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Survival, healing, and swim performance of juvenile migratory sea lamprey (Petromyzon marinus) implanted with a new acoustic microtransmitter designed for small eel-like fishes

Survival, healing, and swim performance of juvenile migratory sea lamprey (Petromyzon marinus)... Background Little is known about the transformer stage of the parasitic lampreys, a brief but critical period that encompasses juvenile out‑migration from rivers to lakes or oceans to begin parasitic feeding. Information about this life stage could have significant conservation implications for both imperiled and invasive lampreys. We investigated tag retention, survival, wound healing, and swim performance of newly transformed sea lamprey (Petromyzon mari- nus) implanted with a new micro‑acoustic transmitter, the eel–lamprey acoustic transmitter (ELAT ), in a controlled laboratory environment. Results The 61‑ day survival of our tagged subjects was 71%, within the range reported in similar studies of juve‑ nile lampreys. However, survival was significantly lower in the tagged animals (vs control), with no effect statistically attributable to measures of animal length, mass, condition, or population of origin (Great Lakes vs. Atlantic drainage). Mortality in tagged fish was concentrated in the first four days post ‑surgery, suggesting injury from the surgical pro ‑ cess. An unusually long recovery time from anesthesia may have contributed to the increased mortality. In a simple burst swim assay, tagged animals swam significantly slower (− 22.5%) than untagged animals, but were not signifi‑ cantly different in endurance swim tests. A composite wound healing score at day four was a significant predictor of maximum burst swim speed at day 20, and wound condition was related to animal mass, but not length, at the time of tagging. Conclusions Impairments to survival and swim performance of juvenile sea lamprey implanted with the ELAT trans‑ mitter were within currently reported ranges for telemetry studies with small, difficult to observe fishes. Our results could be improved with more refined anesthesia and surgical techniques. The ability to track migratory movements of imperiled and pest populations of parasitic lampreys will improve our ability to estimate vital rates that underlie recruitment to the adult population (growth, survival) and to investigate the environmental factors that regulate the timing and rates of movement, in wild populations. *Correspondence: Taylor F. Haas Haastayl@msu.edu Full list of author information is available at the end of the article © The Author(s) 2023. 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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. Haas et al. Animal Biotelemetry (2023) 11:9 Page 2 of 15 Keywords Lamprey, JSATS, ELATS, Acoustic Telemetry, Survival, Burst Swim, Endurance Swim, Wound Healing, Surgery Background sea lampreys would allow treatment decisions to be Migration is a time of heightened threat and uncertainty made based on probable parasite production vs. larval regarding the risk of predation and the localization of abundance, incorporating system-specific differences critical resources [60]. This is particularly so when migra - in rates of survival through migration and first feed - tion occurs early in life, when variation in daily growth ing. For example, in Lake Michigan, the lower reaches and survival may be substantial and influence recruit - of rivers systems often contain drowned river mouth ment to the adult population [24, 37]. A number of eco- lake–wetland complexes that are rich in piscivorous nomically and ecologically valued fishes exhibit juvenile predators [38], and piscivores are important predators feeding migrations from rivers into lakes or oceans, of out-migrating juvenile lampreys [48, 58, 62]. Life including salmon (Oncorhynchus spp.) and lake sturgeon stage-specific spatial population models for sea lam - (Acipenser fulvescens). Threats to the viability of these prey currently assume all out-migrating sea lamprey populations, and to control invasive species with simi- have an equal likelihood of survival until arrival in the lar life histories, have prompted considerable interest in lakes, regardless of differences in migratory distance, ascertaining the behavior, timing, and survival of juvenile river size, habitat types, or predator populations, each fishes as they move downstream [35, 56]. of which contribute to differences in mortality and Several lamprey species are among the most poorly growth among watersheds [31, 59]. understood fishes that exhibit juvenile migration, includ - Survival estimation during migration requires track- ing species that range from imperiled and ecologically ing an animal’s status over considerable distance and/ or commercially valued (e.g., Pacific lamprey Entos - or time. The most frequently used tool to monitor the phenus tridentatus, European river lamprey, Lampetra movements of fishes and other aquatic organisms over uv fl iatilis, sea lamprey Petromyzon marinus in select large distances is telemetry, involving the implantation European regions) to pestilential and targeted for reduc- or attachment of a transmitter that may be detected tion (e.g., invasive sea lamprey in the Laurentian Great when the fish moves into the range of a receiver [32]. Lakes). These lampreys spawn in rivers, after which Until recently, small (≤ 12 mm) passive integrated tran- newly hatched larvae (ammocoetes) bury in stream sedi- sponder (PIT) tags were the only transmitters avail- ments for typically four to seven years feeding on organic able for the study of out-migrating lamprey. PIT tags detritus and algae [14]. At the end of the larval stage, lack an internal power source, requiring tagged fishes they transform and migrate downstream into estuaries to move within 1–2  m of the antenna to be detected or large lakes to commence parasitic feeding on fishes [3, 53]. The proportion of PIT-tagged larval and out- [1, 14, 21]. This period of physiological and geographi - migrating lamprey detected by PIT antennas is rela- cal transition (aka the transformer stage) [9] is of short tively low, with reported detection rates ranging from duration, yet is considered critical to the development 5 to 14% [13, 47]. Internally powered telemetry tags of effective conservation and management practices (acoustic and radio transmitters) offer an alternative [21]. For example, out-migrating lamprey within their that substantially increases the detection range (tens native ranges typically must transit through a gauntlet of to hundreds of meters) and detection probability (as dams and their affiliated water intake structures, result - high as 80–100% on a well-designed array covering ing in physical injury, increased predation, and direct the entirety of the stream channel) at a single receiver or delayed mortality [27, 48]. Providing for safe passage [45]. Acoustic transmitters have several desirable prop- through these structures is necessary for the protection erties for use in small fishes, in particular, they do not of the species [26]. require an external trailing antenna (as radio telemetry In the Laurentian Great Lakes, where a single sea typically does), that may result in negative impacts to lamprey may consume upwards of 21 kg of fish biomass, swim performance, lower likelihood of predator attack, control is achieved through the application of selective and higher survival in tagged individuals (reviewed by pesticides (lampricides) to kill larvae in streams prior Crossin et al. [11] and references therein). to transformation [5, 43]. Rivers are selected for lampri- A primary assumption of telemetry analysis is the cide treatment based on estimates of larval abundance, fish’s movement behavior (e.g., swim speed, timing) is informed by population models and expert opinion not substantially altered by bearing the tag, or because [34]. The ability to estimate the fate of out-migrating of the implantation process. Historically, acoustic Haas  et al. Animal Biotelemetry (2023) 11:9 Page 3 of 15 transmitters have proven too large to implant into small inflammation, and a composite score that combined the fishes with narrow body cavities. Transmitters with two measures into an overall measure of wound condi- sufficient battery life to support demographic stud - tion. Swim performance was analyzed by comparing ies of fishes require large batteries that would impede two performance metrics, maximum burst swim speed movement and survival in small fishes (Liedtke 2019). (20 days post-surgery) and time-to-exhaustion swimming This situation is compounded in anguilliform swim - (29–31  days post-surgery), to untagged control fish. We ming fishes, where tags may physically impede propa - focused on the animal’s burst swim ability, as it is a facul- gation of the propulsive wave or compress organs tative behavior suggestive of ability to escape a perceived along the length of the very narrow body. The fabri - threat, and swim-to-exhaustion, as it is characteristic of cation of a novel microbattery and transmitter suit- long stretches of active swimming during a migration able for use in juvenile sea lamprey—the Eel–Lamprey [19]. The swim measures were separated by ten days to Acoustic Tag or ELAT—offers a potential solution to ensure the stress of the burst swim test did not influence this problem [15, 39]. This tag is compatible with the the results of the time-to-exhaustion test. All measures JSATS (Juvenile Salmon Acoustic Telemetry System) were statistically compared to a group of 54 control ani- receiver, with a detection range of 80–140 m, a distance mals that did not experience the anesthesia, surgery, or 100 × greater than the approximate range of a 12  mm tag implantation. Due to the difficulty in acquiring this PIT tag [17]. The transmitter has a source level of a life history stage in sea lamprey, subjects were collected 147 dB and is in a cylindrical encasing with dimensions from both Great Lakes and Atlantic basin drainages. 12 mm × 2 mm, 0.08 g dry-mass and transmits at a fre- Where appropriate, source was included as a covariate in quency of 416.7  kHz (± 0.5%). Currently, the standard the statistical models. PRI (Pulse Rate Interval) of five seconds allots approxi - mately 30  days of use [16]. Pilot field studies using the Collection and housing of subjects ELAT tag have demonstrated the high detection rates Sea lamprey used in this study were collected from trib- (> 95%) in juveniles of both Pacific lamprey and Ameri - utaries in the Great Lakes Basin (N = 64), and a hydro- can eel (Anguilla rostrata) [17, 39]. At approximately power diversion canal on the Connecticut River that the same size as the PIT tags used in previous stud- flows into the Atlantic Ocean (N = 49). ies of juvenile lampreys (12  mm x 2  mm, 0.08  g), this We selected 113 sea lamprey ranging 140 mm–160 mm is the first acoustic telemetry tag that does not persis - total length (TL) based on recommendations from pre- tently violate the two percent of body mass standard vious studies using similarly sized PIT tags in juvenile for use without impediment of movement in juvenile sea lamprey [63] and Pacific lamprey [46]. We chose to anguilliform fishes due to its cylindrical shape [46, 53, include animals across a range of sizes near the median of 63]. Here, we report an assessment of tag retention, the size distributions in the Great Lakes and the Atlantic survival, wound healing, and impacts to swim perfor- basin (Fig.  1) to examine the relationship of body size to mance of the ELAT transmitter surgically implanted wound healing and swim performance. into newly transformed sea lampreys. Our goal was to Subjects were housed at the U.S. Geological Survey perform a comprehensive evaluation of the impacts of Hammond Bay Biological Station from February 11, 2020 ELAT transmitter implantation to support the estab- to April 13, 2020. Lampreys were separated by source and lishment of criteria for use in field studies designed to kept in eight separate 23L 40 cm x 22 cm x 26 cm tanks enumerate critical demographic parameters (e.g., stage- that were supplied with constant flow-through water specific mortality rates) and the movement ecology of from Lake Huron and continuous aeration. As our find - the poorly understood transformer stage. ings are intended to inform use of the ELAT tag in natu- ral rivers, the holding tanks were constructed to include Methods: certain natural features the animal would experience dur- Study design ing out-migration. First, previous tagging effects studies The objective of this study was to examine the effects observed fungal growth and infection on experimental of the ELAT tag on sea lamprey survival, condition, subjects held in the laboratory [7, 49, 50]. To ensure the and swim performance. To achieve this, we surgically microbiome the sea lamprey were exposed to was akin implanted ELAT tags into 59 newly transformed juve- to the natural flora, we lined the tanks with a 4 cm layer nile parasitic sea lamprey and examined tag retention, of mixed substrate (cobble, sand, fine-grained sediment) survival, wound healing, and swim performance dur- collected from nearby Schmidt’s Creek. In addition, ing a 61-day study period, corresponding to anticipated unfiltered inflowing water from Lake Huron was heated tag life at a PRI of 10  s. Wound healing assessment to a temperature typical of central Lake Michigan tribu- involved two scoring metrics, wound closure and wound taries during the fall migration (~ 4.5° C). Haas et al. Animal Biotelemetry (2023) 11:9 Page 4 of 15 using doses recommended for teleost fishes. Stage-IV anesthesia was induced in (mean ± 1 SD) 17.0 ± 4.5  min −1 via immersion in a solution of 0.7  ml  l AQUI-S-20E (eugenol concentration = 70  ppm). When each animal reached stage-IV anesthesia, it was placed on a damp sur- gery board and the surgeon (T.F. Haas) made a lateral 3  mm incision into the body cavity adjacent to the 13th myomere using a Premier Edge Restricted Depth 3  mm microscalpel (OASIS Medical). A disinfected (immer- sion in 70% ethanol for ≥ 2  min) then