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Best practice recommendations for the use of fully implanted telemetry devices in pinnipeds

Best practice recommendations for the use of fully implanted telemetry devices in pinnipeds Electronic telemetry devices have enabled many novel and important data collection and experimental opportunities for difficult to observe species. Externally attached devices have limited retention and may affect thermoregulation, energetics, social and reproductive behavior, visibility, predation risk and entanglement. Internally placed, surgically implanted devices can mitigate some of these effects and may open additional experimental opportunities. How‑ ever, improper implementation can significantly affect animals and data. From a review of recent studies using fully implanted tags and studying their effects, we present 15 specific best practice recommendations for the use of such tags in pinnipeds. Recommendations address issues including device size, coating and sterilization, implantation surgery and effect assessment, within the framework of the Three R’s: Reduction, Refinement , Replacement. While devel‑ oped for pinnipeds, these recommendations could apply to other aquatic mammals and vertebrates and to partially implanted or even external tags. Keywords: Biotelemetry, Implant, Subcutaneous, Intraperitoneal, Marine mammal, Surgery, Reduction, Refinement, Replacement the risk of entanglement, visibility and predation [5, 7– Background 11]. Surgically implanted internal devices may reduce Electronic telemetry devices have been used effectively to some of these effects, allow longer-duration deployments track location and movement and to monitor foraging and the use of additional sensors, but may also result in and reproductive behavior as well as the physiological substantial and potentially catastrophic effects if improp - and reproductive state of terrestrial, avian and marine erly implemented. Recent discussions [8, 12] and working vertebrates for more than five decades [ 1, 2]. This has group reports on ‘refinements in telemetry procedures’ been particularly useful for difficult to observe taxa such have highlighted that ‘Telemetry is often presented as a as marine vertebrates [3–6]. Most commonly, such refinement, in that it can reduce or eliminate stress devices are externally attached, resulting in limited moni- caused to animals (e.g., by restraint), but it is vital to toring durations for animals that molt or shed on a regu- remember that telemetry, like all other procedures on lar basis. Furthermore, external devices can affect social, animals, also needs to be refined’ [ 13]. reproductive and movement behavior, or the energetics of locomotion and thermoregulation, and may increase *Correspondence: markush@alaskasealife.org Defined here as any active electronic monitoring or transmitting device Alaska SeaLife Center, 301 Railway Avenue, Seward, AK 99664‑1329, USA that once fully implanted into any part of the body does not break the integ- Full list of author information is available at the end of the article ument. © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Horning et al. Anim Biotelemetry (2017) 5:13 Page 2 of 15 the conduct and publication of studies of short-term Existing recommendations by societies and recent and long-term effects of tags [26]. A recent report by workgroups the Joint Working Group on Refinement [13] does not In the USA federal funding agencies have adopted the provide specific recommendations, but does point out policy instituted by the Public Health Service on the that ‘smaller is better,’ and that adding mass can have a humane care and use of laboratory animals, under the significant physiological impact and can alter body mass Animal Welfare Act. This policy requires research to be set points. The report also references multiple studies compliant with the Guide for the Care and Use of Labora- that have shown that animals carrying devices can incur tory Animals [14]. The Guide provides important ethical measurable and significant energetic costs of transporta - guidance on principles of humane animal research with a tion, of a magnitude ranging from about half of the mass focus on biomedical laboratory settings, but few specific percentage (i.e., a tag adding 5% to the mass of a mam- procedural recommendations are applicable to research mal may result in an added energetic burden of 2.5%) to involving wildlife [15]. Recognizing these shortcomings, as high as double the mass percentage in flying birds (see the US National Science Foundation requested profes- also [27–29]). sional societies to develop taxon-specific guidelines suit - able for wild species and field work [15]. Most applicable Implanted telemetry devices in birds professional societies, the Guide and the Joint Working Barron et  al. [30] evaluated 84 published studies using Group on Refinement [13] point out the need to consider external or internal devices on birds for reported pres- and assess the impact of external and internal telem- ence or absence of specific effects. While most effects etry devices on research subjects. However, few consist- were small in magnitude (e.g., device-induced preen- ent guidelines exist across or within taxa with respect ing), the most consistently reported effect of devices in to shape, relative size, mass and volume of devices, with this meta-analysis was increased energy expenditure and respect to surgical procedures or the parameters that reduced nesting likelihood. Attachment methods requir- should be applied in considering the impact of devices ing anesthesia (i.e., anchored and implanted devices) [8]. had the highest reported incidence of mortality, while The American Fisheries Society provides no recom- external devices were the only type resulting in reported mendations for implanted telemetry devices in fishes, ‘device-induced behaviors.’ Furthermore, device effects of any kind [16]. Much of the recent work (since the late were more pronounced in relation to uncaptured controls 1990s) assessing the effects of implanted devices on wild than ‘procedural controls’ (those handled and temporar- animals has been conducted on anadromous fish, due ily captive in the same manner as tagged individuals) to management concerns and regulatory status of some suggesting some of the observed effects were due to han - species [17–21]. Authors have repeatedly challenged the dling and captivity. However, in a subsequent meta-anal- anecdotal, yet never formalized ‘2% rule’ for fish based on ysis of 55 studies on 49 species of birds, White et al. [31] the demonstrated absence of negative effects on swim - specifically compared effects between external and fully ming energetics, growth and survival for relative sizes implanted devices. This meta-analysis revealed consist - of tags up to 6.7% of body mass [17, 19, 22]. The Ameri- ently negative effects of externally attached devices, while can Society of Ichthyologists and Herpetologists suggests no consistent effects were reported for implants. The an upper size limit of 10% of body mass on an anecdo- authors concluded that internal devices are preferable to tal basis for implanted devices in amphibians and rep- external devices provided that risks associated with anes- tiles, but points out that sizes between 1 and 6% are often thesia and surgery can be mitigated. In diving or aquatic achievable [23]. The Ornithological Council quotes stud - birds, Culik and Wilson [28] found energetic and behav- ies suggesting that external or internal telemetry trans- ioral effects of both external (n  =  5 animals) and inter- mitters in birds should not exceed 5% of a subject’s body nal tags (n  =  2 animals) on Adelie penguins (Pygoscelis mass, but also points out that this value or a less com- adeliae). However, sample sizes were extremely small monly applied 3% threshold are completely arbitrary and and the implanted devices were connected to inter- that multiple conflicting studies found both presence and nal electrocardiography electrode wires and were fur- absence of effects of tags in the 1–3% mass range on sur - ther secured to the musculature via sutures. Such wires vival [24]. Guidelines by the American Society of Mam- and fixing sutures may increase the likelihood of device malogists [25] only vaguely recommend external devices effects. Beaulieu et al. [32] compared the effects of exter - not exceed 5–10% of individual body mass but do not nal (n  =  10 animals) and internal (n  =  6 animals) tags (separately) consider implanted devices. Finally, the Soci- on the foraging behavior of Adelie penguins. They noted ety for Marine Mammalogy provides no specific recom - altered foraging behavior in animals carrying internal mendation for external or internal tags, but encourages Horning et al. Anim Biotelemetry (2017) 5:13 Page 3 of 15 tags, but none in animals carrying external tags. How- whether the two remaining sea otters were misclassi- ever, the implants were secured with sutures, and only a fied as pregnant, had stillbirths, aborted prematurely single foraging trip per animal was observed, which for or whether the pups died after birth. Bodkin et  al. [40] implanted birds occurred less than 6  days after surgery. intraperitoneally implanted two telemetry devices into Interestingly, the meta-analysis conducted by White et al. each of 21 sea otters: one VHF transmitter and one [31] showed that most device effects reported tended time–depth recorder. The animals were subsequently toward zero with increasing sample sizes, suggesting that recaptured, and the archival data loggers were surgi- some reported effects may be outliers, or that methods cally removed. Tags were recovered from 14 animals improve with experience of investigators. The absence of that were recaptured after two months. One animal was a proportional mass effect (i.e., bigger tags are associated found dead after four years. No reasons for mortality with a greater effect magnitude) has been used to illus - were reported. One pregnant female that was implanted trate the arbitrary nature of mass-percent device size was subsequently recaptured with a pup. Subsequent thresholds [13, 29, 30]. studies reported on data derived from intraperitoneal tags implanted into sea otters, but possible effects were Fully implanted telemetry devices in aquatic not investigated or reported [47, 48]. mammals Within aquatic mammals, fully implanted telemetry Fully implanted telemetry devices in pinnipeds S I devices (subcutaneous, intraperitoneal ) have been Lander et  al. [41] tested four different kinds of subcu - tested or used in sea otters (Enhydra lutris), Eurasian taneous implants in 10 harbor seals with varied results. I I otters (Lutra lutra), North American river ot ters (Lon- Animals with resin-encased transmitters developed I I tra canadensis), nutria (Myocastor coypus), beavers fluid pockets and mucopurulent discharge, whereas (Castor canadensis), muskrat (Ondatra zibethicus), polar wax-coated devices elicited no such response. CBC and S S,I bears (Ursus maritimus), harbor s eals (Phoca vitulina), serum biochemistry values were within normal ranges Northern elephant seals (Mirounga angustirostris), Cali- within one week of surgery for nine of the 10 animals. S,I fornia sea lions (Zalophus californianus) and Steller sea The authors concluded that wax-coated implants were lions (Eumetopias jubatus) [33–53]. preferable for long-term subcutaneous deployments. As previously summarized [43], several studies that Green et al. [44] conducted trial implantations of subcu- used free-floating intra-abdominal implants reported taneous heart rate data loggers with electrocardiography on the effects of implants on reproduction in aquatic wires into three Northern elephant seals and three Cali- mammals. Reid et  al. [33] specifically studied reproduc - fornia sea lions. All animals recovered uneventfully from tive effects of intraperitoneal implants in North Ameri - the surgery, but the elephant seals then developed a ‘sub- can river otters over one to two reproductive cycles. In stantial inflammatory response’ and the devices had to be seven adult females, they observed 12 possible pregnan- removed. Blundell and collaborators [50] subcutaneously cies that resulted in eight litters. They concluded that the implanted wax-coated VHF transmitters (also used in the implants did not interfere with reproduction. Hernan- Lander study) in 277 harbor seals in Alaska. The trans - dez-Divers et  al. [38] also concluded that implants did mitters were programmed to send an altered signal when not affect survival or reproductive potential in North tag temperature dropped below 27 °C, indicating possible American river otters. Bohrman et  al. [45] reported on mortality or tag extrusion. Animals were released within successful reproduction in one single North American hours of surgery, and no consistent postoperative moni- river otter with an intraperitoneal implant. Fernandez- toring besides automated VHF tracking was reported. Moran et al. [39] reached the same conclusion in a study No altered signals were detected during the study that of Eurasian otters. Nolfo and Hammond [42] implanted could be attributed to an actual mortality. Four isolated VHF transmitters intraperitoneally into 20 adult nutria, tags were recovered, and one animal was recaptured after nine males and 11 females. All females were pregnant. one year with a partially extruded tag. Manugian et  al. One female aborted her near-full-term litter within one [51, 52] reported on the use of wax-coated subcutane- day of surgery and prior to release, likely as a result of ous VHF implants in nine harbor seals closely monitored anesthesia. The authors found no evidence of morbidity up to three weeks before release, and another 32 released or infection. They concluded that the implants did not immediately after implantation. No complications were interfere with reproduction. Monnett and Rotterman reported from this study, though the authors do refer to [37] intraperitoneally implanted devices into 19 adult one instance from a prior study (it is unclear which study female sea otters that were deemed pregnant at time of they refer to) where a subcutaneously implanted wax- implantation based on abdominal palpation. Seventeen coated tag was observed migrating out of a juvenile har- of the 19 pupped successfully. They could not determine bor seal about nine months after implantation. Horning et al. Anim Biotelemetry (2017) 5:13 Page 4 of 15 Life‑long implanted vital rate transmitters In 2004, Horning—in collaboration with Wildlife Com- puters, Inc. (Redmond, WA)—completed the develop- ment of a new implantable telemetry device, the life history transmitter (LHX tag) [54]. LHX tags were spe- cifically designed for vital rate telemetry in California and Steller sea lions. The cylindrical tags with hemispheri - cal ends (42  mm diameter, 128  mm length, 202  ml vol- ume, 118 g mass, 0.87 N buoyancy) are intraperitoneally implanted [43] and record data throughout the life of the host. Summary data are only transmitted via the Argos satellite system postmortem, after the