Thorstad EB, Vøllestad LA, Wennevik V. The major processing of measurement data to obtain statistical threats to Atlantic salmon in Norway. ICES J Mar Sci. 2017;74(6):1496–513. https ://doi.org/10.1093/icesj ms/fsx02 0. information on the fish’s exposure to different water qual - 2. Johnsen BO, Jensen A. The Gyrodactylus story in Norway. Aquaculture. ities over time. 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Riverine and fjord migration of wild and hatchery reared Atlantic salmon smolts. Fish Manage Ecol. 2013;20:544–52. https ://doi.org/10.1111/fme.12042 . Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : fast, convenient online submission thorough peer review by experienced researchers in your field rapid publication on acceptance support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions

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Animal BiotelemetrySpringer Journals

Published: Feb 4, 2021

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