rinsed transmitter was inserted posteriorly into the opening until it was com- pletely enveloped in the animal’s body cavity (mean ± 1 SD = 1.4 ± 0.93  min, range = 0–4  min); no suturing or other method of artificially closing was used [13, 14, 49]. After the transmitter was fully inserted, each animal was placed into an oxygenated recovery tank until active swim- Fig. 1 Density plots of total length (mm) for historic collections of ming or suction attachment to the side of the tank was out‑migrating juvenile sea lamprey for animals captured from Great observed, indicating initial recovery (mean ± 1 SD time to Lakes streams (Gray, N = 267) and Atlantic drainages in the northern United States (red, N = 653) are overlaid with a stacked histogram recovery = 102.08 ± 67.13  min, range = 18–414  min). After representing the two harvest locales and illustrating the experimental recovery, the subjects were returned to their holding tanks subjects total length (Great Lakes: N = 59, Anadromous: N = 54). Data for the experimental phase. for historical collections were compiled by J. Hume, Michigan State University Mortality, wound healing, and condition: Mortalities for both tagged and control treatment groups were enumerated daily. Wounds were visually evaluated by Surgical implantation of the transmitter: a single individual (TFH) at days 4, 20, 29, 44, and 61 for ELAT transmitters were fabricated at the Pacific North - all animals alive and retaining a transmitter at the time of west National Laboratory by Daniel Deng. This experi - observation. For evaluation, animals were removed from ment used a modified ELAT where the microbattery their tank and individually placed in a small, clear, tank was replaced with a PIT transmitter to allow for indi- where a photo was taken when the animal ceased move- vidual identification of the subjects via a hand scanner. ment. No anesthesia was used. Control animals were not The measured dimensions of the modified tags used in examined assessment criteria were modified from that of this study were as follows (mean ± 1 SD): weight in air, Wagner et al. [72] and Moser et al. [49], where wound clo- 0.0809 ± 0.003 gm; length, 12.07 ± 0.10  mm; and width, sure and wound inflammation were scored separately on a 0.20 ± 0.003  mm. On February 12, 2020, 59 fully trans- scale of 1–4 (Table  1). An additional metric, a composite formed sea lamprey (per [76]) were surgically implanted wound score, was produced from the wound closure and with modified ELAT transmitters (30 Great Lakes and wound inflammation scores. This was formulated by plot - 29 Atlantic drainage), and 54 entered the experiment as ting the wound closure and wound inflammation scores on control animals (34 Great Lakes and 20 Atlantic drain- an X–Y plane (axes range from 0 to 4) and measuring the age). Animals in the tagged group measured (mean ± 1 Euclidean distance from the origin to the observed scores SD) 150.16 ± 5.69 (total length, mm) and weighed (Eq.  1). To ease interpretation, that distance was then 4.37 ± 0.64  g. Animals in the control group measured rescaled to a range of 0–10, based on the minimum (1.41, (mean ± 1 SD) 148.30 ± 6.08 (total length, mm) and i.e., wound closure and inflammation scores of 1) and max - weighed 4.18 ± 0.50 g. imum (5.657, i.e., wound closure and inflammation scores The implantation surgery followed protocols established of 4) possible distances from the origin: by Moser et  al. [49] and Christiansen [7]. An anesthetic Euclidean Distance − 2 bath of AQUI-S-20E (10% eugenol) and lake water was √ √ . (1) prepared to sedate the animals undergoing the tagging 32 − 2 /10 procedure. Anesthesia concentrations from prior stud- −1 ies (0.02–0.06 ml  l , USFWS 2013, Simard 2017) proved ineffective at inducing stage-IV anesthesia in pre-surgery Swim performance screening [66]. Similar occurrences have been noted for Twenty days after implantation and after the second other anesthetic agents applied to juvenile lamprey when wound healing assessment, we measured burst swim Haas  et al. Animal Biotelemetry (2023) 11:9 Page 5 of 15 Table 1 Criteria for assessing wound closure and wound inflammation. Modified from Moser et al. [49] and Wagner [72] Score Wound closure Wound inflammation 1 Severed tissue is rejoined and completely healed No inflammation or discoloring internal or external to the wound 2 Tissue is apposed but remains severed Slight gray or pink tissue internal or external to the wound is present. Organs completely internal 3 Portions of the wound are apposed. This may Some tissue internal and external to incision is inflamed or discolored (gray or red). May also include apposition around a protruding tag be characterized by intestines partially protruding through incision site 4 No severed tissue is apposed All tissue internal and external to wound is inflamed or discolored (gray or red). May also be characterized by intestines completely protruding and external from body cavity through incision site velocity in all implanted and control animals remaining of the tube, but rendered the manufacturer’s regression in the study. Animals were placed in a 155 × 13x10cm equation linking power units of the swim-tunnel impel- plastic trough filled with 8  cm of water at ± 1  °C of the ler to water velocity imprecise. COVID-19 restrictions holding tank temperature. A plastic mesh grid marked in prevented empirical water velocity calibration; however, 5 cm intervals was positioned in the bottom of the trough passive particulates were moving through the tunnel −1 to measure distance moved, and all interior surfaces at ~ 15  cm  s (approximately 1 body lengths/s for our were covered with plastic mesh to prevent animals from subjects). Consequently, this assay was used to compare attaching to the trough surface. Each animal was placed differences between groups, not to precisely estimate in the lower end of the trough and allowed a five-minute time-to-exhaustion in tagged and untagged sea lamprey. acclimation period prior to testing. After the acclimation After a 3-min acclimation period with no water flow, period, maximum speed was measured by inducing a animals were induced by water flow to freely swim against fast-start (“startle”) response. This was done by squirting a current. As the test progressed, animals would become approximately 3  ml of water from a 5  ml pipette at the impinged on the mesh barrier at the downstream end of water surface above the animal’s head [12, 50]. Each ani- the tunnel. While the animal maintained position in the mal underwent three burst trials with a 3-min recovery flow, actively swimming against the current, elapsed time period in between trials. A Go-Pro camera (60 frames/ was recorded. If the animal became impinged, but main- sec.) was mounted above the trough to record trials, tained active swimming motions (tail-beating) resist- and video footage was processed and analyzed using ing the current, elapsed time continued to be recorded. Kinovea motion analysis software. Burst speed was In the first instance an animal became impinged with measured as the distance the animal traveled in the initial a continued absence (10  s) of anguilliform movement 30 frames (0.5  s) immediately following the first frame resisting the water current, a Smith-Root backpack elec- showing ripples produced by the pipette ejection. The tro-shocking unit sent a brief 12  V, 1  Hz, and 5% duty maximum observed speed (cm s-1) of the three trials was cycle electrical current into the rear of the swim tunnel used in analyses below, hereafter referred to as an indi- for up to ten seconds. This mild voltage was intended to vidual’s burst speed. irritate rather than stun the animal so swimming could On days 30 through 32 post-surgery, all implanted ani- recommence with full musculature control. Trials con- mals remaining in the study (n = 30) and 32 control ani- tinued for animals induced to resume swimming within mals chosen haphazardly from approximate same source ten seconds of continuous electrical current. We deemed proportions were subjected to an endurance swimming exhaustion occurred (trial completed) when either of two test (time-to-exhaustion) in a swim tunnel. Animals were events occurred: (1) an absence of anguilliform swim- individually placed in a 48.2 L plastic mesh-lined cham- ming for ten seconds after the second impingement, or ber of a 121 L Blazka-type swim respirator, with a Leeson (2) no resumption of active swimming within ten seconds Washguard Adjustable Speed AC Motor and Controller. of electrical current after the initial impingement. If the The impeller was powered to 4.5 Hz. This speed was cho - animal continued to swim for 60 min without exhaustion, sen as a result of preliminary trials where lamprey outside the trial was ended. of the experiment were placed in the swim chamber and subjected to various velocities, with the optimal velocity Data analysis (tag retention and survival) being chosen as swift enough to (A) induce swimming Tanks were monitored daily for shedding of transmit- and (B) prompt the cessation of swimming within several ters and mortalities by visually searching the substrate minutes. The inner-mesh lining of the swim tunnel was for transmitters and immobile animals. No burrowing necessary to prevent subjects from attaching to the side activity was observed during this experiment; therefore, Haas et al. Animal Biotelemetry (2023) 11:9 Page 6 of 15 a visual inspection of the surface ensured that any mor- animals surviving to Day 32, which gave the model an talities or shed tags were seen and that the animals were explicit value to measure the significance and magni - minimally disturbed. Immobile animals were tapped with tude of a tag effect from days 32 to 61. This model was a net to determine if the subject was non-responsive. compared using Akaike Information Criterion (AIC) and Dead animals and shed tags were removed from tanks heteroscedasticity of the Schoenfeld residuals to a null and recorded daily until the end of this study. model of one covariate (Group) to assess the role of the Daily mortality data recorded from a 61-day holding TDC in the model’s fit. We used a counting process form period were used to generate Kaplan–Meier survival data frame to build the TDC into the dataset, constructed curves for control and tagged animals; a log-rank test using methodology similar to that of Zhang et al. [78] and (Mantel-Cox) was used to assess the difference in survival Therneau [70]. An individual animal is represented by among the two groups. The p-value resulting from a Log- one row if mortality was experienced prior to Day 32 and Rank test determines the level of significant difference two rows if mortality was experienced after Day 32 or in survival between tagged and control groups for the the animal survived the experiment in entirety (covariate entirety of the experiment. This potentially creates “blind set to 1 if tagged, 0 if control). Day 32 was chosen as the spots” in the analysis, which would prevent the identifica - break point as it coincided with the first mortality event tion of critical periods when large changes in mortality recorded in the control group. Schoenfeld residuals were occurred between groups (e.g., immediate post-surgi- examined to determine if the assumptions of a propor- cal or post-swim testing mortality). These periods have tional hazard model were met. In both the Kaplan–Meier high informative value for future studies, especially for and Cox-Proportional Hazard analyses, tagged animals field studies seeking to use this technology (e.g., setting that shed their tag were not right-censored at the time of the post-surgical holding period if surgery related mor- the shed event to preserve statistical power through sam- tality is delayed by a few days). We further explored the ple size. Finally, animals experiencing early mortalities data to determine if and when any blind spots occurred. (< 5  days) were compared to animals surviving > 5  days To do this, we repeatedly subset the survival data, creat- through separate logistic regression with the three size ing a new dataset for each day (day ) including data from metrics as predictors. Source (Great Lakes vs. Anadro- day until the end of the experiment. This nullified deaths mous) was the additional covariate. prior to day , thereby establishing day as day 0 in the i i analysis for each dataset (i.e., the first subset equals the Data analysis (wound healing and condition) whole dataset, from day 1 onward, the second contains The two wound healing scores, and the composite score, only day 2 onward, etc.). A Log-Rank test of each dataset were assessed through time via separate non-parametric produced p-values for the period following day that were Friedman tests, with the assessment score as the depend- evaluated by generating Kaplan–Meier survival curves. ent variable and numeric assessment (1–5) as the pre- This progressive p-value provided insight by illustrat - dictor. Post hoc Wilcoxon pairwise rank sum tests using ing the pattern of the significance level in the difference Bonferroni correction explored the significance of rela - between the tagged and control groups survival through tionships between wound scores and numeric assessment time. These p-values were used for qualitative visualiza- [55]. Relationships between each of three size measure- tion only, with statistical significance hinging on the full ments (Total Length in mm, mass in g, and Fulton’s Con- dataset log-rank test. dition Factor; Eq.  2; Ricker [57]) and each wound score Upon reviewing the survival curves of the tagged were explored through simple linear regression [55]: and control groups, it was apparent there was a time- dependent component in the survival curves. Mortalities mass(g) (2) appeared to occur in punctuated events within a group Total Length(mm) ∗ 10 (i.e., were not homogeneous throughout the 61-day holding period). Kaplan–Meier-based survival analyses restricted to only one covariate are unable to capture this Data analysis (swim performance) effect. Therefore, additional analyses were performed A two-way unbalanced ANOVA [22] was performed to using Cox-Proportional