positively buoy- ant tags are liberated from decomposing, dismembered or digested carcasses. In 2014, development of the sec- ond-generation LHX2 tag was completed (with Wildlife Fig. 1 A second‑ generation LHX2 implantable Argos‑ compatible sat‑ Computers, Inc.). LHX2 tags are smaller (Fig.  1, 33  mm ellite transmitter ( Wildlife Computers Inc., Redmond, WA) is shown on the right. Exterior dimensions are 97 mm length by 33 mm diameter. diameter, 97 mm length, 79 ml volume, 54 g mass, 0.26 N The tag mass is 54 g; buoyancy is 0.26 N. The device is coated in Epo‑ buoyancy) and can be programmed to evaluate tempera- Tek 302‑3M resin, a material certified under the USP Class 6 standard ture patterns for parturition events. LHX tags can be for biological reactivity. The QR code links to information on the tag, used to determine date, location and causes of mortality project and rewards for return. A VHF radio transmitter (ATS Inc., Isanti, [49, 55], and also age at primiparity and lifetime number MN) is shown in the middle. Exterior dimensions are 90 mm length by 59 mm width by 30 mm thickness. The transmitter mass is 150 g; of pups born if deployed in pre-parous females. buoyancy is −0.27 N. The device is cast in an unspecified electrical Horning, Mellish and collaborators implanted single or resin and coated with an unspecified USP Class 6‑ certified material (© dual intraperitoneal LHX tags in 49 otariids from 2004 to Markus Horning) 2014 (4 California sea lions and 45 Steller sea lions [43, 46, 49, 54, 55]). For the first two deployments in each species, single tags were used. Subsequently, two tags per animal were used to increase and estimate data return healed upon external, visual examination and palpation, probability. For initial deployments animals were held in and the initial postoperative elevation of blood analytes extended captivity up to eight weeks after surgery prior associated with the inflammatory response had returned to release to allow comprehensive assessments of postop- to pre-surgical levels after five weeks [43, 57, 59]. From erative effects including physiological changes [56–59], these observations, the authors derived a 45-day postop- stress response [60], as well as behavioral indicators of erative survival study inclusion criterion. All 49 otariids pain [61, 62]. Following release, all animals were tracked had survival confirmed beyond the 45-day postoperative via externally attached satellite telemetry transmitters for study inclusion criterion, whether released after one, two periods ranging from one week to four months [57, 63]. or up to eight weeks following surgery [49, 57]. These Following surgery, the study animals exhibited changes in studies also demonstrated that transmitter implantation 2 3 behaviors that are indicative of discomfort or pain [43]. has no detectable effect on postrelease movement and The proportion of time spent standing and in a back arch diving behavior as compared to animals that also under- increased, and the proportion of time spent lying on the went temporary captivity but without LHX tag implants ventral side where the incision was located decreased. [57]. Captivity may have a small but detectable, short- Peak changes occurred for days 1–3 after surgery, and term (2 weeks) effect on postrelease diving behavior in changes diminished but remained above pre-surgical lev- comparison to wild animals that did not undergo tempo- els at days 10–12. The proportion of time spent in loco - rary captivity [63]. Long-term survival beyond the attach- motion decreased for days 1–3, but was at pre-surgery ment of external transmitters was compared between levels for days 10–12 [61]. Surgical wounds appeared implanted animals and non-implanted controls that did not undergo captivity, based on a mark-resight study design using hot-iron branding. No differences in sur - vival patterns between implanted animals and non- Defined here as a non-nociceptive allostatic load potentially affecting well- implanted controls were detectable between the ages of being (e.g., dyspepsia—including nausea and dysmotility, tachycardia, hypo- or hypertension, hypo- or hyperthermia, hyperventilation). 14  months to five years [65]. From the ratio of dual- to Defined as an unpleasant sensory and emotional experience associated single-tag data returns in 20 mortalities detected to date with actual or potential tissue damage or described in terms of such dam- (through 2016) and in 10 dual-tag carcass simulations, age [64]. Horning et al. Anim Biotelemetry (2017) 5:13 Page 5 of 15 data return probability was estimated at >0.98 [49]. Of the 17 female Steller sea lions in that study implanted with single (n = 1 animal) or dual tags (n = 16 animals) between 2005 and 2014, eight animals have died by pre- dation [49], and nine remain alive. Of these, only three have reached a reproductive age. The first female implanted with a single LHX tag in 2005 at the age of 1.4 years was confirmed with a suckling juvenile in 2013 at age nine (see Fig. 2) and with a suckling pup in 2015 at age 11 (L. Jemison, ADFG pers. comm.). The second old - est female was implanted with dual LHX tags in 2008 at the age of 1.8 years, and a live birth was confirmed via a remote video observation system in the region in 2013, at Fig. 3 Lateral abdominal radiograph of a 125‑ day‑ old female harbor the age of seven years (J. Maniscalco, pers. comm). The seal with a body mass of 30.7 kg showing a second‑ generation LHX2 animal was resighted as recently as June 2016, but the tag. The tag was implanted 79 days earlier, at a body mass of 12.4 kg reproductive status could not be ascertained at that time. as described in Horning et al. [53] (© Vancouver Aquarium, DFO permit, Vanc. Aq. ACC no. 2012–06) The third oldest female was last sighted in 2016 at the age of seven and not associated with a pup at that time. In 2014, Horning et  al. [53] abdominally implanted In September of 2016, Horning, Boveng and collabo- single second-generation LHX2 tags into three recently rators implanted dual second-generation intraperito- rehabilitated harbor seal pups (Fig.  3). All three animals neal LHX2 tags into 10 subadult and adult wild harbor exhibited the expected inflammatory response but recov - seals in the Aleutian Islands (Horning et  al. unpubl. ered well. Wound healing and the acute phase of the data, Fig.  4). The animals underwent implant surgery inflammatory response were resolved by six weeks after within 2–4 h of capture and were released 2–3 h after surgery. After that time, all blood analytes were within recovering from anesthesia. Surgeries were conducted ranges observed in non-implanted animals [53]. Survival as described in Horning et  al. [53], within a portable was confirmed, and all three animals tracked for about surgical container setup on the back deck of the 33-m one year after release through external satellite transmit- research support vessel R/V Norseman. All ten ani- ters [53]. mals also received two external satellite transmitters for postrelease studies of movement and dive behavior. All ten animals were successfully tracked for a mini- mum of 60  days after release, and this tracking effort is continuing (Boveng et  al. unpubl. data). These ten ani - mals represent the first instance of at-sea intra-abdom - inal implantation surgeries with same-day release, in a pinniped. Best practice recommendations In the absence of specific guidelines, researchers have relied primarily on select studies in justifying experimen- tal and device designs. Here we propose 15 specific rec - ommendations to guide investigators and regulators in preparing and reviewing applications of fully implanted tags (FITs) in pinnipeds, based on our collective experi- ence over the past decades. Due to their very small size, Fig. 2 Adult female Steller sea lion marked with brand = 908. This extensive use and wide acceptance in veterinary practice, female received a single first ‑ generation LHX implant on September we specifically exclude passive devices (PIT tags) from 27, 2005, and was released on November 22, 2005. The female was approximately 1.4 years old when released. This image with the these considerations. Our recommendations are not female nursing her yearling offspring was taken on July 13, 2013, with societal guidelines and should supplement rather than the female just over nine years old. The female was confirmed with supersede many previously published recommendations a newborn pup in 2015 at the age of 11 years and last resighted in on animal research, capture, handling, sampling, captiv- 2016 at the age of 12 years (© AK Dept. of Fish & Game, photographer ity and telemetry [8, 12, 13]. Betsy Van Burgh, pursuant to NMFS permit no. 14325) Horning et al. Anim Biotelemetry (2017) 5:13 Page 6 of 15 for many vital rate studies in the Gulf of Alaska [66–68], but these approaches have not been techni- cally viable for more remote locations in the Aleutian Islands. FITs such as LHX tags have the potential to provide data that cannot be collected by any other means in remote locations or at sea, such as exact dates, locations and causes of mortality—including predation events—or parturition events. Justifications and alternatives should also be consid - ered within the framework of the Three R’s: Reduc- tion, Refinement, Replacement [12, 69]. Reduction is often understood as the use of a smaller sample size; however, this can also be achieved by the more reliable collection of more or higher resolution data per subject [70]. Refinement refers to improve - ments in the way experiments are carried out that result in reductions of negative effects on animals or improved animal welfare. For example, implanted tags have the potential to reduce or eliminate drag- Fig. 4 Abdominal implantation surgery is being conducted under related energetic costs associated with external tags, standard, aseptic procedures utilizing sterile instruments, surgical which may be considered a refinement [13, 29]. This garb and isoflurane gas for general anesthesia. A harbor seal is placed potential refinement needs to be balanced against on an insulated, elevated table in dorsal recumbency and the surgical area covered in a sterile, fenestrated drape. Positive pressure mechan‑ the impact of surgery. An important consideration ical ventilation is used in a partial rebreathing circuit. The portable is the anticipated duration of deployments in view surgical unit is heated. The surgical team consists of a veterinary of the cumulative effects on energy budgets in rela - surgeon, a sterile assistant and a non‑sterile anesthetist (© Markus tion to progressively waning impacts of surgery. Inci- Horning, pursuant to NMFS permit no. 19309, AUP A/NW2016‑1) dental disturbance effects may be greater for mark- resight designs that may require substantially larger sample sizes and multiple physical site visits to deter- 1. The use of FITs should be justified for specific mine re-encounter rates, as compared to known- experimental designs in view of potential alter- fate sampling designs with spatially and temporally natives and importance of data unrestricted telemetric re-encounter efforts, such as LHX tags. Known-fate sampling designs could be This justification needs to consider the mode, time considered a reduction (in sample size) and a refine - frame and likelihood of data recovery, as well as the ment (reduced disturbance). Replacement avoids the experimental design and sample size. Alternatives use of animals altogether. Recognized techniques to consider may include: mark re-encounter studies for replacement include the use of already collected based on temporary, permanent or natural markings; data. This could be facilitated through the telem - direct or remote observations of individual behav- etric collection of high-resolution, high-density data ior and reproductive status; cross-sectional popula- sets that may lead to enhanced opportunities to use tion counts; the use of externally attached telemetry computer models to simulate animal responses to devices; genetic studies; as well as other approaches. situations or the environment. Thus, there is a direct Valid justifications may include: essential data can - relationship between the quality of data obtained in a not be collected by any other means; or the predicted study and the potential for future replacement. data recovery probability with sufficient statistical power, spatiotemporal resolution or sensitivity is too Experimental designs should consider the a priori low for any alternative; or the alternatives are likely establishment of animal selection criteria. Some cri- to result in greater impacts on individuals or greater teria may be linked to the experimental design such disturbances on larger groups. as sex, age or size and reproductive status. When the selection is not critical to the sampling design (i.e., As an example, video observations combined with differences in health status, size, age or other cri - permanent markings have been successfully used teria are not the focus of the study), animals with Horning et al. Anim Biotelemetry (2017) 5:13 Page 7 of 15 lower risk of complications or those likely to have implants in beavers [74]. Other possible complica- a lower population level impact, could be selected tions include obstruction of other tubular abdominal (e.g., larger or older animals, males). The inclusion structures, such as the reproductive tract, pancre- or exclusion of animals as a function of their health atic ducts or ureters. Device pressure can result in status (e.g., body condition, injuries) is an impor- occlusion of vascular, nervous or lymphatic supply of tant ethical consideration and can also increase abdominal structures and potential tissue necrosis. data return probability and enhance data quality. Early studies using free-floating implants in mam - However, use of such criteria may introduce biases mals ranging in size from deer mice to brown bears in estimates (e.g., behavior or survival) that may or have reported fewer mortalities than those using may not be correctable if the interest lies in under- devices not designed to remain free-floating, and all standing the entire population. Finally, it should be concluded that the former was the preferred tech- pointed out that cost savings alone are generally not nique, generating fewer potentially critical compli- considered an acceptable justification for the use of cations (e.g., dehiscence, hemorrhaging, bacteremia FITs [13]. and sepsis) than a subcutaneous application [72, 2. Consider the most suitable locations for FITs and 75–77]. In pinnipeds, studies have reported compli- device fixation cations from subcutaneous devices [50–52]. How- In pinnipeds, FITs have been placed in subcutaneous ever, no complications attributable to properly con- locations [41, 50] and intraperitoneally [43, 53]. The ducted intra-abdominal placement of sterilized FITs latter may be considered more invasive, and compli- have been reported in literature, or encountered in cations such as dehiscence and infections may lead our studies, suggesting this method as preferable to to severe consequences, and