Hazard (Cox model) regression determine the relationship between maximum observed (R package “survival” v.2.44–1.1, [69, 70]) with a time- burst speed and treatment group (Control vs. Tagged) dependent covariate (TDC) to determine if tag implan- with source (Great Lakes vs. Anadromous) as a covari- tation was associated with an increased risk of mortality, ate. Separate simple linear regression models determined and to what extent differences changed over time. The the relationship of size and composite wound score to time-dependent covariate was a binomial categoriza- maximum burst speed for the tagged animals. A time- tion that was set to one for tagged and zero for control to-event analysis was used to compare the tagged and Haas  et al. Animal Biotelemetry (2023) 11:9 Page 7 of 15 control group’s time-to-exhaustion probabilities by eval- uating their respective Kaplan–Meier survival curves via log-rank test (R package “survival” v.2.44–1.1, [70], sur- vival = continuing to swim). Plotted through time (log- seconds) on the x-axis, survival probabilities dropped on Survived the y-axis as members of the respective groups reached Died their time of exhaustion. The log-rank test assessed the statistical difference between the cumulative exhaus - tion probabilities of each group. To assess significance, the log-rank test statistic, where the expected value is the product of the risk of event (number of exhaustion events/number unexhausted) and the number of unex- hausted animals at the given time, is compared to the critical value (chi-square) for one degree of freedom [25]. Additionally, an unbalanced two-way ANOVA tested the null hypothesis that there was no significant difference between swim-to-exhaustion time and covariates group 1.41.6 1.82.0 2.22.4 2.6 and source. Tag Burden (% body mass) Results Fig. 2 Frequency histogram of tag burden in a group of 56 sea lamprey fitted with an ELAT transmitter. Animals that died (n = 17) are Four days into the experiment one holding tank contain- indicated in orange. The upper box plot reports the median (vertical ing 14 tagged and 1 control animal from the anadromous line), 25/75th percentiles (box), and 10/90th percentiles (whiskers) tank experienced 24  h without inflowing water or aera - with outliers (filled circles) tion. These animals were used in analyses prior to that point and censored from any analysis after that date [41]. Tag retention and survival The cumulative survival probabilities (mean ± 95% Eleven of the 59 tagged animals (19%) shed their tags CI) were 0.849 ± 0.092 and 0.647 ± 0.124 for the control throughout the experiment. Two shedding events and tagged groups, respectively. The observed difference occurred when handling animals for endurance swim in survival was significant (Mantel-Cox log-rank test, performance tests. The majority (5/9) of the remaining p = 0.011). Examination of the Kaplan–Meier survival shedding events occurred within the first four days post- curves and the progressive p-value (Fig.  3) suggests dis- implantation, and all animals that shed their tags had tinct periods of elevated mortality in both groups. The wounds that were completely open with no apposition principal differences in survival between tagged and con - in the initial wound assessment on Day 4 (wound clo- trol groups appear in the four-day period immediately sure score = 4). The four additional shedding events were post-surgery (whereafter, the progressive p-value loses recorded on days 19, 20, and 29 (two individuals). statistical significance), and Days 18–30, roughly cor - Twenty-five sea lamprey died during the experiment (8 responding to the period following the burst swim tests in the control group, 17 implanted with ELAT transmit- (Day 20, Kaplan–Meier curves, Fig.  3). Prior to date of ters). The tagged group experienced increased mortality the swim-to-exhaustion test (Day 30), no mortalities were at the commencement of the experiment, with five ani - recorded in the control group. Following this test, both mals dying within four days post-surgery (Days 1, 1, 2, groups exhibited similar reductions in survival. The Cox- 4, 4). Tag burden (tag weight/body weight, %) averaged Proportional hazard model suggested tagged animals 1.87 ± 0.036 across the entire tagged group, with mor- were 7.4 times more likely to experience mortality in the talities distributed across the range (Fig. 2), but higher in first 32 days of the experiment vs. control animals (coef - animals with a tag burden above 2% (6/15, 40% mortality ficient = 2.00, Hazard ratio = 7.4, p = 0.008). The time- as a group) vs. those at or below 2% (11/44, 25% mortal- dependent covariate coefficient was −  1.80 (p = 0.065, ity as a group). However, no size metric (TL, Mass, Con- 95% CI -3.7—0.11, se = 0.97) which implies that after dition Factor) nor source was a significant predictor of 32 days, the hazard ratio in the tagged group was reduced 2.00−1.80 early mortality (logistic regression, all p-values > 0.1). No to of 1.22 e . The ΔAIC (1.86) relative to the null mortalities were observed in the control group until Day model supports the assertion that the difference of asso - 31, with a total 8 mortalities accumulating gradually over ciated risk through time between the two groups is not the following 25 days. homogeneous. Moreover, the global Schoenfeld residuals Count Haas et al. Animal Biotelemetry (2023) 11:9 Page 8 of 15 condition factor (p = 0.27, Adjusted R = 0.005, SE = 2.5) but negatively associated with mass (p = 0.02, Adjusted R = 0.08, SE = 0.5). Each additional gram of mass was associated with an improvement of 1.2 composite score units (i.e., a 12% improvement in wound condition). Wound closure scores improved throughout the experi- mental period, with the greatest improvement occur- ring between the first and second observation dates (Days 4 and 20, post-surgery, mean change = 0.47 score units ± 0.24). Animals surviving the full experiment showed a slight decline on average in wound inflam - mation from Days 4 to 61 (0.17 score units ± 0.15), but Fig. 3 Kaplan–Meier survival curves with 95% confidence inflammation scores improved between Days 4 and 20, intervals for control (red) and tagged (blue) groups with the overall significance (Mantel‑ Cox log‑rank test). A (x) symbol denotes a with the same mean as wound healing. A Friedman rank right‑ censorship event in the respective group. The progressive sum test revealed time was a significant predictor for P‑ value (black line, right Y‑axis) portrays the significance level each of the wound scoring metrics (Table  2). Post hoc associated with Log‑Rank tests throughout each day of the pairwise Wilcoxon Rank Sum Tests revealed a significant experimental period. Each point on the line corresponds to the improvement in wound scores performed after Day 20 p‑ value for a Log‑Rank test, adjusting the experimental period to begin on that day. The purple dashed line represents a significance (Table 2). level of 0.05 Swim performance Burst speed differed between control and tagged groups of the time-dependent covariate model (p = 0.63) pre- (ANOVA: p = 0.003, F = 9.51), but was not related to sent less heteroscedasticity than those of the null model origin of the animals (Great Lakes vs Atlantic drain- (p = 0.10). ages; p = 0.33, F = 0.9). Mean maximum burst speed in cm/s (± 1 SE) was 26.22 ± 1.81 for the tagged group and Wound healing and condition 33.83 ± 1.42 for the untagged group (Fig. 5). The greatest No animals received a composite score of 0 indicat- burst speed recorded in each group was 57.02  cm/s for ing a completely healed wound by the end of the study tagged animals and 56.88 cm/s for control animals. period (Fig.  4). One animal had a completely closed In the tagged group, condition and body size were not wound (wound closure = 1) on the final wound assess - related to maximum burst swim speed (linear regression: ment, but mild inflammation was present (wound inflam - condition factor, p = 0.36; total length, p = 0.36; mass, mation = 2). The initial composite wound score (Day 4) p = 0.97). There was a significant negative correlation was unrelated to total length (separate univariate linear between observed maximum burst speed and each of regressions: p = 0.07, Adjusted R = 0.04, SE = 0.06) or the wound scores recorded on Day 4 post-surgery (linear Fig. 4 Wound assessment scores. A Distribution of wound closure scores for animals remaining in the study at the time of assessment. B Distribution of wound inflammation scores for animals remaining in the study at the time of assessment. A & B 1 = Violet, 2 = Yellow, 3 = Blue, 4 = Green C Box plots of composite wound scores for animals remaining in the study at the time of assessment, showing median (black line), and maximum and minimum values (lines) Haas  et al. Animal Biotelemetry (2023) 11:9 Page 9 of 15 Table 2 Cumulative wound scores (closure, inflammation, composite) Friedman Rank Sum comparison through time, with total p‑ values and those of pairwise Wilcoxon Rank Sum Tests between successive assessments Assessment Type Total p p: p: Day 20 vs. 29 p: Day 29 vs. Day 44 p: Day 44 Day 4 vs. Day 20- vs. Day 61 Wound Closure 0.01* 0.049* 1.0 1.0 1.0 Wound Inflammation 0.005* 0.086 0.639 1.0 1.0 Composite Score < 0.001* 0.009* 1.0 1.0 1.0 *Represents statistical significance of p < 0.05 differ between control and tagged groups (ANOVA: regression: wound closure, p = 0.031, adjusted R = 0.12; p = 0.32, F = 1.02) and was not related to origin of the wound inflammation, p = 0.022, adjusted R = 0.12; animals (Great Lakes vs Atlantic drainages; p = 0.17, composite wound score, p = 0.007, adjusted R = 0.18) F = 1.96). Median time-to-exhaustion in min. for tagged (Fig. 5B). However, the composite wound score recorded and control groups were 1.45 (Range = 0.73 – 26.28) and on the day of the burst swim test (Day 20) was not a sig- 2.35 (Range = 0.53–60), respectively (Fig.  6A). Similarly, nificant predictor of maximum burst swim speed (linear no significant difference in the Kaplan–Meier survival regression: p = 0.22, adjusted R = 0.02). curves was detected (log-rank test, p = 0.18; Fig. 6B). Three animals in each of the tagged and control groups could not be induced to swim in the swim tunnel and Discussion were not evaluated for swim-to-exhaustion. Two addi- In telemetry studies of juvenile or small fishes, negative tional animals in each group exhibited lethargy upon impacts of the transmitter on behavior, swim perfor- retrieval from their holding tank and were censored mance, and physiology may result in erroneous conclu- from the analysis. Sample sizes used in analysis were sions regarding movement trends, behavioral tendencies, n = 25 tagged and n = 27 control. One animal from the and survival rates. Accurate estimation of these com- control group completed the full trial without exhaust- ponents for out-migrating juveniles is critical to under- ing, whereas all other animals in both groups exhausted standing the efficacy of conservation measures, such as prior to 60 min. Time-to-exhaustion did not significantly the installation of fish passage devices and the restoration Fig. 5 A Violin plots of recorded maximum burst speeds for control and tagged sea lamprey, overlaid with box plots exhibiting median (red, black bar), 25% and 75% quartiles (boxes) and non‑ outlying maximum and minimum speeds (lines, within 1.5 × interquartile range). The raw data are jittered on the X‑axis to ease interpretation. B Scatterplot and regression of the maximum burst swim speed vs. Day 4 composite wound score. For reference, the mean (± 95% CI) maximum burst speed for the control group is plotted at a value of 0 on the x‑axis (black), but was not included in the regression analysis Haas et al. Animal Biotelemetry (2023) 11:9 Page 10 of 15 Fig. 6 A Violin plots of recorded time‑to ‑ exhaustion for control and tagged sea lamprey, overlaid with box plots exhibiting median (red, black bar), 25% and 25% quartiles (boxes) and maximum and minimum values for non‑ outlying results (lines). Data are jittered on the X‑axis to ease interpretation. B Survival (exhaustion) curves for control (red) and tagged (blue) animals in Swim‑to ‑Exhaustion tests (p = 0.18) of spawning and rearing habitats. The results of this consistent with descriptions of internal hemorrhaging study suggest implantation of an ELAT transmitter into provided by Dawson et  al. [13, 14]. Two of 5 animals newly transformed sea lamprey results in survival and tag experiencing early mortality in this study exhibited retention akin to that reported for similar sized PIT tags. protruding intestines and visual evidence of internal The 61-day survival of our tagged subjects was 71%, well hemorrhaging near the wound site. Second, all tagged within the range reported in previous studies with lar- animals that survived the four days post-surgery also val and juvenile lampreys 25–100%; [14, 29, 49–51, 63]. survived the following two weeks leading up to the first However, survival was significantly lower in the tagged swim test and exhibited clear improvement in wound animals (vs control), with no effect statistically attribut - condition. Third, the time to stage-IV anesthesia was able to measures of animal length, mass, condition, or long relative to other anesthetics used with lampreys, population of origin (Great Lakes vs. Atlantic drainage). and longer than recommendations of all anesthetics There was some evidence that individuals with higher (Summerfelt & Smith 1990). Data reported by Chris- tag burdens were more likely to experience mortality, but tiansen et  al. [7] regarding Pacific lamprey transform - given the small sample sizes, that finding should be inter - ers suggest a 70  mg/L dose of AQUI-S should result preted with caution. in full sedation in six to nine minutes, we observed a The significant time-dependent covariate in the mean time to Stage-IV sedation of 17  min. Strikingly, Cox model and visualization of the progressive p-val- the time to recovery reported by Christiansen et  al. ues suggest the statistical difference between the two (3–8  min) was considerably faster than we observed groups was heavily weighted by mortalities occurring (a mean of 102  min). Because our goal was to investi- in the first four days of the experiment. Three lines of gate the use of the ELAT in field studies, our holding evidence suggest the immediate post-surgical mor- tanks and anesthetic bath were maintained at the typi- talities and tag losses were likely caused by imperfect cal water temperature experienced by an out-migrating surgical technique, the acute stress of the surgery, or transformer in Great Lakes streams (4.5 °C), a tempera- both. First, mortalities and tag losses were distributed ture substantially colder than reported by Christiansen across a range of body size, a pattern consistent with et  al. (12° C). In fishes, colder water temperature can a surgeon/surgery effect rather than the consequences substantially increase the time to uptake and recovery of tag internalization [4, 10]. Prior work noted nicking from various anesthetic agents, leading to increases in the gastrointestinal tract or other internal organs, and/ the rate of post-surgical complications and death [64, or protrusion of the intestine through the incision, was 77]. Our results suggest that use of alternative anes- associated with rapid mortality (< ~ 7  days) in juvenile thetics (e.g., MS-222) should be considered when per- lampreys [13, 49, 63] as observed here. Although we forming surgeries in cold water on juvenile sea lamprey. did not measure it explicitly, we observed visual evi- In addition, our study was required to follow Federal dence of discoloration around the wound site that is Investigational New Animal Drug (INAD) guidelines Haas  et al. Animal Biotelemetry (2023) 11:9 Page 11 of 15 for the use of AQUI-S (i.e., dosage and exposure time) Implantation with an ELAT transmitter negatively contained in INAD #11-741 [71]. At a minimum, anes- affected swim performance. Maximum burst swim thesia management procedures for cold-water use of speed in tagged animals was 7.6  cm/s (22%) less than AQUI-S need to be better developed for use in juve- untagged animals, regardless of source population, sug- nile sea lamprey. Future studies with greater availabil- gesting a substantial reduction in the ability to perform ity of subjects should also include anesthesia-only and high-speed acceleration. Interestingly, the composite anesthesia+surgery sham controls to better disentangle wound score taken four days post-surgery was a signifi - the relative effects of each factor in survival and perfor - cant predictor of burst swim speed measured more than mance tests. two weeks later, whereas the score on the day of the test It is noteworthy that wound healing was slower in our was not. Further, the predicted burst swim speed for a subjects when compared to the two available studies of wound score of zero (completely healed) was 36.9  cm/s, PIT tagging transforming or transformed juvenile lam- similar to the mean burst speed observed in untagged preys despite a similar incision size (3 mm). In the present animals (33.8 ± 1.4  cm/s). Mueller et  al. [50] report a study, one surviving tagged fish exhibited a fully closed 6  cm/s reduction in the burst swim speed of actively wound at the conclusion of the 61-day study period out-migrating Pacific lamprey, although the relative (2.2%), with the majority of improvement in the wounds reduction vs. untagged animals (7%) was substantially occurring between Days 4 and 20. Simard et al. [63], stud- lower than in our study, despite using similarly sized ying metamorphosing anadromous (Fort River, MA) and subjects. The difference is largely attributable to that land-locked (Lake Champlain) sea lamprey, report post- the recorded burst swimming speeds of Pacific lamprey surgical skin closure rates of approximately 15–20% after are much higher which appears consistent across stud- 60 days of healing, though rates varied across populations ies (means of 51–76  cm/s), e.g., [12, 67]. It is important (12  mm PIT tag surgically inserted, ~ 5  °C). Mesa et  al. to note that these studies were also performed at higher [46] report only 2.2% of transformed Pacific lamprey held temperatures (12 and 20  °C, respectively) and that swim at 9–18  °C exhibited signs of poorly healed or infected performance may be strongly affected by temperature in incisions 40  days following implantation of a 9  mm PIT fishes [6, 74, 75]. Conversely, and despite a 38% decrease tag. At Day 20, our results were akin to those reported by in median value, we failed to detect a significant negative Moser et al. [49] for Pacific lamprey ammocoetes tagged effect of the transmitter in the time-to-exhaustion swim with an 8.4 mm PIT tag and held in the field for 15 days test. Why the effect of the tag manifested more strongly at 6– 11  °C (i.e., no healed wounds). Despite frequent during burst vs. steady swimming is of interest, as burst reports of fungal infections in other laboratory studies or “escape” swimming is more associated with success- using juvenile lampreys [46, 50, 61, 63], infections did not ful passage through hydraulic challenges and the avoid- arise in our subjects. The water temperature used here ance of predators during out-migration [21]. When a was predominantly lower than that of the studies men- juvenile sea lamprey accelerates from rest, it generates a tioned, in most cases by > 4 °C (~ 5–18 °C); thus, the use high amplitude body bend (double that of steady swim- of metamorphosed animals held at low water tempera- ming) that propagates over 75% of the body length [20]. ture may have both slowed the rate of wound healing and It is plausible there is an amplitude threshold where the inhibited fungal infection. However, it is likely that use of transmitter becomes impinged on the viscera, restricting this transmitter in out-migrating lamprey within Great the ability to generate thrust, and aggravating any inter- Lakes watersheds will involve animals experiencing simi- nal injury associated with the tag implantation surgery. lar water temperatures. Slow healing may be a significant That threshold is more likely to be breached during high concern in field studies, where more vigorous swim - acceleration swimming, and conceivably may affect the ming and burial behaviors may further slow wound clo- estimation of natural mortality rates in field studies with sure and may also increase the likelihood of tag loss (vs. small, narrow-bodied anguilliform fishes. that observed in tank studies). Moser et  al. [49] report A core assumption in telemetry studies is that tagged slower healing for juvenile Pacific lamprey held in a natu - individuals are characteristic of the natural population ral stream vs. those held in laboratory tanks. Options for in terms of size, sex, movement characteristics, and fate defending against this outcome in field studies include [30]. Our experimental animals were somewhat smaller the addition of a suture to hasten wound closure and bet- than the historic mean size observed in the Great Lakes, ter retain the transmitter, performing surgeries under and did not encompass the full size range of available fish. warmer water in the laboratory (with appropriate accli- Although we did not observe significant statistical effects mation periods), or simply targeting studies to warmer of animal size on the measured outcomes, the surgeon times of year. reported difficulty inserting the transmitter into subjects with smaller body cavities, and there was some evidence Haas et al. Animal Biotelemetry (2023) 11:9 Page 12 of 15 that individuals with tag burdens in excess of two percent with an improved composite wound score, suggesting of body mass suffered greater mortality. Several lam - lesser injury during the surgery. Post-metamorphosis, prey also exhibited light discoloration posterior to the the intestines of a sea lamprey range laterally through- implanted tag soon after surgery, a symptom of blood out the body of the animal, lessoning the available space impediment through the dorsal aorta caused by pressure between the viscera and the body wall [42]. We suggest from the tag [13] that appeared prior to recovery from that body girth at the tag location, or a similar metric (e.g., anesthesia. However, it was not a consistent indicator of ratio of body depth to length), or a measure of condition impending mortality. Two of 5 animals displaying this factor, may prove more suitable metrics to set the mini- symptom no longer exhibited discoloration by the first mum threshold for implantation. These metrics require wound assessment on Day 4 and survived the length of a larger dataset, perhaps integrated across previous and the study, perhaps due to a posterior shift in tag position future studies to solidify a concrete threshold. Our find - as posited by Moser et al. [49]. It was also notable that in ings support a ratio of 3.33:1 (length (mm) to mass (mg)), both swim tests there was substantial variation in perfor- above a minimum length and mass of 150 mm and 45 mg, mance among individuals that was unrelated to measures should ensure high survival. We further recommend a of body size or population of origin. A number of stud- brief holding period (2–4 days) after recovery from anes- ies demonstrate both burst and steady swimming speeds, thesia and prior to release to assess wound condition and and the underlying aerobic scope for activity, are repeata- potential early tag loss. If the wound does not appear to ble traits within individual fish during swim performance have inflammation over a moderate level and/or a com - tests, e.g., [8, 23, 36, 52]. Understanding consistent indi- plete lack of apposed tissue around the incision, it is likely vidual differences in tag effects on swim performance is that the animal will experience limited physical incapaci- likely an important metric to understanding whether and tation compared to an untagged conspecific. Addition - how the effects of the transmitter on swimming will man - ally, although not experienced in our study, prior work ifest in studies designed to measure movement rates and with juvenile lampreys suggest fungal infection is a risk survival in the wild [73]. Further, out-migrating juvenile whenever the fish are held in tanks, especially at warmer lampreys exhibit strong nocturnal patterning in down- temperatures. A prophylactic anti-fungal regime may be stream movements, burrowing into sediment or seek- needed in those conditions. ing shelter during daylight hours [12, 47, 54]. In a study with smaller (means of < 120  mm) larval sea lamprey Conclusions implanted with 8 or 9 mm PIT tags, the tag significantly The ELAT transmitter has now proven feasible in labo - increased both the time (2.3 × longer) and effort (defined ratory and field settings across a range of anguilliform as number of “stops” while burrowing, 1 additional stop species with relevant behavioral unknowns, such as on average) necessary for the animal to successfully bur- the regionally endangered American brook lamprey row (vs. untagged fish; [13]). (Lethenteron appendix) of the United States Eastern It is routine for tag effect studies to recommend mini - Seaboard and the critically endangered European eel mum size limits for use of animals in telemetry work, (Anguilla Anguilla) (Department, N.H. Fish and Game based on the desire to satisfy the criteria of minimal tag [18], The IUCN Red List of Threatened Species [68]) [16, effect on the animal’s performance. However, this prac - 17, 39]. Our findings demonstrate its utility for juvenile tice conflicts with the need to use representative animals, sea lamprey. The ability to gain insight into the fate of as demographic measures, such as mortality, are highly migrants as a function of the features of the rivers that size dependent in juvenile fishes [2 , 65]. In other words, regulate mortality (e.g., predator density, habitat type, preferential use of larger subjects that are less likely to etc.) is likely to lead to the development of new control suffer tag effects (i.e., non-probability sampling) may methods to target sea lamprey in their last phase before bias estimates of vital rates made using those animals in the initiation of parasitism [33]. In addition, it allows for field studies. Conceivably, this may be compensated in the investigation of the effects of habitat degradation the modeling of mortality rates from telemetry studies by and barriers to downstream migration (dams and weirs, using size-dependent estimates of tag-induced mortal- water intake structures), and overharvesting; the princi- ity. Similar studies to ours in larval and juvenile Pacific pal threats to several migratory lampreys in their native and sea lamprey offer minimum size recommendations range [28, 35, 40, 44, 48]. Ultimately, the ELAT trans- of 120–150  mm total length, based on the relationship mitter has the potential to open the door to a greater between mortality and length observed in the lab [46, understanding of the out-migration parasitic lampreys, a 50, 61, 63]. While there was no significant correlation of critical and poorly understood stanza in the lives of these any size measurement and mortality in our tagged ani- consequential and enigmatic creatures. mals, larger mass, but not total length, was associated Haas  et al. Animal Biotelemetry (2023) 11:9 Page 13 of 15 Abbreviations Received: 14 April 2022 Accepted: 31 January 2023 ELAT E el–lamprey acoustic transmitter PIT Passive Integrated Transponder JSATS Juv enile Salmon Acoustic Telemetry System PRI Pulse Rate Interval USFWS United States Fish & Wildlife Service References INAD Investigational New Animal Drug 1. Baer J, Hartmann F, Brinker A. Abiotic triggers for sea and river lamprey TDC Time‑Dependent Covariate spawning migration and juvenile outmigration in the River Rhine Ger‑ AIC Akaike Information Criterion many. Ecol Freshwater Fish. 2018;27(4):988–98. 2. Bailey KM, Houde ED. Predation on Eggs and Larvae of Marine Fishes Acknowledgements and the Recruitment Problem. 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Survival, healing, and swim performance of juvenile migratory sea lamprey (Petromyzon marinus) implanted with a new acoustic microtransmitter designed for small eel-like fishes