even death. However, subcutaneous implantation [33, 37–40, 42, 45, 47, 49, the subcutaneous blubber layer in aquatic mammals, 53]. and especially in phocids, is a highly vascularized 3. Validate safe designs for FITs and metabolically very active tissue [71]. This may We recommend that safe device designs be vali- result in a substantially greater likelihood of compli- dated through the empirically confirmed absence cations ranging from tissue reaction and inflamma - of detectable effects beyond an initial, time-limited tory response to infection and extrusion (e.g., [41, and expected response, for animals of comparable 50, 72]). Devices placed within or underneath blub- body shape, size, behavior, physiology and life his- ber are somewhat fixed by the requirement to cre - tory. There is a clear need to separately consider each ate a space to accommodate the tag. Intraperitoneal species and life history stage rather than developing devices however can be surgically fixed or remain a single rule that fits all [8]. This applies to the selec - free-floating in the abdominal cavity. Some research - tion of effect parameters monitored as well as the ers prefer to promote connective tissue growth and size and shape of FITs [9]. The expected responses adhesion, in part to facilitate recovery of implanted to implant surgery that have to be considered at devices [73], or to reduce likelihood of interfering the very least include a foreign body response and a with pregnancies and parturition. However, recov- wound healing response. Monitoring parameters to ery of implanted devices has been feasible with free- consider include any that could be indicative of these floating implants in sea otters [40, 47]. two responses, examples include CBC including The potential for complications in free-floating total white blood cell count and differentials, clini - devices should be considered: devices may become cal chemistry values (e.g., total protein, globulins), attached to the mesentery or omentum, may enter acute-phase protein levels (e.g., fibrinogen, hapto - the omental bursa or may become lodged across the globin), as well as visual tracking of incision site heal- pelvic canal. Attachment may occur if the external ing. We further propose that device volume, mass, surface of tags is coated with a material that allows density or buoyancy and cross-sectional area all be or promotes adhesion, development of scar tis- considered and reported in validating safe designs. sue and fibrous encapsulation. Entrapment may Traditionally, mass thresholds have been sug- occur depending on the size, shape and mass of a gested but also criticized [8]. From the early days of device, in relation to the size of the bursa or the pel- implantable telemetry, recommendations were made vic canal. Adhesion or entrapment may secondarily for the mass of implanted telemetry devices not to result in obstructed or torsed intestines, depending exceed 2–5% of animal body mass [78–80], though on the size, shape and mass of the device. Adhesion these were not based on any quantitative assessment has been reported as responsible for some of the of effects of implants of various sizes on behavior and very few observed complications in intraperitoneal survival. Indeed, some references to largely anecdo- Horning et al. Anim Biotelemetry (2017) 5:13 Page 8 of 15 Table 1 Recommended descriptive device parameters, shown here for select tags used in recent marine mammal studies (see Table 2) a b c d e f Device Volume Mass Area Length Force (static, Force (dynamic) Pressure Pressure 2 −2 (ml) (g) (cm ) (mm) submerged) at a = 9.8 ms (static) (N/ (dynamic) 2 −2 (N) (N) mm ) at a = 9.8 ms (N/mm ) LHX1 202 118 13.85 128 −0.87 1.16 6.28 8.38 LHX2 79 54 8.55 97 −0.26 0.53 3.04 6.20 VHF 119 150 13.37 90 0.27 1.47 2.02 10.99 TDR 17 35 2.3 69 0.18 0.34 7.83 14.78 Effect Body mass Cost of Entrapment Entrapment Cost of Cost of locomotion Tissue effects Tissue effects set point locomotion locomotion Smallest cross-sectional area Longest exterior dimension −2 Force is calculated for subjects fully submerged in saltwater (density 1.025) as F(N) =[volume (ml) × 1.025 − mass (g)]× 9.8067 (ms )/1000; a negative value indicates the device is buoyant d −2 This corresponds to the inertial force resulting from the tag mass being exposed to an acceleration a and is calculated as F(N) = m (kg) × a (ms ). For −2 a = g = 9.8067 ms , the force is also equal to the tag weight in air at sea level e,f This is a measure of the maximum pressure the tag exerts on surrounding tissue, and is calculated as force per unit area. Static pressure is exerted by the buoyancy in a non-moving submerged animal, and dynamic pressure is resulting from dynamic acceleration of the animal and varies with a. For a = g, this equals the pressure exerted by a tag in a non-moving, non-submerged animal tal suggestions of size limits are based on completely of tag entrapment in the omental bursa, mesentery arbitrary considerations such as the typical size or or the pelvic canal. Intestinal torsion secondary to mass of mature eggs or fetus at the end of gestation omental entrapment or adhesion may be a function (see [13]). Device mass is likely related to increased of the inertial or rotational forces an adhered device cost of locomotion, especially for birds [81, 82]. Para- can generate for a given acceleration. Localized tis- doxically, some larger birds may be more affected by sue effects may also be a function of the amount identical mass percentages than smaller birds ([81], of pressure a tag can exert on surrounding tissue. and see [8]). Furthermore, device volume may be Though a simplification, these effects can be stand - more closely related to altered body mass set points ardized for comparative purposes via area-specific in some animals [83], and buoyancy may affect cost force (pressure), which may be approximated from of locomotion more than mass [84, 85]. Several device mass and shape. researchers have suggested that implant size indi- Table 1 lists the parameters we recommend as com- ces based on the percentage device weight in water parative device descriptors, for a number of tags or volume to body mass ratios should be preferable used in recent studies. All standardized, compara- for aquatic vertebrates [13, 17, 19, 31, 32]. Beaulieu tive static and dynamic forces and pressures can be et al. [32] specifically suggested using device volume calculated from volume, mass and area, and only the per body mass (ml/kg) as a metric. They compared first four parameters need to be included in publi - results from their own study to eight other stud- cations. It should be noted that dynamic values are ies on aquatic birds (mostly penguins). Their own of course dependent on animal movement. Values ratios were approximately 4.5  ml/kg. Two studies listed in Table 1 are based on a standard acceleration −2 with comparably larger devices reported no effects of 1  g (9.8  ms ) solely for comparative purposes. on common eider (6.5  ml/kg) and harlequin ducks Quick acceleration or turns could result in much (7.5 ml/kg), though they cite the study by Culik and higher values. Wilson [28] as reporting effects at a mean ratio of Volume effects (on body mass set point) and mass 1.8 ml/kg (but note the above-mentioned electrodes, effects (on cost of locomotion) are likely relative to and anchored devices in the two bird studies). These host size, and thus species-specific demonstrated divergent results further support the notion that for safe ratios expressed in proportion to body mass aquatic animals as well as other taxa, one size rule seem reasonable. Safe ratios for four aquatic mam- does not necessarily fit all. mals in which devices from Table  1 have been vali- Physical dimensions including length and the small- dated at least partially through the absence of nega- est cross-sectional area may relate to the likelihood tive effects, are shown in Table 2. Horning et al. Anim Biotelemetry (2017) 5:13 Page 9 of 15 Table 2 Tag volumes and  mass relative to  body mass from  select recent studies in  four aquatic mammal species using intra‑abdominal dual FITs Species Tags n ml/kg % Body mass Eec ff t testing References California sea lion LHX 2 2.2 (3.1) 0.13 (0.18) 1,2,5,6 [43] California sea lion LHX + LHX 2 2.4 (2.9) 0.14 (0.17) 1,2,5,6 [43] Steller sea lion LHX 2 1.8 (1.9) 0.10 (0.11) 1,2,3,4,5,6,7,8 [43, 46, 49, 57, 60, 63, 65] Steller sea lion LHX + LHX 34 3.1 (5.5) 0.18 (0.32) 1,2,3,4,5,6,7,8,10 [43, 46, 49, 57, 59–65] Steller sea lion LHX + LHX2 9 2.8 (3.8) 0.17 (0.23) 1,2,3,4,5,6,7,8,9,10 [49, 59–65] Harbor seal (pup) LHX2 3 6.0 (6.3) 0.41 (0.43) 1,2,3,4,5,6,7,8,10 [53] Harbor seal LHX2 + LHX2 10 2.5 (3.6) 0.17 (0.24) 6,7,8,9,10 [Horning et al. unpubl. data] Sea otter VHF + TDR 31 5.0 (7.1) 0.68 (0.97) n/a [40, 47] For applications with multiple internal tags, volumes and masses are summed. n refers to sample sizes in referenced studies. Mean values are listed with maximum ratios in parentheses, and sample size is indicated. Effect testing conducted in these studies—some continuing—is indicated with references to publications Effect testing 1. captive postop monitoring ≥6 weeks, mass (gain), appetence, 2. postoperative transmitted temperatures, 3. CBC and differential, 4. acute and chronic inflammatory responses measures, 5. captive behavior, 6. postrelease movement, 7. postrelease behavior, 8. postrelease survival, 9. postrelease reproduction, 10. in progress/continuing The effects of forces that tags can exert to raise the and foreign body giant cell growth, which may also cost of locomotion and that may contribute to intes- reduce delays in wound healing. The type of material tinal torsion, and also the effects of pressure on sur - used (polymeric, ceramic, metallic) is not connected rounding tissues (see Table  1) are directly driven by to biocompatibility, but passivating the material sur- physical properties of the tag and are independent face to minimize non-specific protein interaction from the size of their host. The above considerations may be key [89]. also suggest that smaller is not necessarily always We strongly recommend to only use devices with better, and that safe volume and mass ratios should outer materials that have been tested and approved not be interpreted as thresholds. Values below tested either under the United States Pharmacopeia (USP) ratios may only be considered safe in conjunction Class 6 standard for biological reactivity or preferen- with an evaluation of static and dynamic forces and tially the newer ISO-10993 standard for biocompati- pressures. Published ratios and force values should bility [90]. Alternatively, investigators could consider be useful in comparing and optimizing tag designs, conducting assessments similar to those allowed and informing experimental designs, but do not under the ISO standard. The USP standard investi - eliminate the need to conduct impact assessments. gates biological reactivity of elastomers, plastics and Priority should be given to validating and reporting polymeric materials in vitro and in vivo. Under Class safe designs. 6, these standardized tests are conducted on mate- 4. Use devices with an outer material tested for rials in non-polymerized and cured states: acute biological reactivity or conduct biocompatibility system toxicity test, intracutaneous test and implan- testing with actual FITs tation test. Certified cured compounds must fur - As a general rule, the materials encasing or leach- thermore meet strict requirements on leachates. The ing out of an FIT have the potential to evoke a for- duration of implantation test is however very limited eign body response [86]. Foreign body reactions to five  days. Certification of coatings and materials to implanted objects vary in severity and may lead to the USP standard does not prove favorable bio- to phagocytic attacks, fibrous encapsulations and compatibility of devices. However, the use of USP- chronic inflammation, as well as many other acute, certified materials is more likely to result in favorable medium- and long-term effects [86]. Very few stud - biocompatibility results. ISO-10993 addresses bio- ies have investigated long-term histochemical effects compatibility and moves well beyond the USP cer- of FITs on wild animals. A number of studies have tification by considering cytotoxicity, sensitization, identified persistent pathological reactions attribut - acute systemic toxicity, chronic toxicity, subchronic able to FITs, ranging from organ-invading granula- toxicity, genotoxicity, hemocompatibility, throm- tion in wild carp [87] to peritoneal sarcomatosis in bogenicity, pyrogenicity, carcinogenicity as well as laboratory rats [88]. Surface coating FITs with bio- reproductive and developmental toxicity and bio- compatible materials is one way to minimize inflam - degradation. Using devices coated with an ISO- matory response and reduce macrophage adhesion 10993-certified material is one option for investiga - Horning et al. Anim Biotelemetry (2017) 5:13 Page 10 of 15 tors. However, under ISO-10993-6, an in  vivo study to limit current and temperature (such as ther- of the FIT may replace some of the above-listed mal fuses). Multi-cell systems need to be protected in vitro tests of constituent materials if the study was against imbalanced discharge of cells. Complete dis- designed for this purpose, with appropriate assess- charge of lithium primary cells can be problematic, ment endpoints, and all recommended scientific and needs to be managed by device electronics, or principles were applied. Appropriate assessments tested. may include laparoscopic or histological screening 7. Properly sterilize all FITs for inflammatory response. Recommended durations Like any vertebrate, pinnipeds are susceptible to for in vivo implant testing range from 12 to 78 weeks. infections from contaminated FITs, and full steri- Durations for testing constituent components and lization is therefore absolutely essential. Steriliza- materials can be shorter, from 8 to 12 weeks [90]. In tion requires the complete removal or destruction addition to device descriptors listed in Table  1, all of all pathogens including microorganisms, spores studies should always include details on the type of and virus from the FIT and is distinct from disin- material coating all FITs used, and how biocompat- fection. Dipping FITs in disinfectant solutions, such ibility was determined. as any alcohol or chlorhexidine, does not result in 5. Use devices that meet pressure ratings with a 3× sterilization and is therefore not acceptable for any margin of safety for the species of interest FIT applications. There are liquid sterilants such as Damage to an FIT deployed in a diving animal glutaraldehyde that can be used only if the required from excessive pressurization is likely to have cata- concentrations, temperatures and immersion dura- strophic and potentially fatal consequences for the tions (often on the order of hours) are strictly host, especially for FITs containing hollow spaces maintained. Gas sterilization by ethylene oxide or or lithium batteries. Yet, no safety ratings exist for