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Springer Journals
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Copyright © The Author(s) 2023
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10.1186/s40317-023-00318-1
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Abstract

Background Little is known about the transformer stage of the parasitic lampreys, a brief but critical period that encompasses juvenile out‑migration from rivers to lakes or oceans to begin parasitic feeding. Information about this life stage could have significant conservation implications for both imperiled and invasive lampreys. We investigated tag retention, survival, wound healing, and swim performance of newly transformed sea lamprey (Petromyzon mari- nus) implanted with a new micro‑acoustic transmitter, the eel–lamprey acoustic transmitter (ELAT ), in a controlled laboratory environment. Results The 61‑ day survival of our tagged subjects was 71%, within the range reported in similar studies of juve‑ nile lampreys. However, survival was significantly lower in the tagged animals (vs control), with no effect statistically attributable to measures of animal length, mass, condition, or population of origin (Great Lakes vs. Atlantic drainage). Mortality in tagged fish was concentrated in the first four days post ‑surgery, suggesting injury from the surgical pro ‑ cess. An unusually long recovery time from anesthesia may have contributed to the increased mortality. In a simple burst swim assay, tagged animals swam significantly slower (− 22.5%) than untagged animals, but were not signifi‑ cantly different in endurance swim tests. A composite wound healing score at day four was a significant predictor of maximum burst swim speed at day 20, and wound condition was related to animal mass, but not length, at the time of tagging. Conclusions Impairments to survival and swim performance of juvenile sea lamprey implanted with the ELAT trans‑ mitter were within currently reported ranges for telemetry studies with small, difficult to observe fishes. Our results could be improved with more refined anesthesia and surgical techniques. The ability to track migratory movements of imperiled and pest populations of parasitic lampreys will improve our ability to estimate vital rates that underlie recruitment to the adult population (growth, survival) and to investigate the environmental factors that regulate the timing and rates of movement, in wild populations. *Correspondence: Taylor F. Haas Haastayl@msu.edu Full list of author information is available at the end of the article © The Author(s) 2023. Open Access 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. Haas et al. Animal Biotelemetry (2023) 11:9 Page 2 of 15 Keywords Lamprey, JSATS, ELATS, Acoustic Telemetry, Survival, Burst Swim, Endurance Swim, Wound Healing, Surgery Background sea lampreys would allow treatment decisions to be Migration is a time of heightened threat and uncertainty made based on probable parasite production vs. larval regarding the risk of predation and the localization of abundance, incorporating system-specific differences critical resources [60]. This is particularly so when migra - in rates of survival through migration and first feed - tion occurs early in life, when variation in daily growth ing. For example, in Lake Michigan, the lower reaches and survival may be substantial and influence recruit - of rivers systems often contain drowned river mouth ment to the adult population [24, 37]. A number of eco- lake–wetland complexes that are rich in piscivorous nomically and ecologically valued fishes exhibit juvenile predators [38], and piscivores are important predators feeding migrations from rivers into lakes or oceans, of out-migrating juvenile lampreys [48, 58, 62]. Life including salmon (Oncorhynchus spp.) and lake sturgeon stage-specific spatial population models for sea lam - (Acipenser fulvescens). Threats to the viability of these prey currently assume all out-migrating sea lamprey populations, and to control invasive species with simi- have an equal likelihood of survival until arrival in the lar life histories, have prompted considerable interest in lakes, regardless of differences in migratory distance, ascertaining the behavior, timing, and survival of juvenile river size, habitat types, or predator populations, each fishes as they move downstream [35, 56]. of which contribute to differences in mortality and Several lamprey species are among the most poorly growth among watersheds [31, 59]. understood fishes that exhibit juvenile migration, includ - Survival estimation during migration requires track- ing species that range from imperiled and ecologically ing an animal’s status over considerable distance and/ or commercially valued (e.g., Pacific lamprey Entos - or time. The most frequently used tool to monitor the phenus tridentatus, European river lamprey, Lampetra movements of fishes and other aquatic organisms over uv fl iatilis, sea lamprey Petromyzon marinus in select large distances is telemetry, involving the implantation European regions) to pestilential and targeted for reduc- or attachment of a transmitter that may be detected tion (e.g., invasive sea lamprey in the Laurentian Great when the fish moves into the range of a receiver [32]. Lakes). These lampreys spawn in rivers, after which Until recently, small (≤ 12 mm) passive integrated tran- newly hatched larvae (ammocoetes) bury in stream sedi- sponder (PIT) tags were the only transmitters avail- ments for typically four to seven years feeding on organic able for the study of out-migrating lamprey. PIT tags detritus and algae [14]. At the end of the larval stage, lack an internal power source, requiring tagged fishes they transform and migrate downstream into estuaries to move within 1–2  m of the antenna to be detected or large lakes to commence parasitic feeding on fishes [3, 53]. The proportion of PIT-tagged larval and out- [1, 14, 21]. This period of physiological and geographi - migrating lamprey detected by PIT antennas is rela- cal transition (aka the transformer stage) [9] is of short tively low, with reported detection rates ranging from duration, yet is considered critical to the development 5 to 14% [13, 47]. Internally powered telemetry tags of effective conservation and management practices (acoustic and radio transmitters) offer an alternative [21]. For example, out-migrating lamprey within their that substantially increases the detection range (tens native ranges typically must transit through a gauntlet of to hundreds of meters) and detection probability (as dams and their affiliated water intake structures, result - high as 80–100% on a well-designed array covering ing in physical injury, increased predation, and direct the entirety of the stream channel) at a single receiver or delayed mortality [27, 48]. Providing for safe passage [45]. Acoustic transmitters have several desirable prop- through these structures is necessary for the protection erties for use in small fishes, in particular, they do not of the species [26]. require an external trailing antenna (as radio telemetry In the Laurentian Great Lakes, where a single sea typically does), that may result in negative impacts to lamprey may consume upwards of 21 kg of fish biomass, swim performance, lower likelihood of predator attack, control is achieved through the application of selective and higher survival in tagged individuals (reviewed by pesticides (lampricides) to kill larvae in streams prior Crossin et al. [11] and references therein). to transformation [5, 43]. Rivers are selected for lampri- A primary assumption of telemetry analysis is the cide treatment based on estimates of larval abundance, fish’s movement behavior (e.g., swim speed, timing) is informed by population models and expert opinion not substantially altered by bearing the tag, or because [34]. The ability to estimate the fate of out-migrating of the implantation process. Historically, acoustic Haas  et al. Animal Biotelemetry (2023) 11:9 Page 3 of 15 transmitters have proven too large to implant into small inflammation, and a composite score that combined the fishes with narrow body cavities. Transmitters with two measures into an overall measure of wound condi- sufficient battery life to support demographic stud - tion. Swim performance was analyzed by comparing ies of fishes require large batteries that would impede two performance metrics, maximum burst swim speed movement and survival in small fishes (Liedtke 2019). (20 days post-surgery) and time-to-exhaustion swimming This situation is compounded in anguilliform swim - (29–31  days post-surgery), to untagged control fish. We ming fishes, where tags may physically impede propa - focused on the animal’s burst swim ability, as it is a facul- gation of the propulsive wave or compress organs tative behavior suggestive of ability to escape a perceived along the length of the very narrow body. The fabri - threat, and swim-to-exhaustion, as it is characteristic of cation of a novel microbattery and transmitter suit- long stretches of active swimming during a migration able for use in juvenile sea lamprey—the Eel–Lamprey [19]. The swim measures were separated by ten days to Acoustic Tag or ELAT—offers a potential solution to ensure the stress of the burst swim test did not influence this problem [15, 39]. This tag is compatible with the the results of the time-to-exhaustion test. All measures JSATS (Juvenile Salmon Acoustic Telemetry System) were statistically compared to a group of 54 control ani- receiver, with a detection range of 80–140 m, a distance mals that did not experience the anesthesia, surgery, or 100 × greater than the approximate range of a 12  mm tag implantation. Due to the difficulty in acquiring this PIT tag [17]. The transmitter has a source level of a life history stage in sea lamprey, subjects were collected 147 dB and is in a cylindrical encasing with dimensions from both Great Lakes and Atlantic basin drainages. 12 mm × 2 mm, 0.08 g dry-mass and transmits at a fre- Where appropriate, source was included as a covariate in quency of 416.7  kHz (± 0.5%). Currently, the standard the statistical models. PRI (Pulse Rate Interval) of five seconds allots approxi - mately 30  days of use [16]. Pilot field studies using the Collection and housing of subjects ELAT tag have demonstrated the high detection rates Sea lamprey used in this study were collected from trib- (> 95%) in juveniles of both Pacific lamprey and Ameri - utaries in the Great Lakes Basin (N = 64), and a hydro- can eel (Anguilla rostrata) [17, 39]. At approximately power diversion canal on the Connecticut River that the same size as the PIT tags used in previous stud- flows into the Atlantic Ocean (N = 49). ies of juvenile lampreys (12  mm x 2  mm, 0.08  g), this We selected 113 sea lamprey ranging 140 mm–160 mm is the first acoustic telemetry tag that does not persis - total length (TL) based on recommendations from pre- tently violate the two percent of body mass standard vious studies using similarly sized PIT tags in juvenile for use without impediment of movement in juvenile sea lamprey [63] and Pacific lamprey [46]. We chose to anguilliform fishes due to its cylindrical shape [46, 53, include animals across a range of sizes near the median of 63]. Here, we report an assessment of tag retention, the size distributions in the Great Lakes and the Atlantic survival, wound healing, and impacts to swim perfor- basin (Fig.  1) to examine the relationship of body size to mance of the ELAT transmitter surgically implanted wound healing and swim performance. into newly transformed sea lampreys. Our goal was to Subjects were housed at the U.S. Geological Survey perform a comprehensive evaluation of the impacts of Hammond Bay Biological Station from February 11, 2020 ELAT transmitter implantation to support the estab- to April 13, 2020. Lampreys were separated by source and lishment of criteria for use in field studies designed to kept in eight separate 23L 40 cm x 22 cm x 26 cm tanks enumerate critical demographic parameters (e.g., stage- that were supplied with constant flow-through water specific mortality rates) and the movement ecology of from Lake Huron and continuous aeration. As our find - the poorly understood transformer stage. ings are intended to inform use of the ELAT tag in natu- ral rivers, the holding tanks were constructed to include Methods: certain natural features the animal would experience dur- Study design ing out-migration. First, previous tagging effects studies The objective of this study was to examine the effects observed fungal growth and infection on experimental of the ELAT tag on sea lamprey survival, condition, subjects held in the laboratory [7, 49, 50]. To ensure the and swim performance. To achieve this, we surgically microbiome the sea lamprey were exposed to was akin implanted ELAT tags into 59 newly transformed juve- to the natural flora, we lined the tanks with a 4 cm layer nile parasitic sea lamprey and examined tag retention, of mixed substrate (cobble, sand, fine-grained sediment) survival, wound healing, and swim performance dur- collected from nearby Schmidt’s Creek. In addition, ing a 61-day study period, corresponding to anticipated unfiltered inflowing water from Lake Huron was heated tag life at a PRI of 10  s. Wound healing assessment to a temperature typical of central Lake Michigan tribu- involved two scoring metrics, wound closure and wound taries during the fall migration (~ 4.5° C). Haas et al. Animal Biotelemetry (2023) 11:9 Page 4 of 15 using doses recommended for teleost fishes. Stage-IV anesthesia was induced in (mean ± 1 SD) 17.0 ± 4.5  min −1 via immersion in a solution of 0.7  ml  l AQUI-S-20E (eugenol concentration = 70  ppm). When each animal reached stage-IV anesthesia, it was placed on a damp sur- gery board and the surgeon (T.F. Haas) made a lateral 3  mm incision into the body cavity adjacent to the 13th myomere using a Premier Edge Restricted Depth 3  mm microscalpel (OASIS Medical). A disinfected (immer- sion in 70% ethanol for ≥ 2  min) then rinsed transmitter was inserted posteriorly into the opening until it was com- pletely enveloped in the animal’s body cavity (mean ± 1 SD = 1.4 ± 0.93  min, range = 0–4  min); no suturing or other method of artificially closing was used [13, 14, 49]. After the transmitter was fully inserted, each animal was placed into an oxygenated recovery tank until active swim- Fig. 1 Density plots of total length (mm) for historic collections of ming or suction attachment to the side of the tank was out‑migrating juvenile sea lamprey for animals captured from Great observed, indicating initial recovery (mean ± 1 SD time to Lakes streams (Gray, N = 267) and Atlantic drainages in the northern United States (red, N = 653) are overlaid with a stacked histogram recovery = 102.08 ± 67.13  min, range = 18–414  min). After representing the two harvest locales and illustrating the experimental recovery, the subjects were returned to their holding tanks subjects total length (Great Lakes: N = 59, Anadromous: N = 54). Data for the experimental phase. for historical collections were compiled by J. Hume, Michigan State University Mortality, wound healing, and condition: Mortalities for both tagged and control treatment groups were enumerated daily. Wounds were visually evaluated by Surgical implantation of the transmitter: a single individual (TFH) at days 4, 20, 29, 44, and 61 for ELAT transmitters were fabricated at the Pacific North - all animals alive and retaining a transmitter at the time of west National Laboratory by Daniel Deng. This experi - observation. For evaluation, animals were removed from ment used a modified ELAT where the microbattery their tank and individually placed in a small, clear, tank was replaced with a PIT transmitter to allow for indi- where a photo was taken when the animal ceased move- vidual identification of the subjects via a hand scanner. ment. No anesthesia was used. Control animals were not The measured dimensions of the modified tags used in examined assessment criteria were modified from that of this study were as follows (mean ± 1 SD): weight in air, Wagner et al. [72] and Moser et al. [49], where wound clo- 0.0809 ± 0.003 gm; length, 12.07 ± 0.10  mm; and width, sure and wound inflammation were scored separately on a 0.20 ± 0.003  mm. On February 12, 2020, 59 fully trans- scale of 1–4 (Table  1). An additional metric, a composite formed sea lamprey (per [76]) were surgically implanted wound score, was produced from the wound closure and with modified ELAT transmitters (30 Great Lakes and wound inflammation scores. This was formulated by plot - 29 Atlantic drainage), and 54 entered the experiment as ting the wound closure and wound inflammation scores on control animals (34 Great Lakes and 20 Atlantic drain- an X–Y plane (axes range from 0 to 4) and measuring the age). Animals in the tagged group measured (mean ± 1 Euclidean distance from the origin to the observed scores SD) 150.16 ± 5.69 (total length, mm) and weighed (Eq.  1). To ease interpretation, that distance was then 4.37 ± 0.64  g. Animals in the control group measured rescaled to a range of 0–10, based on the minimum (1.41, (mean ± 1 SD) 148.30 ± 6.08 (total length, mm) and i.e., wound closure and inflammation scores of 1) and max - weighed 4.18 ± 0.50 g. imum (5.657, i.e., wound closure and inflammation scores The implantation surgery followed protocols established of 4) possible distances from the origin: by Moser et  al. [49] and Christiansen [7]. An anesthetic Euclidean Distance − 2 bath of AQUI-S-20E (10% eugenol) and lake water was √ √ . (1) prepared to sedate the animals undergoing the tagging 32 − 2 /10 procedure. Anesthesia concentrations from prior stud- −1 ies (0.02–0.06 ml  l , USFWS 2013, Simard 2017) proved ineffective at inducing stage-IV anesthesia in pre-surgery Swim performance screening [66]. Similar occurrences have been noted for Twenty days after implantation and after the second other anesthetic agents applied to juvenile lamprey when wound healing assessment, we measured burst swim Haas  et al. Animal Biotelemetry (2023) 11:9 Page 5 of 15 Table 1 Criteria for assessing wound closure and wound inflammation. Modified from Moser et al. [49] and Wagner [72] Score Wound closure Wound inflammation 1 Severed tissue is rejoined and completely healed No inflammation or discoloring internal or external to the wound 2 Tissue is apposed but remains severed Slight gray or pink tissue internal or external to the wound is present. Organs completely internal 3 Portions of the wound are apposed. This may Some tissue internal and external to incision is inflamed or discolored (gray or red). May also include apposition around a protruding tag be characterized by intestines partially protruding through incision site 4 No severed tissue is apposed All tissue internal and external to wound is inflamed or discolored (gray or red). May also be characterized by intestines completely protruding and external from body cavity through incision site velocity in all implanted and control animals remaining of the tube, but rendered the manufacturer’s regression in the study. Animals were placed in a 155 × 13x10cm equation linking power units of the swim-tunnel impel- plastic trough filled with 8  cm of water at ± 1  °C of the ler to water velocity imprecise. COVID-19 restrictions holding tank temperature. A plastic mesh grid marked in prevented empirical water velocity calibration; however, 5 cm intervals was positioned in the bottom of the trough passive particulates were moving through the tunnel −1 to measure distance moved, and all interior surfaces at ~ 15  cm  s (approximately 1 body lengths/s for our were covered with plastic mesh to prevent animals from subjects). Consequently, this assay was used to compare attaching to the trough surface. Each animal was placed differences between groups, not to precisely estimate in the lower end of the trough and allowed a five-minute time-to-exhaustion in tagged and untagged sea lamprey. acclimation period prior to testing. After the acclimation After a 3-min acclimation period with no water flow, period, maximum speed was measured by inducing a animals were induced by water flow to freely swim against fast-start (“startle”) response. This was done by squirting a current. As the test progressed, animals would become approximately 3  ml of water from a 5  ml pipette at the impinged on the mesh barrier at the downstream end of water surface above the animal’s head [12, 50]. Each ani- the tunnel. While the animal maintained position in the mal underwent three burst trials with a 3-min recovery flow, actively swimming against the current, elapsed time period in between trials. A Go-Pro camera (60 frames/ was recorded. If the animal became impinged, but main- sec.) was mounted above the trough to record trials, tained active swimming motions (tail-beating) resist- and video footage was processed and analyzed using ing the current, elapsed time continued to be recorded. Kinovea motion analysis software. Burst speed was In the first instance an animal became impinged with measured as the distance the animal traveled in the initial a continued absence (10  s) of anguilliform movement 30 frames (0.5  s) immediately following the first frame resisting the water current, a Smith-Root backpack elec- showing ripples produced by the pipette ejection. The tro-shocking unit sent a brief 12  V, 1  Hz, and 5% duty maximum observed speed (cm s-1) of the three trials was cycle electrical current into the rear of the swim tunnel used in analyses below, hereafter referred to as an indi- for up to ten seconds. This mild voltage was intended to vidual’s burst speed. irritate rather than stun the animal so swimming could On days 30 through 32 post-surgery, all implanted ani- recommence with full musculature control. Trials con- mals remaining in the study (n = 30) and 32 control ani- tinued for animals induced to resume swimming within mals chosen haphazardly from approximate same source ten seconds of continuous electrical current. We deemed proportions were subjected to an endurance swimming exhaustion occurred (trial completed) when either of two test (time-to-exhaustion) in a swim tunnel. Animals were events occurred: (1) an absence of anguilliform swim- individually placed in a 48.2 L plastic mesh-lined cham- ming for ten seconds after the second impingement, or ber of a 121 L Blazka-type swim respirator, with a Leeson (2) no resumption of active swimming within ten seconds Washguard Adjustable Speed AC Motor and Controller. of electrical current after the initial impingement. If the The impeller was powered to 4.5 Hz. This speed was cho - animal continued to swim for 60 min without exhaustion, sen as a result of preliminary trials where lamprey outside the trial was ended. of the experiment were placed in the swim chamber and subjected to various velocities, with the optimal velocity Data analysis (tag retention and survival) being chosen as swift enough to (A) induce swimming Tanks were monitored daily for shedding of transmit- and (B) prompt the cessation of swimming within several ters and mortalities by visually searching the substrate minutes. The inner-mesh lining of the swim tunnel was for transmitters and immobile animals. No burrowing necessary to prevent subjects from attaching to the side activity was observed during this experiment; therefore, Haas et al. Animal Biotelemetry (2023) 11:9 Page 6 of 15 a visual inspection of the surface ensured that any mor- animals surviving to Day 32, which gave the model an talities or shed tags were seen and that the animals were explicit value to measure the significance and magni - minimally disturbed. Immobile animals were tapped with tude of a tag effect from days 32 to 61. This model was a net to determine if the subject was non-responsive. compared using Akaike Information Criterion (AIC) and Dead animals and shed tags were removed from tanks heteroscedasticity of the Schoenfeld residuals to a null and recorded daily until the end of this study. model of one covariate (Group) to assess the role of the Daily mortality data recorded from a 61-day holding TDC in the model’s fit. We used a counting process form period were used to generate Kaplan–Meier survival data frame to build the TDC into the dataset, constructed curves for control and tagged animals; a log-rank test using methodology similar to that of Zhang et al. [78] and (Mantel-Cox) was used to assess the difference in survival Therneau [70]. An individual animal is represented by among the two groups. The p-value resulting from a Log- one row if mortality was experienced prior to Day 32 and Rank test determines the level of significant difference two rows if mortality was experienced after Day 32 or in survival between tagged and control groups for the the animal survived the experiment in entirety (covariate entirety of the experiment. This potentially creates “blind set to 1 if tagged, 0 if control). Day 32 was chosen as the spots” in the analysis, which would prevent the identifica - break point as it coincided with the first mortality event tion of critical periods when large changes in mortality recorded in the control group. Schoenfeld residuals were occurred between groups (e.g., immediate post-surgi- examined to determine if the assumptions of a propor- cal or post-swim testing mortality). These periods have tional hazard model were met. In both the Kaplan–Meier high informative value for future studies, especially for and Cox-Proportional Hazard analyses, tagged animals field studies seeking to use this technology (e.g., setting that shed their tag were not right-censored at the time of the post-surgical holding period if surgery related mor- the shed event to preserve statistical power through sam- tality is delayed by a few days). We further explored the ple size. Finally, animals experiencing early mortalities data to determine if and when any blind spots occurred. (< 5  days) were compared to animals surviving > 5  days To do this, we repeatedly subset the survival data, creat- through separate logistic regression with the three size ing a new dataset for each day (day ) including data from metrics as predictors. Source (Great Lakes vs. Anadro- day until the end of the experiment. This nullified deaths mous) was the additional covariate. prior to day , thereby establishing day as day 0 in the i i analysis for each dataset (i.e., the first subset equals the Data analysis (wound healing and condition) whole dataset, from day 1 onward, the second contains The two wound healing scores, and the composite score, only day 2 onward, etc.). A Log-Rank test of each dataset were assessed through time via separate non-parametric produced p-values for the period following day that were Friedman tests, with the assessment score as the depend- evaluated by generating Kaplan–Meier survival curves. ent variable and numeric assessment (1–5) as the pre- This progressive p-value provided insight by illustrat - dictor. Post hoc Wilcoxon pairwise rank sum tests using ing the pattern of the significance level in the difference Bonferroni correction explored the significance of rela - between the tagged and control groups survival through tionships between wound scores and numeric assessment time. These p-values were used for qualitative visualiza- [55]. Relationships between each of three size measure- tion only, with statistical significance hinging on the full ments (Total Length in mm, mass in g, and Fulton’s Con- dataset log-rank test. dition Factor; Eq.  2; Ricker [57]) and each wound score Upon reviewing the survival curves of the tagged were explored through simple linear regression [55]: and control groups, it was apparent there was a time- dependent component in the survival curves. Mortalities mass(g) (2) appeared to occur in punctuated events within a group Total Length(mm) ∗ 10 (i.e., were not homogeneous throughout the 61-day holding period). Kaplan–Meier-based survival analyses restricted to only one covariate are unable to capture this Data analysis (swim performance) effect. Therefore, additional analyses were performed A two-way unbalanced ANOVA [22] was performed to using Cox-Proportional Hazard (Cox model) regression determine the relationship