hydrogen peroxide plasma is effective and has the such applications. There are two aspects to con - advantage of allowing prepackaging of FITs for easy sider: uncertainty about the likely maximum depth transport and field use after sterilization. All meth - exposure and engineering design rules for fatigue ods may have advantages and disadvantages, such and manufacturing tolerances. We propose the fol- as toxicity of agents, the requirement of specialized lowing safety factors. With standard deviations for equipment, presence of residue and chemical or the maximum dive depths reported for most spe- thermodynamic interactions with FITs. It is essen- cies averaging about 25% [91], the mean of reported tial that sterilization is fully maintained until and maxima plus 4× the standard deviation is likely to during FIT insertion, and that any sterilizing agents contain 99.999% of cases, suggesting a safety factor are properly outgassed and any residue rinsed off via of 2× mean of reported maximum depths. Deep sterile saline prior to insertion. Any FIT with possi- ocean high-pressure manufacturing industry uses a bly compromised sterility should not be used. For a design rule safety factor of 1.5× [92, 93]. Together, review, see [10, 13, 95]. these yield a 3× safety factor for FIT pressure rat- 8. Use accepted, standardized aseptic surgery pro- ings. Data from adults should be used for FITs likely cedures to remain implanted into adulthood. For sexu- For the same reasons described under recommen- ally dimorphic species, data from the targeted sex dation 7, following standard aseptic procedures is should be used. To give an example, if the mean of all essential. This includes use of a clean environment maximum dive depths reported for adults of a spe- and sterile equipment including drapes, surgical cies is 350 m ± 25% SD, then a rating of 700 m will garbs, gloves and instruments. The skin incision site likely not be exceeded by more than 1 in 1000 indi- should be properly prepared using aseptic technique viduals. Applying the engineering factor of 1.5× will and isolated by sterile drapes. See [10, 13, 29]. then lead to a pressure rating design requirement of 9. Use appropriate anesthesia and analgesia 1050 m for FITs used in this project. The surgical implantation of an FIT without a surgi - 6. Use approved designs for lithium primary cells in cal plane of anesthesia is an inhumane act and should FITs not be performed. Subjects should be appropriately Most FITs use lithium primary batteries as a result monitored during procedures and recovery. Mod- of their high energy density. Such cells are safe to use ern, multi-modal peri- and postoperative analgesia for biomedical implants and FITs, providing stand- should always be used to mitigate pain [13, 95–97]. ard safety measures are implemented [94]. These Proper pain management will likely prevent delayed include using only cells with a lithium metal content recovery and improve the outcomes of projects using less than 1  g per cell and with protective measures FITs. Horning et al. Anim Biotelemetry (2017) 5:13 Page 11 of 15 10. Surgeries, anesthesia and postoperative monitor- include discomfort and pain, as well as reduced ing should be conducted or directly supervised by appetence, mobility or vigilance. Assessments qualified and appropriately trained personnel may include physiology (temperature, stress hor- Personnel should also be knowledgeable and experi- mones, blood metabolites), behavior and move- enced in medical and surgical care of subject species ment (posture, resting), and changes in food including emergency treatment. intake, and could take advantage of data from 11. Consider the advantages and disadvantages of the FITs (e.g., body core temperatures, data from prophylactic treatment with antibiotics, within accelerometers) (e.g., [53, 59–62]). regulatory constraints b) Medium-term effects ranging from days to The prophylactic application of antibiotics has been months proposed and practiced but is not without contro- These effects are critical in determining possible versy, in part as a result of increased incidence of impacts on data. Until demonstrated otherwise, pathogens resistant to antibiotics (e.g., [98, 99]). A it is necessary to assume that for a given period determination for use of prophylactic antibiotics after surgery and until all healing processes are should be made based on a number of factors includ- completed, implanted subjects may experience ing the nature of the procedure, technique used, impaired movement, performance or foraging facilities available, potential surgical complications, ability. postsurgical release site and anticipated behavior Two recent FIT studies revealed measurable of the animal. Considerations should include use of physiological responses linked to inflamma - antimicrobial suture material. Because pinnipeds tory processes that persisted through at least may be legally harvested in some localities, regula- five weeks after surgery [53, 57]. Such assess- tory constraints related to food animals may also ments may initially require captive work under apply. See [13, 29, 95]. controlled conditions for the purpose of devel- 12. Plan, conduct and report on assessment of short-, oping a study inclusion criterion (see recom- medium- and long-term FIT effects mendation #13). Alternatively, a controlled effort As researchers using FITs, we have to consider any in captivity could identify suitable proxies to possible effects of devices or associated procedures derive a study inclusion criterion after release, on the data to be collected and on the study subjects especially given the desirability of minimizing [8–10, 13, 29, 95]. The former is an absolutely essen - captivity (see recommendation #14), and since tial component of the scientific process. The latter captivity may also lead to effects. Assessments derives from the application of accepted principles for medium-term effects may include monitor - of ethical treatment of research subjects. Ethical ing of inflammatory response, analysis of activ - considerations also dictate that the determination of ity patterns and effects on growth, foraging FIT impacts be extended at least through the likely behavior, reproductive behavior, movement and period of device retention and not just through the migration. Data from internal or external tags period of collection of data from FITs. Some pro- may prove useful, providing the devices will not jects have successfully carried out the deployment affect the assessment (e.g., [53, 57, 60, 63]). and subsequent recovery of FITs in wild aquatic c) Long-term effects ranging from months to mammals [40, 47, 48]. However, the majority of FITs years and through the likely period of FIT deployed on wild animals will never be recovered retention [49–52] and will therefore be carried by the host ani- Understanding and quantifying long-term mal for the remainder of their lives. As a result, we effects is crucial to any vital rate studies. Fur - should consider three broad time periods when plan- thermore, some effects may have low-level accu - ning and conducting studies of FIT effects: mulating impacts that may become more detect- able when integrated over longer periods of time [11, 100]. While short- and medium-term effects a) Short-term effects ranging from hours to may be studied at the level of proximate mecha- days nisms, long-term effects can more readily be assessed via ultimate impacts on growth, migra- Detecting and understanding short-term effects tion, reproduction and survival (e.g., [65]). may be critical to determining how quickly after It is inappropriate to assume that FITs will not a procedure animals may be safely released and affect data or subjects simply based on size or to improving procedures and mitigating effects. mass percentages (see recommendation #3) or Examples of possible short-term effects may Horning et al. Anim Biotelemetry (2017) 5:13 Page 12 of 15 based on demonstrated absence of effects in ‘Carefully consider the duration of postsurgery cap- other species carrying similar devices. Evidence tivity.’ In connection with FIT implantation surgery, supports that effect magnitudes are specific to project planners should therefore weigh any poten- species, devices, animal state and circumstances tial benefits of controlled access and monitoring and [8]. Transferability of such findings across spe - potential disadvantages of stress and delayed return cies and devices is therefore limited, and it is to the natural environment when under temporary prudent to always carry out and report control captivity. Amount and lengths of manipulations studies [8, 9]. as well as duration of temporary captivity for wild Implanted tags may also passively or actively animals before and after surgery should be limited increase the detectability of hosts by predators. as much as possible [8, 101, 102]. However, captive Some tags may be echogenic and may produce monitoring is an extremely valuable experimental acoustic or electromagnetic signatures. Acous- tool and can lead to refinements in considering post - tic emissions could also be perceived by hosts operative recovery and monitoring periods through and may alter their behaviors. Where possi- detailed studies of discomfort and pain, wound heal- ble, researchers should consider using FITs and ing, observations of postoperative complications or external tags to provide assessment data. Recent confirmation of their absence and observations of developments enable life-long FITs to provide postoperative behaviors. survival and reproductive data, and develop- 15. Report all findings in accessible, peer-reviewed ments to enable electronic mark-resight designs literature using FITs are underway (e.g., [6]). If FITs are It is imperative that all findings, including nega - used to collect vital rate or assessment data, then tive effects, are reported in readily accessible peer- the failure rate of tags or data recovery prob- reviewed literature. This includes details on safe ability needs to be accurately quantified and FIT designs, surface materials and biocompatibility, corrected for [46, 49]. Even outside of vital rate study inclusion criteria, results from all effect assess - studies, data on tag failure rates will be useful in ments, as well as tag failure rates and data recovery planning future telemetry studies. The simulta - probabilities. The latter are essential for sample size neous deployment of multiple internal or exter- estimation and the development of future projects. nal tags may be a powerful tool in support of long-term vital rate and FIT assessment studies. Conclusions However, with increasing manipulations and tag We present 15 specific best practice recommenda - burdens proper assessments on combined loads tions for the application of fully implanted telemetry will become even more critical. devices in pinnipeds. These recommendations should 13. Derive and apply a specific study inclusion crite - be considered by researchers preparing projects and rion by regulatory bodies authorizing projects. These initial Many FIT studies referenced here were designed to recommendations may be refined or adjusted through collect primary data within days of surgery, when new studies, within the guiding principles of the Three the presence of effects from surgery and devices has R’s [69]. Deviations or exceptions should be considered to be assumed. Very few of these studies specifically only when convincingly justified. While we developed derived and reported a study inclusion criterion these recommendations specifically for pinnipeds, some (see also [5, 9]). An arbitrary cutoff not backed by may be applicable to other groups of aquatic animals, applicable data does not support the absence of FIT such as sea otters or aquatic birds, or other applica- effects in the data set and is no better than not using tions, such as partially implanted (transdermal) tags, or a criterion. Without a specific, quantitative criterion even external tags. For all users and regulators of FITs, backed by demonstrated absence of effects or a valid it will be important to avoid creating a ‘catch 22’ situ- argument about transferability of inclusion criteria, ation, where studies are not allowed to proceed or be reported findings lack scientific validity. published until the absence of negative effects has been 14. Minimize manipulations and temporary captiv- demonstrated. Such determinations cannot be carried ity out without risking these effects and will require sam - The report by the Joint Working Group on Refine - ple sizes that cannot usually be achieved through single ment [13] recognizes that ‘wild animals are liable studies. A prudent approach may therefore gradually to find capture and handling extremely stressful build on initial control and validation studies, while and that this represents an experimental harm.’ The providing plans to carry out effect assessments at all working group report specifically recommends to appropriate temporal scales. Horning et al. Anim Biotelemetry (2017) 5:13 Page 13 of 15 Abbreviations 9. Walker KA, Trites AW, Haulena M, Weary DM. A review of the effects of CBC: complete blood count; FIT: fully implanted tag; LHX: life history transmit‑ different marking and tagging techniques on marine mammals. Wildl ter; VHF: very high frequency. Res. 2012;39:15–30. 10. Mulcahy DM. Legal, ethical, and procedural bases for the use of Authors’ contributions aseptic techniques to implant electronic devices. J Fish Wildl Manag. MHo drafted manuscript and designed referenced FITs, MHa and PAT devel‑ 2013;4:211–9. oped referenced implant surgery protocol, MHo, JEM and MHa designed and 11. Maresh JL, Adachi T, Takahashi A, Naito Y, Crocker DE, Horning M, Wil‑ conducted referenced FIT studies, MHa, PAT, CEG, RKB, KW and SJ conducted liams TM, Costa DP. Summing the strokes: energy economy in northern implant surgeries, MHo, JEM, KAW, CRS, JPS and PLB designed or conducted elephant seals during large‑scale foraging migrations. Mov Ecol. referenced assessment studies. All authors participated in referenced implant 2015;3:22. studies, postoperative monitoring or assessment studies referenced here. All 12. Einstein R, Rowan C, Billing R, Lavidis N. The use of telemetry to refine authors read and approved final manuscript. experimental technique. In: Balls M, van Zeller A‑M, Halder ME, editors. Progress in reduction, refinement and replacement of animal experi‑ Author details mentation. Amsterdam: Elsevier; 2000. p. 1187–97. Alaska SeaLife Center, 301 Railway Avenue, Seward, AK 99664‑1329, USA. 13. Hawkins P, (editor). Refinements in telemetry procedures. Seventh Marine Mammal Institute, Oregon State University, 2030 SE Marine Sci‑ Report of the BVAAWF/FRAME/RSPCA/UFAW Joint Working Group on ence Drive, Newport, OR 97365, USA. Vancouver Aquarium, 845 Avison Refinement, Part A, vol 37, pp 261–299. Laboratory Animals; 2003. Way, Vancouver, BC V6G 3E2, Canada. Bridge Veterinary Services LLC, 9162 14. National Research Council 2011. Guide for the care and use of labora‑ Glacierwood Drive, Juneau, AK 99801, USA. The Marine Mammal Center, 2000 tory animals. 8th ed. Institute for Laboratory Animal Research, p. 246. Bunker Rd, Sausalito, CA 95965, USA. Department of Biosciences, Durham Washington, DC: National Academies Press; 2011. 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Best practice recommendations for the use of fully implanted telemetry devices in pinnipeds