between maximum observed (R package “survival” v.2.44–1.1, [69, 70]) with a time- burst speed and treatment group (Control vs. Tagged) dependent covariate (TDC) to determine if tag implan- with source (Great Lakes vs. Anadromous) as a covari- tation was associated with an increased risk of mortality, ate. Separate simple linear regression models determined and to what extent differences changed over time. The the relationship of size and composite wound score to time-dependent covariate was a binomial categoriza- maximum burst speed for the tagged animals. A time- tion that was set to one for tagged and zero for control to-event analysis was used to compare the tagged and Haas  et al. Animal Biotelemetry (2023) 11:9 Page 7 of 15 control group’s time-to-exhaustion probabilities by eval- uating their respective Kaplan–Meier survival curves via log-rank test (R package “survival” v.2.44–1.1, [70], sur- vival = continuing to swim). Plotted through time (log- seconds) on the x-axis, survival probabilities dropped on Survived the y-axis as members of the respective groups reached Died their time of exhaustion. The log-rank test assessed the statistical difference between the cumulative exhaus - tion probabilities of each group. To assess significance, the log-rank test statistic, where the expected value is the product of the risk of event (number of exhaustion events/number unexhausted) and the number of unex- hausted animals at the given time, is compared to the critical value (chi-square) for one degree of freedom [25]. Additionally, an unbalanced two-way ANOVA tested the null hypothesis that there was no significant difference between swim-to-exhaustion time and covariates group 1.41.6 1.82.0 2.22.4 2.6 and source. Tag Burden (% body mass) Results Fig. 2 Frequency histogram of tag burden in a group of 56 sea lamprey fitted with an ELAT transmitter. Animals that died (n = 17) are Four days into the experiment one holding tank contain- indicated in orange. The upper box plot reports the median (vertical ing 14 tagged and 1 control animal from the anadromous line), 25/75th percentiles (box), and 10/90th percentiles (whiskers) tank experienced 24  h without inflowing water or aera - with outliers (filled circles) tion. These animals were used in analyses prior to that point and censored from any analysis after that date [41]. Tag retention and survival The cumulative survival probabilities (mean ± 95% Eleven of the 59 tagged animals (19%) shed their tags CI) were 0.849 ± 0.092 and 0.647 ± 0.124 for the control throughout the experiment. Two shedding events and tagged groups, respectively. The observed difference occurred when handling animals for endurance swim in survival was significant (Mantel-Cox log-rank test, performance tests. The majority (5/9) of the remaining p = 0.011). Examination of the Kaplan–Meier survival shedding events occurred within the first four days post- curves and the progressive p-value (Fig.  3) suggests dis- implantation, and all animals that shed their tags had tinct periods of elevated mortality in both groups. The wounds that were completely open with no apposition principal differences in survival between tagged and con - in the initial wound assessment on Day 4 (wound clo- trol groups appear in the four-day period immediately sure score = 4). The four additional shedding events were post-surgery (whereafter, the progressive p-value loses recorded on days 19, 20, and 29 (two individuals). statistical significance), and Days 18–30, roughly cor - Twenty-five sea lamprey died during the experiment (8 responding to the period following the burst swim tests in the control group, 17 implanted with ELAT transmit- (Day 20, Kaplan–Meier curves, Fig.  3). Prior to date of ters). The tagged group experienced increased mortality the swim-to-exhaustion test (Day 30), no mortalities were at the commencement of the experiment, with five ani - recorded in the control group. Following this test, both mals dying within four days post-surgery (Days 1, 1, 2, groups exhibited similar reductions in survival. The Cox- 4, 4). Tag burden (tag weight/body weight, %) averaged Proportional hazard model suggested tagged animals 1.87 ± 0.036 across the entire tagged group, with mor- were 7.4 times more likely to experience mortality in the talities distributed across the range (Fig. 2), but higher in first 32 days of the experiment vs. control animals (coef - animals with a tag burden above 2% (6/15, 40% mortality ficient = 2.00, Hazard ratio = 7.4, p = 0.008). The time- as a group) vs. those at or below 2% (11/44, 25% mortal- dependent covariate coefficient was −  1.80 (p = 0.065, ity as a group). However, no size metric (TL, Mass, Con- 95% CI -3.7—0.11, se = 0.97) which implies that after dition Factor) nor source was a significant predictor of 32 days, the hazard ratio in the tagged group was reduced 2.00−1.80 early mortality (logistic regression, all p-values > 0.1). No to of 1.22 e . The ΔAIC (1.86) relative to the null mortalities were observed in the control group until Day model supports the assertion that the difference of asso - 31, with a total 8 mortalities accumulating gradually over ciated risk through time between the two groups is not the following 25 days. homogeneous. Moreover, the global Schoenfeld residuals Count Haas et al. Animal Biotelemetry (2023) 11:9 Page 8 of 15 condition factor (p = 0.27, Adjusted R = 0.005, SE = 2.5) but negatively associated with mass (p = 0.02, Adjusted R = 0.08, SE = 0.5). Each additional gram of mass was associated with an improvement of 1.2 composite score units (i.e., a 12% improvement in wound condition). Wound closure scores improved throughout the experi- mental period, with the greatest improvement occur- ring between the first and second observation dates (Days 4 and 20, post-surgery, mean change = 0.47 score units ± 0.24). Animals surviving the full experiment showed a slight decline on average in wound inflam - mation from Days 4 to 61 (0.17 score units ± 0.15), but Fig. 3 Kaplan–Meier survival curves with 95% confidence inflammation scores improved between Days 4 and 20, intervals for control (red) and tagged (blue) groups with the overall significance (Mantel‑ Cox log‑rank test). A (x) symbol denotes a with the same mean as wound healing. A Friedman rank right‑ censorship event in the respective group. The progressive sum test revealed time was a significant predictor for P‑ value (black line, right Y‑axis) portrays the significance level each of the wound scoring metrics (Table  2). Post hoc associated with Log‑Rank tests throughout each day of the pairwise Wilcoxon Rank Sum Tests revealed a significant experimental period. Each point on the line corresponds to the improvement in wound scores performed after Day 20 p‑ value for a Log‑Rank test, adjusting the experimental period to begin on that day. The purple dashed line represents a significance (Table 2). level of 0.05 Swim performance Burst speed differed between control and tagged groups of the time-dependent covariate model (p = 0.63) pre- (ANOVA: p = 0.003, F = 9.51), but was not related to sent less heteroscedasticity than those of the null model origin of the animals (Great Lakes vs Atlantic drain- (p = 0.10). ages; p = 0.33, F = 0.9). Mean maximum burst speed in cm/s (± 1 SE) was 26.22 ± 1.81 for the tagged group and Wound healing and condition 33.83 ± 1.42 for the untagged group (Fig. 5). The greatest No animals received a composite score of 0 indicat- burst speed recorded in each group was 57.02  cm/s for ing a completely healed wound by the end of the study tagged animals and 56.88 cm/s for control animals. period (Fig.  4). One animal had a completely closed In the tagged group, condition and body size were not wound (wound closure = 1) on the final wound assess - related to maximum burst swim speed (linear regression: ment, but mild inflammation was present (wound inflam - condition factor, p = 0.36; total length, p = 0.36; mass, mation = 2). The initial composite wound score (Day 4) p = 0.97). There was a significant negative correlation was unrelated to total length (separate univariate linear between observed maximum burst speed and each of regressions: p = 0.07, Adjusted R = 0.04, SE = 0.06) or the wound scores recorded on Day 4 post-surgery (linear Fig. 4 Wound assessment scores. A Distribution of wound closure scores for animals remaining in the study at the time of assessment. B Distribution of wound inflammation scores for animals remaining in the study at the time of assessment. A & B 1 = Violet, 2 = Yellow, 3 = Blue, 4 = Green C Box plots of composite wound scores for animals remaining in the study at the time of assessment, showing median (black line), and maximum and minimum values (lines) Haas  et al. Animal Biotelemetry (2023) 11:9 Page 9 of 15 Table 2 Cumulative wound scores (closure, inflammation, composite) Friedman Rank Sum comparison through time, with total p‑ values and those of pairwise Wilcoxon Rank Sum Tests between successive assessments Assessment Type Total p p: p: Day 20 vs. 29 p: Day 29 vs. Day 44 p: Day 44 Day 4 vs. Day 20- vs. Day 61 Wound Closure 0.01* 0.049* 1.0 1.0 1.0 Wound Inflammation 0.005* 0.086 0.639 1.0 1.0 Composite Score < 0.001* 0.009* 1.0 1.0 1.0 *Represents statistical significance of p < 0.05 differ between control and tagged groups (ANOVA: regression: wound closure, p = 0.031, adjusted R = 0.12; p = 0.32, F = 1.02) and was not related to origin of the wound inflammation, p = 0.022, adjusted R = 0.12; animals (Great Lakes vs Atlantic drainages; p = 0.17, composite wound score, p = 0.007, adjusted R = 0.18) F = 1.96). Median time-to-exhaustion in min. for tagged (Fig. 5B). However, the composite wound score recorded and control groups were 1.45 (Range = 0.73 – 26.28) and on the day of the burst swim test (Day 20) was not a sig- 2.35 (Range = 0.53–60), respectively (Fig.  6A). Similarly, nificant predictor of maximum burst swim speed (linear no significant difference in the Kaplan–Meier survival regression: p = 0.22, adjusted R = 0.02). curves was detected (log-rank test, p = 0.18; Fig. 6B). Three animals in each of the tagged and control groups could not be induced to swim in the swim tunnel and Discussion were not evaluated for swim-to-exhaustion. Two addi- In telemetry studies of juvenile or small fishes, negative tional animals in each group exhibited lethargy upon impacts of the transmitter on behavior, swim perfor- retrieval from their holding tank and were censored mance, and physiology may result in erroneous conclu- from the analysis. Sample sizes used in analysis were sions regarding movement trends, behavioral tendencies, n = 25 tagged and n = 27 control. One animal from the and survival rates. Accurate estimation of these com- control group completed the full trial without exhaust- ponents for out-migrating juveniles is critical to under- ing, whereas all other animals in both groups exhausted standing the efficacy of conservation measures, such as prior to 60 min. Time-to-exhaustion did not significantly the installation of fish passage devices and the restoration Fig. 5 A Violin plots of recorded maximum burst speeds for control and tagged sea lamprey, overlaid with box plots exhibiting median (red, black bar), 25% and 75% quartiles (boxes) and non‑ outlying maximum and minimum speeds (lines, within 1.5 × interquartile range). The raw data are jittered on the X‑axis to ease interpretation. B Scatterplot and regression of the maximum burst swim speed vs. Day 4 composite wound score. For reference, the mean (± 95% CI) maximum burst speed for the control group is plotted at a value of 0 on the x‑axis (black), but was not included in the regression analysis Haas et al. Animal Biotelemetry (2023) 11:9 Page 10 of 15 Fig. 6 A Violin plots of recorded time‑to ‑ exhaustion for control and tagged sea lamprey, overlaid with box plots exhibiting median (red, black bar), 25% and 25% quartiles (boxes) and maximum and minimum values for non‑ outlying results (lines). Data are jittered on the X‑axis to ease interpretation. B Survival (exhaustion) curves for control (red) and tagged (blue) animals in Swim‑to ‑Exhaustion tests (p = 0.18) of spawning and rearing habitats. The results of this consistent with descriptions of internal hemorrhaging study suggest implantation of an ELAT transmitter into provided by Dawson et  al. [13, 14]. Two of 5 animals newly transformed sea lamprey results in survival and tag experiencing early mortality in this study exhibited retention akin to that reported for similar sized PIT tags. protruding intestines and visual evidence of internal The 61-day survival of our tagged subjects was 71%, well hemorrhaging near the wound site. Second, all tagged within the range reported in previous studies with lar- animals that survived the four days post-surgery also val and juvenile lampreys 25–100%; [14, 29, 49–51, 63]. survived the following two weeks leading up to the first However, survival was significantly lower in the tagged swim test and exhibited clear improvement in wound animals (vs control), with no effect statistically attribut - condition. Third, the time to stage-IV anesthesia was able to measures of animal length, mass, condition, or long relative to other anesthetics used with lampreys, population of origin (Great Lakes vs. Atlantic drainage). and longer than recommendations of all anesthetics There was some evidence that individuals with higher (Summerfelt & Smith 1990). Data reported by Chris- tag burdens were more likely to experience mortality, but tiansen et  al. [7] regarding Pacific lamprey transform - given the small sample sizes, that finding should be inter - ers suggest a 70  mg/L dose of AQUI-S should result preted with caution. in full sedation in six to nine minutes, we observed a The significant time-dependent covariate in the mean time to Stage-IV sedation of 17  min. Strikingly, Cox model and visualization of the progressive p-val- the time to recovery reported by Christiansen et  al. ues suggest the statistical difference between the two (3–8  min) was considerably faster than we observed groups was heavily weighted by mortalities occurring (a mean of 102  min). Because our goal