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Springer Journals
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Copyright © 2017 by The Author(s)
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Life Sciences; Animal Systematics/Taxonomy/ Biogeography; Conservation Biology/Ecology; Terrestial Ecology; Bioinformatics; Freshwater & Marine Ecology
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2050-3385
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10.1186/s40317-017-0128-9
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Abstract

Electronic telemetry devices have enabled many novel and important data collection and experimental opportunities for difficult to observe species. Externally attached devices have limited retention and may affect thermoregulation, energetics, social and reproductive behavior, visibility, predation risk and entanglement. Internally placed, surgically implanted devices can mitigate some of these effects and may open additional experimental opportunities. How‑ ever, improper implementation can significantly affect animals and data. From a review of recent studies using fully implanted tags and studying their effects, we present 15 specific best practice recommendations for the use of such tags in pinnipeds. Recommendations address issues including device size, coating and sterilization, implantation surgery and effect assessment, within the framework of the Three R’s: Reduction, Refinement , Replacement. While devel‑ oped for pinnipeds, these recommendations could apply to other aquatic mammals and vertebrates and to partially implanted or even external tags. Keywords: Biotelemetry, Implant, Subcutaneous, Intraperitoneal, Marine mammal, Surgery, Reduction, Refinement, Replacement the risk of entanglement, visibility and predation [5, 7– Background 11]. Surgically implanted internal devices may reduce Electronic telemetry devices have been used effectively to some of these effects, allow longer-duration deployments track location and movement and to monitor foraging and the use of additional sensors, but may also result in and reproductive behavior as well as the physiological substantial and potentially catastrophic effects if improp - and reproductive state of terrestrial, avian and marine erly implemented. Recent discussions [8, 12] and working vertebrates for more than five decades [ 1, 2]. This has group reports on ‘refinements in telemetry procedures’ been particularly useful for difficult to observe taxa such have highlighted that ‘Telemetry is often presented as a as marine vertebrates [3–6]. Most commonly, such refinement, in that it can reduce or eliminate stress devices are externally attached, resulting in limited moni- caused to animals (e.g., by restraint), but it is vital to toring durations for animals that molt or shed on a regu- remember that telemetry, like all other procedures on lar basis. Furthermore, external devices can affect social, animals, also needs to be refined’ [ 13]. reproductive and movement behavior, or the energetics of locomotion and thermoregulation, and may increase *Correspondence: markush@alaskasealife.org Defined here as any active electronic monitoring or transmitting device Alaska SeaLife Center, 301 Railway Avenue, Seward, AK 99664‑1329, USA that once fully implanted into any part of the body does not break the integ- Full list of author information is available at the end of the article ument. © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Horning et al. Anim Biotelemetry (2017) 5:13 Page 2 of 15 the conduct and publication of studies of short-term Existing recommendations by societies and recent and long-term effects of tags [26]. A recent report by workgroups the Joint Working Group on Refinement [13] does not In the USA federal funding agencies have adopted the provide specific recommendations, but does point out policy instituted by the Public Health Service on the that ‘smaller is better,’ and that adding mass can have a humane care and use of laboratory animals, under the significant physiological impact and can alter body mass Animal Welfare Act. This policy requires research to be set points. The report also references multiple studies compliant with the Guide for the Care and Use of Labora- that have shown that animals carrying devices can incur tory Animals [14]. The Guide provides important ethical measurable and significant energetic costs of transporta - guidance on principles of humane animal research with a tion, of a magnitude ranging from about half of the mass focus on biomedical laboratory settings, but few specific percentage (i.e., a tag adding 5% to the mass of a mam- procedural recommendations are applicable to research mal may result in an added energetic burden of 2.5%) to involving wildlife [15]. Recognizing these shortcomings, as high as double the mass percentage in flying birds (see the US National Science Foundation requested profes- also [27–29]). sional societies to develop taxon-specific guidelines suit - able for wild species and field work [15]. Most applicable Implanted telemetry devices in birds professional societies, the Guide and the Joint Working Barron et  al. [30] evaluated 84 published studies using Group on Refinement [13] point out the need to consider external or internal devices on birds for reported pres- and assess the impact of external and internal telem- ence or absence of specific effects. While most effects etry devices on research subjects. However, few consist- were small in magnitude (e.g., device-induced preen- ent guidelines exist across or within taxa with respect ing), the most consistently reported effect of devices in to shape, relative size, mass and volume of devices, with this meta-analysis was increased energy expenditure and respect to surgical procedures or the parameters that reduced nesting likelihood. Attachment methods requir- should be applied in considering the impact of devices ing anesthesia (i.e., anchored and implanted devices) [8]. had the highest reported incidence of mortality, while The American Fisheries Society provides no recom- external devices were the only type resulting in reported mendations for implanted telemetry devices in fishes, ‘device-induced behaviors.’ Furthermore, device effects of any kind [16]. Much of the recent work (since the late were more pronounced in relation to uncaptured controls 1990s) assessing the effects of implanted devices on wild than ‘procedural controls’ (those handled and temporar- animals has been conducted on anadromous fish, due ily captive in the same manner as tagged individuals) to management concerns and regulatory status of some suggesting some of the observed effects were due to han - species [17–21]. Authors have repeatedly challenged the dling and captivity. However, in a subsequent meta-anal- anecdotal, yet never formalized ‘2% rule’ for fish based on ysis of 55 studies on 49 species of birds, White et al. [31] the demonstrated absence of negative effects on swim - specifically compared effects between external and fully ming energetics, growth and survival for relative sizes implanted devices. This meta-analysis revealed consist - of tags up to 6.7% of body mass [17, 19, 22]. The Ameri- ently negative effects of externally attached devices, while can Society of Ichthyologists and Herpetologists suggests no consistent effects were reported for implants. The an upper size limit of 10% of body mass on an anecdo- authors concluded that internal devices are preferable to tal basis for implanted devices in amphibians and rep- external devices provided that risks associated with anes- tiles, but points out that sizes between 1 and 6% are often thesia and surgery can be mitigated. In diving or aquatic achievable [23]. The Ornithological Council quotes stud - birds, Culik and Wilson [28] found energetic and behav- ies suggesting that external or internal telemetry trans- ioral effects of both external (n  =  5 animals) and inter- mitters in birds should not exceed 5% of a subject’s body nal tags (n  =  2 animals) on Adelie penguins (Pygoscelis mass, but also points out that this value or a less com- adeliae). However, sample sizes were extremely small monly applied 3% threshold are completely arbitrary and and the implanted devices were connected to inter- that multiple conflicting studies found both presence and nal electrocardiography electrode wires and were fur- absence of effects of tags in the 1–3% mass range on sur - ther secured to the musculature via sutures. Such wires vival [24]. Guidelines by the American Society of Mam- and fixing sutures may increase the likelihood of device malogists [25] only vaguely recommend external devices effects. Beaulieu et al. [32] compared the effects of exter - not exceed 5–10% of individual body mass but do not nal (n  =  10 animals) and internal (n  =  6 animals) tags (separately) consider implanted devices. Finally, the Soci- on the foraging behavior of Adelie penguins. They noted ety for Marine Mammalogy provides no specific recom - altered foraging behavior in animals carrying internal mendation for external or internal tags, but encourages Horning et al. Anim Biotelemetry (2017) 5:13 Page 3 of 15 tags, but none in animals carrying external tags. How- whether the two remaining sea otters were misclassi- ever, the implants were secured with sutures, and only a fied as pregnant, had stillbirths, aborted prematurely single foraging trip per animal was observed, which for or whether the pups died after birth. Bodkin et  al. [40] implanted birds occurred less than 6  days after surgery. intraperitoneally implanted two telemetry devices into Interestingly, the meta-analysis conducted by White et al. each of 21 sea otters: one VHF transmitter and one [31] showed that most device effects reported tended time–depth recorder. The animals were subsequently toward zero with increasing sample sizes, suggesting that recaptured, and the archival data loggers were surgi- some reported effects may be outliers, or that methods cally removed. Tags were recovered from 14 animals improve with experience of investigators. The absence of that were recaptured after two months. One animal was a proportional mass effect (i.e., bigger tags are associated found dead after four years. No reasons for mortality with a greater effect magnitude) has been used to illus - were reported. One pregnant female that was implanted trate the arbitrary nature of mass-percent device size was subsequently recaptured with a pup. Subsequent thresholds [13, 29, 30]. studies reported on data derived from intraperitoneal tags implanted into sea otters, but possible effects were Fully implanted telemetry devices in aquatic not investigated or reported [47, 48]. mammals Within aquatic mammals, fully implanted telemetry Fully implanted telemetry devices in pinnipeds S I devices (subcutaneous, intraperitoneal ) have been Lander et  al. [41] tested four different kinds of subcu - tested or used in sea otters (Enhydra lutris), Eurasian taneous implants in 10 harbor seals with varied results. I I otters (Lutra lutra), North American river ot ters (Lon- Animals with resin-encased transmitters developed I I tra canadensis), nutria (Myocastor coypus), beavers fluid pockets and mucopurulent discharge, whereas (Castor canadensis), muskrat (Ondatra zibethicus), polar wax-coated devices elicited no such response. CBC and S S,I bears (Ursus maritimus), harbor s eals (Phoca vitulina), serum biochemistry values were within normal ranges Northern elephant seals (Mirounga angustirostris), Cali- within one week of surgery for nine of the 10 animals. S,I fornia sea lions (Zalophus californianus) and Steller sea The authors concluded that wax-coated implants were lions (Eumetopias jubatus) [33–53]. preferable for long-term subcutaneous deployments. As previously summarized [43], several studies that Green et al. [44] conducted trial implantations of subcu- used free-floating intra-abdominal implants reported taneous heart rate data loggers with electrocardiography on the effects of implants on reproduction in aquatic wires into three Northern elephant seals and three Cali- mammals. Reid et  al. [33] specifically studied reproduc - fornia sea lions. All animals recovered uneventfully from tive effects of intraperitoneal implants in North Ameri - the surgery, but the elephant seals then developed a ‘sub- can river otters over one to two reproductive cycles. In stantial inflammatory response’ and the devices had to be seven adult females, they observed 12 possible pregnan- removed. Blundell and collaborators [50] subcutaneously cies that resulted in eight litters. They concluded that the implanted wax-coated VHF transmitters (also used in the implants did not interfere with reproduction. Hernan- Lander study) in 277 harbor seals in Alaska. The trans - dez-Divers et  al. [38] also concluded that implants did mitters were programmed to send an altered signal when not affect survival or reproductive potential in North tag temperature dropped below 27 °C, indicating possible American river otters. Bohrman et  al. [45] reported on mortality or tag extrusion. Animals were released within successful reproduction in one single North American hours of surgery, and no consistent postoperative moni- river otter with an intraperitoneal implant. Fernandez- toring besides automated VHF tracking was reported. Moran et al. [39] reached the same conclusion in a study No altered signals were detected during the study that of Eurasian otters. Nolfo and Hammond [42] implanted could be attributed to an actual mortality. Four isolated VHF transmitters intraperitoneally into 20 adult nutria, tags were recovered, and one animal was recaptured after nine males and 11 females. All females were pregnant. one year with a partially extruded tag. Manugian et  al. One female aborted her near-full-term litter within one [51, 52] reported on the use of wax-coated subcutane- day of surgery and prior to release, likely as a result of ous VHF implants in nine harbor seals closely monitored anesthesia. The authors found no evidence of morbidity up to three weeks before release, and another 32 released or infection. They concluded that the implants did not immediately after implantation. No complications were interfere with reproduction. Monnett and Rotterman reported from this study, though the authors do refer to [37] intraperitoneally implanted devices into 19 adult one instance from a prior study (it is unclear which study female sea otters that were deemed pregnant at time of they refer to) where a subcutaneously implanted wax- implantation based on abdominal palpation. Seventeen coated tag was observed migrating out of a juvenile har- of the 19 pupped successfully. They could not determine bor seal about nine months after implantation. Horning et al. Anim Biotelemetry (2017) 5:13 Page 4 of 15 Life‑long implanted vital rate transmitters In 2004, Horning—in collaboration with Wildlife Com- puters, Inc. (Redmond, WA)—completed the develop- ment of a new implantable telemetry device, the life history transmitter (LHX tag) [54]. LHX tags were spe- cifically designed for vital rate telemetry in California and Steller sea lions. The cylindrical tags with hemispheri - cal ends (42  mm diameter, 128  mm length, 202  ml vol- ume, 118 g mass, 0.87 N buoyancy) are intraperitoneally implanted [43] and record data throughout the life of the host. Summary data are only transmitted via the Argos satellite system postmortem, after the positively buoy- ant tags are liberated from decomposing, dismembered or digested carcasses. In 2014, development of the sec- ond-generation LHX2 tag was completed (with Wildlife Fig. 1 A second‑ generation LHX2 implantable Argos‑ compatible sat‑ Computers, Inc.). LHX2 tags are smaller (Fig.  1, 33  mm ellite transmitter ( Wildlife Computers Inc., Redmond, WA) is shown on the right. Exterior dimensions are 97 mm length by 33 mm diameter. diameter, 97 mm length, 79 ml volume, 54 g mass, 0.26 N The tag mass is 54 g; buoyancy is 0.26 N. The device is coated in Epo‑ buoyancy) and can be programmed to evaluate tempera- Tek 302‑3M resin, a material certified under the USP Class 6 standard ture patterns for parturition events. LHX tags can be for biological reactivity. The QR code links to information on the tag, used to determine date, location and causes of mortality project and rewards for return. A VHF radio transmitter (ATS Inc., Isanti, [49, 55], and also age at primiparity and lifetime number MN) is shown in the middle. Exterior dimensions are 90 mm length by 59 mm width by 30 mm thickness. The transmitter mass is 150 g; of pups born if deployed in pre-parous females. buoyancy is −0.27 N. The device is cast in an unspecified electrical Horning, Mellish and collaborators implanted single or resin and coated with an unspecified USP Class 6‑ certified material (© dual intraperitoneal LHX tags in 49 otariids from 2004 to Markus Horning) 2014 (4 California sea lions and 45 Steller sea lions [43, 46, 49, 54, 55]). For the first two deployments in each species, single tags were used. Subsequently, two tags per animal were used to increase and estimate data return healed upon external, visual examination and palpation, probability. For initial deployments animals were held in and the initial postoperative elevation of blood analytes extended captivity up to eight weeks after surgery prior associated with the inflammatory response had returned to release to allow comprehensive assessments of postop- to pre-surgical levels after five weeks [43, 57, 59]. From erative effects including physiological changes [56–59], these observations, the authors derived a 45-day postop- stress response [60], as well as behavioral indicators of erative survival study inclusion criterion. All 49 otariids pain [61, 62]. Following release, all animals were tracked had survival confirmed beyond the 45-day postoperative via externally attached satellite telemetry transmitters for study inclusion criterion, whether released after one, two periods ranging from one week to four months [57, 63]. or up to eight weeks following surgery [49, 57]. These Following surgery, the study animals exhibited changes in studies also demonstrated that transmitter implantation 2 3 behaviors that are indicative of discomfort or pain [43]. has no detectable effect on postrelease movement and The proportion of time spent standing and in a back arch diving behavior as compared to animals that also under- increased, and the proportion of time spent lying on the went temporary captivity but without LHX tag implants ventral side where the incision was located decreased. [57]. Captivity may have a small but detectable, short- Peak changes occurred for days 1–3 after surgery, and term (2 weeks) effect on postrelease diving behavior in changes diminished but remained above pre-surgical lev- comparison to wild animals that did not undergo tempo- els at days 10–12. The proportion of time spent in loco - rary captivity [63]. Long-term survival beyond the attach- motion decreased for days 1–3, but was at pre-surgery ment of external transmitters was compared between levels for days 10–12 [61]. Surgical wounds appeared implanted animals and non-implanted controls that did not undergo captivity, based on a mark-resight study design using hot-iron branding. No differences in sur - vival patterns between implanted animals and non- Defined here as a non-nociceptive allostatic load potentially affecting well- implanted controls were detectable between the ages of being (e.g., dyspepsia—including nausea and dysmotility, tachycardia, hypo- or hypertension, hypo- or hyperthermia, hyperventilation). 14  months to five years [65]. From the ratio of dual- to Defined as an unpleasant sensory and emotional experience associated single-tag data returns in 20 mortalities detected to date with actual or potential tissue damage or described in terms of such dam- (through 2016) and in 10 dual-tag carcass simulations, age [64]. Horning et al. Anim Biotelemetry (2017) 5:13 Page 5 of 15 data return probability was estimated at >0.98 [49]. Of the 17 female Steller sea lions in that study implanted with single (n = 1 animal) or dual tags (n = 16 animals) between 2005 and 2014, eight animals have died by pre- dation [49], and nine remain alive. Of these, only three have reached a reproductive age. The first female implanted with a single LHX tag in 2005 at the age of 1.4 years was confirmed with a suckling juvenile in 2013 at age nine (see Fig. 2) and with a suckling pup in 2015 at age 11 (L. Jemison, ADFG pers. comm.). The second old - est female was implanted with dual LHX tags in 2008 at the age of 1.8 years, and a live birth was confirmed via a remote video observation system in the region in 2013, at Fig. 3 Lateral abdominal radiograph of a 125‑ day‑ old female harbor the age of seven years (J. Maniscalco, pers. comm). The seal with a body mass of 30.7 kg showing a second‑ generation LHX2 animal was resighted as recently as June 2016, but the tag. The tag was implanted 79 days earlier, at a body mass of 12.4 kg reproductive status could not be ascertained at that time. as described in Horning et al. [53] (© Vancouver Aquarium, DFO permit, Vanc. Aq. ACC no. 2012–06) The third oldest female was last sighted in 2016 at the age of seven and not associated with a pup at that time. In 2014, Horning et  al. [53] abdominally implanted In September of 2016, Horning, Boveng and collabo- single second-generation LHX2 tags into three recently rators implanted dual second-generation intraperito- rehabilitated harbor seal pups (Fig.  3). All three animals neal LHX2 tags into 10 subadult and adult wild harbor exhibited the expected inflammatory response but recov - seals in the Aleutian Islands (Horning et  al. unpubl. ered well. Wound healing and the acute phase of the data, Fig.  4). The animals underwent implant surgery inflammatory response were resolved by six weeks after within 2–4 h of capture and were released 2–3 h after surgery. After that time, all blood analytes were within recovering from anesthesia. Surgeries were conducted ranges observed in non-implanted animals [53]. Survival as described in Horning et  al. [53], within a portable was confirmed, and all three animals tracked for about surgical container setup on the back deck of the 33-m one year after release through external satellite transmit- research support vessel R/V Norseman. All ten ani- ters [53]. mals also received two external satellite transmitters for postrelease studies of movement and dive behavior. All ten animals were successfully tracked for a mini- mum of 60  days after release, and this tracking effort is continuing (Boveng et  al. unpubl. data). These ten ani - mals represent the first instance of at-sea intra-abdom - inal implantation surgeries with same-day release, in a pinniped. Best practice recommendations In the absence of specific guidelines, researchers have relied primarily on select studies in justifying experimen- tal and device designs. Here we propose 15 specific rec - ommendations to guide investigators and regulators in preparing and reviewing applications of fully implanted tags (FITs) in pinnipeds, based on our collective experi- ence over the past decades. Due to their very small size, Fig. 2 Adult female Steller sea lion marked with brand = 908. This extensive use and wide acceptance in veterinary practice, female received a single first ‑ generation LHX implant on September we specifically exclude passive devices (PIT tags) from 27, 2005, and was released on November 22, 2005. The female was approximately 1.4 years old when released. This image with the these considerations. Our recommendations are not female nursing her yearling offspring was taken on July 13, 2013, with societal guidelines and should supplement rather than the female just over nine years old. The female was confirmed with supersede many previously published recommendations a newborn pup in 2015 at the age of 11 years and last resighted in on animal research, capture, handling, sampling, captiv- 2016 at the age of 12 years (© AK Dept. of Fish & Game, photographer ity and telemetry [8, 12, 13]. Betsy Van Burgh, pursuant to NMFS permit no. 14325) Horning et al. Anim Biotelemetry (2017) 5:13 Page 6 of 15 for many vital rate studies in the Gulf of Alaska [66–68], but these approaches have not been techni- cally viable for more remote locations in the Aleutian Islands. FITs such as LHX tags have the potential to provide data that cannot be collected by any other means in remote locations or at sea, such as exact dates, locations and causes of mortality—including predation events—or parturition events. Justifications and alternatives should also be consid - ered within the framework of the Three R’s: Reduc- tion, Refinement, Replacement [12, 69]. Reduction is often understood as the use of a smaller sample size; however, this can also be achieved by the more reliable collection of more or higher resolution data per subject [70]. Refinement refers to improve - ments in the way experiments are carried out that result in reductions of negative effects on animals or improved animal welfare. For example, implanted tags have the potential to reduce or eliminate drag- Fig. 4 Abdominal implantation surgery is being conducted under related energetic costs associated with external tags, standard, aseptic procedures utilizing sterile instruments, surgical which may be considered a refinement [13, 29]. This garb and isoflurane gas for general anesthesia. A harbor seal is placed potential refinement needs to be balanced against on an insulated, elevated table in dorsal recumbency and the surgical area covered in a sterile, fenestrated drape. Positive pressure mechan‑ the impact of surgery. An important consideration ical ventilation is used in a partial rebreathing circuit. The portable is the anticipated duration of deployments in view surgical unit is heated. The surgical team consists of a veterinary of the cumulative effects on energy budgets in rela - surgeon, a sterile assistant and a non‑sterile anesthetist (© Markus tion to progressively waning impacts of surgery. Inci- Horning, pursuant to NMFS permit no. 19309, AUP A/NW2016‑1) dental disturbance effects may be greater for mark- resight designs that may require substantially larger sample sizes and multiple physical site visits to deter- 1. The use of FITs should be justified for specific mine re-encounter rates, as compared to known- experimental designs in view of potential alter- fate sampling designs with spatially and temporally natives and importance of data unrestricted telemetric re-encounter efforts, such as LHX tags. Known-fate sampling designs could be This justification needs to consider the mode, time considered a reduction (in sample size) and a refine - frame and likelihood of data recovery, as well as the ment (reduced disturbance). Replacement avoids the experimental design and sample size. Alternatives use of animals altogether. Recognized techniques to consider may include: mark re-encounter studies for replacement include the use of already collected based on temporary, permanent or natural markings; data. This could be facilitated through the telem - direct or remote observations of individual behav- etric collection of high-resolution, high-density data ior and reproductive status; cross-sectional popula- sets that may lead to enhanced opportunities to use tion counts; the use of externally attached telemetry computer models to simulate animal responses to devices; genetic studies; as well as other approaches. situations or the environment. Thus, there is a direct Valid justifications may include: essential data can - relationship between the quality of data obtained in a not be collected by any other means; or the predicted study and the potential for future replacement. data recovery probability with sufficient statistical power, spatiotemporal resolution or sensitivity is too Experimental designs should consider the a priori low for any alternative; or the alternatives are likely establishment of animal selection criteria. Some cri- to result in greater impacts on individuals or greater teria may be linked to the experimental design such disturbances on larger groups. as sex, age or size and reproductive status. When the selection is not critical to the sampling design (i.e., As an example, video observations combined with differences in health status, size, age or other cri - permanent markings have been successfully used teria are not the focus of the study), animals with Horning et al. Anim Biotelemetry (2017) 5:13 Page 7 of 15 lower risk of complications or those likely to have implants in beavers [74]. Other possible complica- a lower population level impact, could be selected tions include obstruction of other tubular abdominal (e.g., larger or older animals, males). The inclusion structures, such as the reproductive tract, pancre- or exclusion of animals as a function of their health atic ducts or ureters. Device pressure can result in status (e.g., body condition, injuries) is an impor- occlusion of vascular, nervous or lymphatic supply of tant ethical consideration and can also increase abdominal structures and potential tissue necrosis. data return probability and enhance data quality. Early studies using free-floating implants in mam - However, use of such criteria may introduce biases mals ranging in size from deer mice to brown bears in estimates (e.g., behavior or survival) that may or have reported fewer mortalities than those using may not be correctable if the interest lies in under- devices not designed to remain free-floating, and all standing the entire population. Finally, it should be concluded that the former was the preferred tech- pointed out that cost savings alone are generally not nique, generating fewer potentially critical compli- considered an acceptable justification for the use of cations (e.g., dehiscence, hemorrhaging, bacteremia FITs [13]. and sepsis) than a subcutaneous application [72, 2. Consider the most suitable locations for FITs and 75–77]. In pinnipeds, studies have reported compli- device fixation cations from subcutaneous devices [50–52]. How- In pinnipeds, FITs have been placed in subcutaneous ever, no complications attributable to properly con- locations [41, 50] and intraperitoneally [43, 53]. The ducted intra-abdominal placement of sterilized FITs latter may be considered more invasive, and compli- have been reported in literature, or encountered in cations such as dehiscence and infections may lead our studies, suggesting this method as preferable to to severe consequences, and even death. However, subcutaneous implantation [33, 37–40, 42, 45, 47, 49, the subcutaneous blubber layer in aquatic mammals, 53]. and especially in phocids, is a highly vascularized 3. Validate safe designs for FITs and metabolically very active tissue [71]. This may We recommend that safe device designs be vali- result in a substantially greater likelihood of compli- dated through the empirically confirmed absence cations ranging from tissue reaction and inflamma - of detectable effects beyond an initial, time-limited tory response to infection and extrusion (e.g., [41, and expected response, for animals of comparable 50, 72]). Devices placed within or underneath blub- body shape, size, behavior, physiology and life his- ber are somewhat fixed by the requirement to cre - tory. There is a clear need to separately consider each ate a space to accommodate the tag. Intraperitoneal species and life history stage rather than developing devices however can be surgically fixed or remain a single rule that fits all [8]. This applies to the selec - free-floating in the abdominal cavity. Some research - tion of effect parameters monitored as well as the ers prefer to promote connective tissue growth and size and shape of FITs [9]. The expected responses adhesion, in part to facilitate recovery of implanted to implant surgery that have to be considered at devices [73], or to reduce likelihood of interfering the very least include a foreign body response and a with pregnancies and parturition. However, recov- wound healing response. Monitoring parameters to ery of implanted devices has been feasible with free- consider include any that could be indicative of these floating implants in sea otters [40, 47]. two responses, examples include CBC including The potential for complications in free-floating total white blood cell count and differentials, clini - devices should be considered: devices may become cal chemistry values (e.g., total protein, globulins), attached to the mesentery or omentum, may enter acute-phase protein levels (e.g., fibrinogen, hapto - the omental bursa or may become lodged across the globin), as well as visual tracking of incision site heal- pelvic canal. Attachment may occur if the external ing. We further propose that device volume, mass, surface of tags is coated with a material that allows density or buoyancy and cross-sectional area all be or promotes adhesion, development of scar tis- considered and reported in validating safe designs. sue and fibrous encapsulation. Entrapment may Traditionally, mass thresholds have been sug- occur depending on the size, shape and mass of a gested but also criticized [8]. From the early days of device, in relation to the size of the bursa or the pel- implantable telemetry, recommendations were made vic canal. Adhesion or entrapment may secondarily for the mass of implanted telemetry devices not to result in obstructed or torsed intestines, depending exceed 2–5% of animal body mass [78–80], though on the size, shape and mass of the device. Adhesion these were not based on any quantitative assessment has been reported as responsible for some of the of effects of implants of various sizes on behavior and very few observed complications in intraperitoneal survival. Indeed, some references to largely anecdo- Horning et al. Anim Biotelemetry (2017) 5:13 Page 8 of 15 Table 1 Recommended descriptive device parameters, shown here for select tags used in recent marine mammal studies (see Table 2) a b c d e f Device Volume Mass Area Length Force (static, Force (dynamic) Pressure Pressure 2 −2 (ml) (g) (cm ) (mm) submerged) at a = 9.8 ms (static) (N/ (dynamic) 2 −2 (N) (N) mm ) at a = 9.8 ms (N/mm ) LHX1 202 118 13.85 128 −0.87 1.16 6.28 8.38 LHX2 79 54 8.55 97 −0.26 0.53 3.04 6.20 VHF 119 150 13.37 90 0.27 1.47 2.02 10.99 TDR 17 35 2.3 69 0.18 0.34 7.83 14.78 Effect Body mass Cost of Entrapment Entrapment Cost of Cost of locomotion Tissue effects Tissue effects set point locomotion locomotion Smallest cross-sectional area Longest exterior dimension −2 Force is calculated for subjects fully submerged in saltwater (density 1.025) as F(N) =[volume (ml) × 1.025 − mass (g)]× 9.8067 (ms )/1000; a negative value indicates the device is buoyant d −2 This corresponds to the inertial force resulting from the tag mass being exposed to an acceleration a and is calculated as F(N) = m (kg) × a (ms ). For −2 a = g = 9.8067 ms , the force is also equal to the tag weight in air at sea level e,f This is a measure of the maximum pressure the tag exerts on surrounding tissue, and is calculated as force per unit area. Static pressure is exerted by the buoyancy in a non-moving submerged animal, and dynamic pressure is resulting from dynamic acceleration of the animal and varies with a. For a = g, this equals the pressure exerted by a tag in a non-moving, non-submerged animal tal suggestions of size limits are based on completely of tag entrapment in the omental bursa, mesentery arbitrary considerations such as the typical size or or the pelvic canal. Intestinal torsion secondary to mass of mature eggs or fetus at the end of gestation omental entrapment or adhesion may be a function (see [13]). Device mass is likely related to increased of the inertial or rotational forces an adhered device cost of locomotion, especially for birds [81, 82]. Para- can generate for a given acceleration. Localized tis- doxically, some larger birds may be more affected by sue effects may also be a function of the amount identical mass percentages than smaller birds ([81], of pressure a tag can exert on surrounding tissue. and see [8]). Furthermore, device volume may be Though a simplification, these effects can be stand - more closely related to altered body mass set points ardized for comparative purposes via area-specific in some animals [83], and buoyancy may affect cost force (pressure), which may be approximated from of locomotion more than mass [84, 85]. Several device mass and shape. researchers have suggested that implant size indi- Table 1 lists the parameters we recommend as com- ces based on the percentage device weight in water parative device descriptors, for a number of tags or volume to body mass ratios should be preferable used in recent studies. All standardized, compara- for aquatic vertebrates [13, 17, 19, 31, 32]. Beaulieu tive static and dynamic forces and pressures can be et al. [32] specifically suggested using device volume calculated from volume, mass and area, and only the per body mass (ml/kg) as a metric. They compared first four parameters need to be included in publi - results from their own study to eight other stud- cations. It should be noted that dynamic values are ies on aquatic birds (mostly penguins). Their own of course dependent on animal movement. Values ratios were approximately 4.5  ml/kg. Two studies listed in Table 1 are based on a standard acceleration −2 with comparably larger devices reported no effects of 1  g (9.8  ms ) solely for comparative purposes. on common eider (6.5  ml/kg) and harlequin ducks Quick acceleration or turns could result in much (7.5 ml/kg), though they cite the study by Culik and higher values. Wilson [28] as reporting effects at a mean ratio of Volume effects (on body mass set point) and mass 1.8 ml/kg (but note the above-mentioned electrodes, effects (on cost of locomotion) are likely relative to and anchored devices in the two bird studies). These host size, and thus species-specific demonstrated divergent results further support the notion that for safe ratios expressed in proportion to body mass aquatic animals as well as other taxa, one size rule seem reasonable. Safe ratios for four aquatic mam- does not necessarily fit all. mals in which devices from Table  1 have been vali- Physical dimensions including length and the small- dated at least partially through the absence of nega- est cross-sectional area may relate to the likelihood tive effects, are shown in Table 2. Horning et al. Anim Biotelemetry (2017) 5:13 Page 9 of 15 Table 2 Tag volumes and  mass relative to  body mass from  select recent studies in  four aquatic mammal species using intra‑abdominal dual FITs Species Tags n ml/kg % Body mass Eec ff t testing References California sea lion LHX 2 2.2 (3.1) 0.13 (0.18) 1,2,5,6 [43] California sea lion LHX + LHX 2 2.4 (2.9) 0.14 (0.17) 1,2,5,6 [43] Steller sea lion LHX 2 1.8 (1.9) 0.10 (0.11) 1,2,3,4,5,6,7,8 [43, 46, 49, 57, 60, 63, 65] Steller sea lion LHX + LHX 34 3.1 (5.5) 0.18 (0.32) 1,2,3,4,5,6,7,8,10 [43, 46, 49, 57, 59–65] Steller sea lion LHX + LHX2 9 2.8 (3.8) 0.17 (0.23) 1,2,3,4,5,6,7,8,9,10 [49, 59–65] Harbor seal (pup) LHX2 3 6.0 (6.3) 0.41 (0.43) 1,2,3,4,5,6,7,8,10 [53] Harbor seal LHX2 + LHX2 10 2.5 (3.6) 0.17 (0.24) 6,7,8,9,10 [Horning et al. unpubl. data] Sea otter VHF + TDR 31 5.0 (7.1) 0.68 (0.97) n/a [40, 47] For applications with multiple internal tags, volumes and masses are summed. n refers to sample sizes in referenced studies. Mean values are listed with maximum ratios in parentheses, and sample size is indicated. Effect testing conducted in these studies—some continuing—is indicated with references to publications Effect testing 1. captive postop monitoring ≥6 weeks, mass (gain), appetence, 2. postoperative transmitted temperatures, 3. CBC and differential, 4. acute and chronic inflammatory responses measures, 5. captive behavior, 6. postrelease movement, 7. postrelease behavior, 8. postrelease survival, 9. postrelease reproduction, 10. in progress/continuing The effects of forces that tags can exert to raise the and foreign body giant cell growth, which may also cost of locomotion and that may contribute to intes- reduce delays in wound healing. The type of material tinal torsion, and also the effects of pressure on sur - used (polymeric, ceramic, metallic) is not connected rounding tissues (see Table  1) are directly driven by to biocompatibility, but passivating the material sur- physical properties of the tag and are independent face to minimize non-specific protein interaction from the size of their host. The above considerations may be key [89]. also suggest that smaller is not necessarily always We strongly recommend to only use devices with better, and that safe volume and mass ratios should outer materials that have been tested and approved not be interpreted as thresholds. Values below tested either under the United States Pharmacopeia (USP) ratios may only be considered safe in conjunction Class 6 standard for biological reactivity or preferen- with an evaluation of static and dynamic forces and tially the newer ISO-10993 standard for biocompati- pressures. Published ratios and force values should bility [90]. Alternatively, investigators could consider be useful in comparing and optimizing tag designs, conducting assessments similar to those allowed and informing experimental designs, but do not under the ISO standard. The USP standard investi - eliminate the need to conduct impact assessments. gates biological reactivity of elastomers, plastics and Priority should be given to validating and reporting polymeric materials in vitro and in vivo. Under Class safe designs. 6, these standardized tests are conducted on mate- 4. Use devices with an outer material tested for rials in non-polymerized and cured states: acute biological reactivity or conduct biocompatibility system toxicity test, intracutaneous test and implan- testing with actual FITs tation test. Certified cured compounds must fur - As a general rule, the materials encasing or leach- thermore meet strict requirements on leachates. The ing out of an FIT have the potential to evoke a for- duration of implantation test is however very limited eign body response [86]. Foreign body reactions to five  days. Certification of coatings and materials to implanted objects vary in severity and may lead to the USP standard does not prove favorable bio- to phagocytic attacks, fibrous encapsulations and compatibility of devices. However, the use of USP- chronic inflammation, as well as many other acute, certified materials is more likely to result in favorable medium- and long-term effects [86]. Very few stud - biocompatibility results. ISO-10993 addresses bio- ies have investigated long-term histochemical effects compatibility and moves well beyond the USP cer- of FITs on wild animals. A number of studies have tification by considering cytotoxicity, sensitization, identified persistent pathological reactions attribut - acute systemic toxicity, chronic toxicity, subchronic able to FITs, ranging from organ-invading granula- toxicity, genotoxicity, hemocompatibility, throm- tion in wild carp [87] to peritoneal sarcomatosis in bogenicity, pyrogenicity, carcinogenicity as well as laboratory rats [88]. Surface coating FITs with bio- reproductive and developmental toxicity and bio- compatible materials is one way to minimize inflam - degradation. Using devices coated with an ISO- matory response and reduce macrophage adhesion 10993-certified material is one option for investiga - Horning et al. Anim Biotelemetry (2017) 5:13 Page 10 of 15 tors. However, under ISO-10993-6, an in  vivo study to limit current and temperature (such as ther- of the FIT may replace some of the above-listed mal fuses). Multi-cell systems need to be protected in vitro tests of constituent materials if the study was against imbalanced discharge of cells. Complete dis- designed for this purpose, with appropriate assess- charge of lithium primary cells can be problematic, ment endpoints, and all recommended scientific and needs to be managed by device electronics, or principles were applied. Appropriate assessments tested. may include laparoscopic or histological screening 7. Properly sterilize all FITs for inflammatory response. Recommended durations Like any vertebrate, pinnipeds are susceptible to for in vivo implant testing range from 12 to 78 weeks. infections from contaminated FITs, and full steri- Durations for testing constituent components and lization is therefore absolutely essential. Steriliza- materials can be shorter, from 8 to 12 weeks [90]. In tion requires the complete removal or destruction addition to device descriptors listed in Table  1, all of all pathogens including microorganisms, spores studies should always include details on the type of and virus from the FIT and is distinct from disin- material coating all FITs used, and how biocompat- fection. Dipping FITs in disinfectant solutions, such ibility was determined. as any alcohol or chlorhexidine, does not result in 