was to investi- in the first four days of the experiment. Three lines of gate the use of the ELAT in field studies, our holding evidence suggest the immediate post-surgical mor- tanks and anesthetic bath were maintained at the typi- talities and tag losses were likely caused by imperfect cal water temperature experienced by an out-migrating surgical technique, the acute stress of the surgery, or transformer in Great Lakes streams (4.5 °C), a tempera- both. First, mortalities and tag losses were distributed ture substantially colder than reported by Christiansen across a range of body size, a pattern consistent with et  al. (12° C). In fishes, colder water temperature can a surgeon/surgery effect rather than the consequences substantially increase the time to uptake and recovery of tag internalization [4, 10]. Prior work noted nicking from various anesthetic agents, leading to increases in the gastrointestinal tract or other internal organs, and/ the rate of post-surgical complications and death [64, or protrusion of the intestine through the incision, was 77]. Our results suggest that use of alternative anes- associated with rapid mortality (< ~ 7  days) in juvenile thetics (e.g., MS-222) should be considered when per- lampreys [13, 49, 63] as observed here. Although we forming surgeries in cold water on juvenile sea lamprey. did not measure it explicitly, we observed visual evi- In addition, our study was required to follow Federal dence of discoloration around the wound site that is Investigational New Animal Drug (INAD) guidelines Haas  et al. Animal Biotelemetry (2023) 11:9 Page 11 of 15 for the use of AQUI-S (i.e., dosage and exposure time) Implantation with an ELAT transmitter negatively contained in INAD #11-741 [71]. At a minimum, anes- affected swim performance. Maximum burst swim thesia management procedures for cold-water use of speed in tagged animals was 7.6  cm/s (22%) less than AQUI-S need to be better developed for use in juve- untagged animals, regardless of source population, sug- nile sea lamprey. Future studies with greater availabil- gesting a substantial reduction in the ability to perform ity of subjects should also include anesthesia-only and high-speed acceleration. Interestingly, the composite anesthesia+surgery sham controls to better disentangle wound score taken four days post-surgery was a signifi - the relative effects of each factor in survival and perfor - cant predictor of burst swim speed measured more than mance tests. two weeks later, whereas the score on the day of the test It is noteworthy that wound healing was slower in our was not. Further, the predicted burst swim speed for a subjects when compared to the two available studies of wound score of zero (completely healed) was 36.9  cm/s, PIT tagging transforming or transformed juvenile lam- similar to the mean burst speed observed in untagged preys despite a similar incision size (3 mm). In the present animals (33.8 ± 1.4  cm/s). Mueller et  al. [50] report a study, one surviving tagged fish exhibited a fully closed 6  cm/s reduction in the burst swim speed of actively wound at the conclusion of the 61-day study period out-migrating Pacific lamprey, although the relative (2.2%), with the majority of improvement in the wounds reduction vs. untagged animals (7%) was substantially occurring between Days 4 and 20. Simard et al. [63], stud- lower than in our study, despite using similarly sized ying metamorphosing anadromous (Fort River, MA) and subjects. The difference is largely attributable to that land-locked (Lake Champlain) sea lamprey, report post- the recorded burst swimming speeds of Pacific lamprey surgical skin closure rates of approximately 15–20% after are much higher which appears consistent across stud- 60 days of healing, though rates varied across populations ies (means of 51–76  cm/s), e.g., [12, 67]. It is important (12  mm PIT tag surgically inserted, ~ 5  °C). Mesa et  al. to note that these studies were also performed at higher [46] report only 2.2% of transformed Pacific lamprey held temperatures (12 and 20  °C, respectively) and that swim at 9–18  °C exhibited signs of poorly healed or infected performance may be strongly affected by temperature in incisions 40  days following implantation of a 9  mm PIT fishes [6, 74, 75]. Conversely, and despite a 38% decrease tag. At Day 20, our results were akin to those reported by in median value, we failed to detect a significant negative Moser et al. [49] for Pacific lamprey ammocoetes tagged effect of the transmitter in the time-to-exhaustion swim with an 8.4 mm PIT tag and held in the field for 15 days test. Why the effect of the tag manifested more strongly at 6– 11  °C (i.e., no healed wounds). Despite frequent during burst vs. steady swimming is of interest, as burst reports of fungal infections in other laboratory studies or “escape” swimming is more associated with success- using juvenile lampreys [46, 50, 61, 63], infections did not ful passage through hydraulic challenges and the avoid- arise in our subjects. The water temperature used here ance of predators during out-migration [21]. When a was predominantly lower than that of the studies men- juvenile sea lamprey accelerates from rest, it generates a tioned, in most cases by > 4 °C (~ 5–18 °C); thus, the use high amplitude body bend (double that of steady swim- of metamorphosed animals held at low water tempera- ming) that propagates over 75% of the body length [20]. ture may have both slowed the rate of wound healing and It is plausible there is an amplitude threshold where the inhibited fungal infection. However, it is likely that use of transmitter becomes impinged on the viscera, restricting this transmitter in out-migrating lamprey within Great the ability to generate thrust, and aggravating any inter- Lakes watersheds will involve animals experiencing simi- nal injury associated with the tag implantation surgery. lar water temperatures. Slow healing may be a significant That threshold is more likely to be breached during high concern in field studies, where more vigorous swim - acceleration swimming, and conceivably may affect the ming and burial behaviors may further slow wound clo- estimation of natural mortality rates in field studies with sure and may also increase the likelihood of tag loss (vs. small, narrow-bodied anguilliform fishes. that observed in tank studies). Moser et  al. [49] report A core assumption in telemetry studies is that tagged slower healing for juvenile Pacific lamprey held in a natu - individuals are characteristic of the natural population ral stream vs. those held in laboratory tanks. Options for in terms of size, sex, movement characteristics, and fate defending against this outcome in field studies include [30]. Our experimental animals were somewhat smaller the addition of a suture to hasten wound closure and bet- than the historic mean size observed in the Great Lakes, ter retain the transmitter, performing surgeries under and did not encompass the full size range of available fish. warmer water in the laboratory (with appropriate accli- Although we did not observe significant statistical effects mation periods), or simply targeting studies to warmer of animal size on the measured outcomes, the surgeon times of year. reported difficulty inserting the transmitter into subjects with smaller body cavities, and there was some evidence Haas et al. Animal Biotelemetry (2023) 11:9 Page 12 of 15 that individuals with tag burdens in excess of two percent with an improved composite wound score, suggesting of body mass suffered greater mortality. Several lam - lesser injury during the surgery. Post-metamorphosis, prey also exhibited light discoloration posterior to the the intestines of a sea lamprey range laterally through- implanted tag soon after surgery, a symptom of blood out the body of the animal, lessoning the available space impediment through the dorsal aorta caused by pressure between the viscera and the body wall [42]. We suggest from the tag [13] that appeared prior to recovery from that body girth at the tag location, or a similar metric (e.g., anesthesia. However, it was not a consistent indicator of ratio of body depth to length), or a measure of condition impending mortality. Two of 5 animals displaying this factor, may prove more suitable metrics to set the mini- symptom no longer exhibited discoloration by the first mum threshold for implantation. These metrics require wound assessment on Day 4 and survived the length of a larger dataset, perhaps integrated across previous and the study, perhaps due to a posterior shift in tag position future studies to solidify a concrete threshold. Our find - as posited by Moser et al. [49]. It was also notable that in ings support a ratio of 3.33:1 (length (mm) to mass (mg)), both swim tests there was substantial variation in perfor- above a minimum length and mass of 150 mm and 45 mg, mance among individuals that was unrelated to measures should ensure high survival. We further recommend a of body size or population of origin. A number of stud- brief holding period (2–4 days) after recovery from anes- ies demonstrate both burst and steady swimming speeds, thesia and prior to release to assess wound condition and and the underlying aerobic scope for activity, are repeata- potential early tag loss. If the wound does not appear to ble traits within individual fish during swim performance have inflammation over a moderate level and/or a com - tests, e.g., [8, 23, 36, 52]. Understanding consistent indi- plete lack of apposed tissue around the incision, it is likely vidual differences in tag effects on swim performance is that the animal will experience limited physical incapaci- likely an important metric to understanding whether and tation compared to an untagged conspecific. Addition - how the effects of the transmitter on swimming will man - ally, although not experienced in our study, prior work ifest in studies designed to measure movement rates and with juvenile lampreys suggest fungal infection is a risk survival in the wild [73]. Further, out-migrating juvenile whenever the fish are held in tanks, especially at warmer lampreys exhibit strong nocturnal patterning in down- temperatures. A prophylactic anti-fungal regime may be stream movements, burrowing into sediment or seek- needed in those conditions. ing shelter during daylight hours [12, 47, 54]. In a study with smaller (means of < 120  mm) larval sea lamprey Conclusions implanted with 8 or 9 mm PIT tags, the tag significantly The ELAT transmitter has now proven feasible in labo - increased both the time (2.3 × longer) and effort (defined ratory and field settings across a range of anguilliform as number of “stops” while burrowing, 1 additional stop species with relevant behavioral unknowns, such as on average) necessary for the animal to successfully bur- the regionally endangered American brook lamprey row (vs. untagged fish; [13]). (Lethenteron appendix) of the United States Eastern It is routine for tag effect studies to recommend mini - Seaboard and the critically endangered European eel mum size limits for use of animals in telemetry work, (Anguilla Anguilla) (Department, N.H. Fish and Game based on the desire to satisfy the criteria of minimal tag [18], The IUCN Red List of Threatened Species [68]) [16, effect on the animal’s performance. However, this prac - 17, 39]. Our findings demonstrate its utility for juvenile tice conflicts with the need to use representative animals, sea lamprey. The ability to gain insight into the fate of as demographic measures, such as mortality, are highly migrants as a function of the features of the rivers that size dependent in juvenile fishes [2 , 65]. In other words, regulate mortality (e.g., predator density, habitat type, preferential use of larger subjects that are less likely to etc.) is likely to lead to the development of new control suffer tag effects (i.e., non-probability sampling) may methods to target sea lamprey in their last phase before bias estimates of vital rates made using those animals in the initiation of parasitism [33]. In addition, it allows for field studies. Conceivably, this may be compensated in the investigation of the effects of habitat degradation the modeling of mortality rates from telemetry studies by and barriers to downstream migration (dams and weirs, using size-dependent estimates of tag-induced mortal- water intake structures), and overharvesting; the princi- ity. Similar studies to ours in larval and juvenile Pacific pal threats to several migratory lampreys in their native and sea lamprey offer minimum size recommendations range [28, 35, 40, 44, 48]. Ultimately, the ELAT trans- of 120–150  mm total length, based on the relationship mitter has the potential to open the door to a greater between mortality and length observed in the lab [46, understanding of the out-migration parasitic lampreys, a 50, 61, 63]. While there was no significant correlation of critical and poorly understood stanza in the lives of these any size measurement and mortality in our tagged ani- consequential and enigmatic creatures. mals, larger mass, but not total length, was associated Haas  et al. Animal Biotelemetry (2023) 11:9 Page 13 of 15 Abbreviations Received: 14 April 2022 Accepted: 31 January 2023 ELAT E el–lamprey acoustic transmitter PIT Passive Integrated Transponder JSATS Juv enile Salmon Acoustic Telemetry System PRI Pulse Rate Interval USFWS United States Fish & Wildlife Service References INAD Investigational New Animal Drug 1. Baer J, Hartmann F, Brinker A. Abiotic triggers for sea and river lamprey TDC Time‑Dependent Covariate spawning migration and juvenile outmigration in the River Rhine Ger‑ AIC Akaike Information Criterion many. Ecol Freshwater Fish. 2018;27(4):988–98. 2. Bailey KM, Houde ED. Predation on Eggs and Larvae of Marine Fishes Acknowledgements and the Recruitment Problem. 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Journal

Animal BiotelemetrySpringer Journals

Published: Mar 11, 2023

Keywords: Lamprey; JSATS; ELATS; Acoustic Telemetry; Survival; Burst Swim; Endurance Swim; Wound Healing; Surgery

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