5. Use devices that meet pressure ratings with a 3× sterilization and is therefore not acceptable for any margin of safety for the species of interest FIT applications. There are liquid sterilants such as Damage to an FIT deployed in a diving animal glutaraldehyde that can be used only if the required from excessive pressurization is likely to have cata- concentrations, temperatures and immersion dura- strophic and potentially fatal consequences for the tions (often on the order of hours) are strictly host, especially for FITs containing hollow spaces maintained. Gas sterilization by ethylene oxide or or lithium batteries. Yet, no safety ratings exist for hydrogen peroxide plasma is effective and has the such applications. There are two aspects to con - advantage of allowing prepackaging of FITs for easy sider: uncertainty about the likely maximum depth transport and field use after sterilization. All meth - exposure and engineering design rules for fatigue ods may have advantages and disadvantages, such and manufacturing tolerances. We propose the fol- as toxicity of agents, the requirement of specialized lowing safety factors. With standard deviations for equipment, presence of residue and chemical or the maximum dive depths reported for most spe- thermodynamic interactions with FITs. It is essen- cies averaging about 25% [91], the mean of reported tial that sterilization is fully maintained until and maxima plus 4× the standard deviation is likely to during FIT insertion, and that any sterilizing agents contain 99.999% of cases, suggesting a safety factor are properly outgassed and any residue rinsed off via of 2× mean of reported maximum depths. Deep sterile saline prior to insertion. Any FIT with possi- ocean high-pressure manufacturing industry uses a bly compromised sterility should not be used. For a design rule safety factor of 1.5× [92, 93]. Together, review, see [10, 13, 95]. these yield a 3× safety factor for FIT pressure rat- 8. Use accepted, standardized aseptic surgery pro- ings. Data from adults should be used for FITs likely cedures to remain implanted into adulthood. For sexu- For the same reasons described under recommen- ally dimorphic species, data from the targeted sex dation 7, following standard aseptic procedures is should be used. To give an example, if the mean of all essential. This includes use of a clean environment maximum dive depths reported for adults of a spe- and sterile equipment including drapes, surgical cies is 350 m ± 25% SD, then a rating of 700 m will garbs, gloves and instruments. The skin incision site likely not be exceeded by more than 1 in 1000 indi- should be properly prepared using aseptic technique viduals. Applying the engineering factor of 1.5× will and isolated by sterile drapes. See [10, 13, 29]. then lead to a pressure rating design requirement of 9. Use appropriate anesthesia and analgesia 1050 m for FITs used in this project. The surgical implantation of an FIT without a surgi - 6. Use approved designs for lithium primary cells in cal plane of anesthesia is an inhumane act and should FITs not be performed. Subjects should be appropriately Most FITs use lithium primary batteries as a result monitored during procedures and recovery. Mod- of their high energy density. Such cells are safe to use ern, multi-modal peri- and postoperative analgesia for biomedical implants and FITs, providing stand- should always be used to mitigate pain [13, 95–97]. ard safety measures are implemented [94]. These Proper pain management will likely prevent delayed include using only cells with a lithium metal content recovery and improve the outcomes of projects using less than 1  g per cell and with protective measures FITs. Horning et al. Anim Biotelemetry (2017) 5:13 Page 11 of 15 10. Surgeries, anesthesia and postoperative monitor- include discomfort and pain, as well as reduced ing should be conducted or directly supervised by appetence, mobility or vigilance. Assessments qualified and appropriately trained personnel may include physiology (temperature, stress hor- Personnel should also be knowledgeable and experi- mones, blood metabolites), behavior and move- enced in medical and surgical care of subject species ment (posture, resting), and changes in food including emergency treatment. intake, and could take advantage of data from 11. Consider the advantages and disadvantages of the FITs (e.g., body core temperatures, data from prophylactic treatment with antibiotics, within accelerometers) (e.g., [53, 59–62]). regulatory constraints b) Medium-term effects ranging from days to The prophylactic application of antibiotics has been months proposed and practiced but is not without contro- These effects are critical in determining possible versy, in part as a result of increased incidence of impacts on data. Until demonstrated otherwise, pathogens resistant to antibiotics (e.g., [98, 99]). A it is necessary to assume that for a given period determination for use of prophylactic antibiotics after surgery and until all healing processes are should be made based on a number of factors includ- completed, implanted subjects may experience ing the nature of the procedure, technique used, impaired movement, performance or foraging facilities available, potential surgical complications, ability. postsurgical release site and anticipated behavior Two recent FIT studies revealed measurable of the animal. Considerations should include use of physiological responses linked to inflamma - antimicrobial suture material. Because pinnipeds tory processes that persisted through at least may be legally harvested in some localities, regula- five weeks after surgery [53, 57]. Such assess- tory constraints related to food animals may also ments may initially require captive work under apply. See [13, 29, 95]. controlled conditions for the purpose of devel- 12. Plan, conduct and report on assessment of short-, oping a study inclusion criterion (see recom- medium- and long-term FIT effects mendation #13). Alternatively, a controlled effort As researchers using FITs, we have to consider any in captivity could identify suitable proxies to possible effects of devices or associated procedures derive a study inclusion criterion after release, on the data to be collected and on the study subjects especially given the desirability of minimizing [8–10, 13, 29, 95]. The former is an absolutely essen - captivity (see recommendation #14), and since tial component of the scientific process. The latter captivity may also lead to effects. Assessments derives from the application of accepted principles for medium-term effects may include monitor - of ethical treatment of research subjects. Ethical ing of inflammatory response, analysis of activ - considerations also dictate that the determination of ity patterns and effects on growth, foraging FIT impacts be extended at least through the likely behavior, reproductive behavior, movement and period of device retention and not just through the migration. Data from internal or external tags period of collection of data from FITs. Some pro- may prove useful, providing the devices will not jects have successfully carried out the deployment affect the assessment (e.g., [53, 57, 60, 63]). and subsequent recovery of FITs in wild aquatic c) Long-term effects ranging from months to mammals [40, 47, 48]. However, the majority of FITs years and through the likely period of FIT deployed on wild animals will never be recovered retention [49–52] and will therefore be carried by the host ani- Understanding and quantifying long-term mal for the remainder of their lives. As a result, we effects is crucial to any vital rate studies. Fur - should consider three broad time periods when plan- thermore, some effects may have low-level accu - ning and conducting studies of FIT effects: mulating impacts that may become more detect- able when integrated over longer periods of time [11, 100]. While short- and medium-term effects a) Short-term effects ranging from hours to may be studied at the level of proximate mecha- days nisms, long-term effects can more readily be assessed via ultimate impacts on growth, migra- Detecting and understanding short-term effects tion, reproduction and survival (e.g., [65]). may be critical to determining how quickly after It is inappropriate to assume that FITs will not a procedure animals may be safely released and affect data or subjects simply based on size or to improving procedures and mitigating effects. mass percentages (see recommendation #3) or Examples of possible short-term effects may Horning et al. Anim Biotelemetry (2017) 5:13 Page 12 of 15 based on demonstrated absence of effects in ‘Carefully consider the duration of postsurgery cap- other species carrying similar devices. Evidence tivity.’ In connection with FIT implantation surgery, supports that effect magnitudes are specific to project planners should therefore weigh any poten- species, devices, animal state and circumstances tial benefits of controlled access and monitoring and [8]. Transferability of such findings across spe - potential disadvantages of stress and delayed return cies and devices is therefore limited, and it is to the natural environment when under temporary prudent to always carry out and report control captivity. Amount and lengths of manipulations studies [8, 9]. as well as duration of temporary captivity for wild Implanted tags may also passively or actively animals before and after surgery should be limited increase the detectability of hosts by predators. as much as possible [8, 101, 102]. However, captive Some tags may be echogenic and may produce monitoring is an extremely valuable experimental acoustic or electromagnetic signatures. Acous- tool and can lead to refinements in considering post - tic emissions could also be perceived by hosts operative recovery and monitoring periods through and may alter their behaviors. Where possi- detailed studies of discomfort and pain, wound heal- ble, researchers should consider using FITs and ing, observations of postoperative complications or external tags to provide assessment data. Recent confirmation of their absence and observations of developments enable life-long FITs to provide postoperative behaviors. survival and reproductive data, and develop- 15. Report all findings in accessible, peer-reviewed ments to enable electronic mark-resight designs literature using FITs are underway (e.g., [6]). If FITs are It is imperative that all findings, including nega - used to collect vital rate or assessment data, then tive effects, are reported in readily accessible peer- the failure rate of tags or data recovery prob- reviewed literature. This includes details on safe ability needs to be accurately quantified and FIT designs, surface materials and biocompatibility, corrected for [46, 49]. Even outside of vital rate study inclusion criteria, results from all effect assess - studies, data on tag failure rates will be useful in ments, as well as tag failure rates and data recovery planning future telemetry studies. The simulta - probabilities. The latter are essential for sample size neous deployment of multiple internal or exter- estimation and the development of future projects. nal tags may be a powerful tool in support of long-term vital rate and FIT assessment studies. Conclusions However, with increasing manipulations and tag We present 15 specific best practice recommenda - burdens proper assessments on combined loads tions for the application of fully implanted telemetry will become even more critical. devices in pinnipeds. These recommendations should 13. Derive and apply a specific study inclusion crite - be considered by researchers preparing projects and rion by regulatory bodies authorizing projects. These initial Many FIT studies referenced here were designed to recommendations may be refined or adjusted through collect primary data within days of surgery, when new studies, within the guiding principles of the Three the presence of effects from surgery and devices has R’s [69]. Deviations or exceptions should be considered to be assumed. Very few of these studies specifically only when convincingly justified. While we developed derived and reported a study inclusion criterion these recommendations specifically for pinnipeds, some (see also [5, 9]). An arbitrary cutoff not backed by may be applicable to other groups of aquatic animals, applicable data does not support the absence of FIT such as sea otters or aquatic birds, or other applica- effects in the data set and is no better than not using tions, such as partially implanted (transdermal) tags, or a criterion. Without a specific, quantitative criterion even external tags. For all users and regulators of FITs, backed by demonstrated absence of effects or a valid it will be important to avoid creating a ‘catch 22’ situ- argument about transferability of inclusion criteria, ation, where studies are not allowed to proceed or be reported findings lack scientific validity. published until the absence of negative effects has been 14. Minimize manipulations and temporary captiv- demonstrated. Such determinations cannot be carried ity out without risking these effects and will require sam - The report by the Joint Working Group on Refine - ple sizes that cannot usually be achieved through single ment [13] recognizes that ‘wild animals are liable studies. A prudent approach may therefore gradually to find capture and handling extremely stressful build on initial control and validation studies, while and that this represents an experimental harm.’ The providing plans to carry out effect assessments at all working group report specifically recommends to appropriate temporal scales. Horning et al. Anim Biotelemetry (2017) 5:13 Page 13 of 15 Abbreviations 9. Walker KA, Trites AW, Haulena M, Weary DM. A review of the effects of CBC: complete blood count; FIT: fully implanted tag; LHX: life history transmit‑ different marking and tagging techniques on marine mammals. Wildl ter; VHF: very high frequency. Res. 2012;39:15–30. 10. Mulcahy DM. Legal, ethical, and procedural bases for the use of Authors’ contributions aseptic techniques to implant electronic devices. J Fish Wildl Manag. MHo drafted manuscript and designed referenced FITs, MHa and PAT devel‑ 2013;4:211–9. oped referenced implant surgery protocol, MHo, JEM and MHa designed and 11. Maresh JL, Adachi T, Takahashi A, Naito Y, Crocker DE, Horning M, Wil‑ conducted referenced FIT studies, MHa, PAT, CEG, RKB, KW and SJ conducted liams TM, Costa DP. Summing the strokes: energy economy in northern implant surgeries, MHo, JEM, KAW, CRS, JPS and PLB designed or conducted elephant seals during large‑scale foraging migrations. Mov Ecol. referenced assessment studies. All authors participated in referenced implant 2015;3:22. studies, postoperative monitoring or assessment studies referenced here. All 12. Einstein R, Rowan C, Billing R, Lavidis N. The use of telemetry to refine authors read and approved final manuscript. experimental technique. 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Animal Biotelemetry – Springer Journals

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