Challenges associated with the study of marine megafauna often arise from characteristics of their life histories, which span large spatio-temporal scales in a dynamic seascape [1]. Research on the distribution, behaviour, and eco-physiology of such species at times and in locations that are inaccessible for direct observation has been facilitated, in part, through the development of a broad suite of archival and satellite-linked data loggers [2]. Insights from biotelemetry have been particularly important for the conservation of marine organisms with protected status, such as sea turtles, as the collection of empirical ecological data is essential for successful management and recovery planning [3, 4].
While satellite telemetry has contributed much towards our understanding of the movements and ecology of marine animals like sea turtles, there are still limits on the quantity and quality of data collected and/or relayed, and the lifespan of the associated instruments. Many of these limitations relate to the challenges of deploying electronic equipment in the marine environment; the mass, shape, memory, battery capacity, and sensor resolution of available tags; and the relatively narrow bandwidth through which data must be transmitted via satellite [5]. Furthermore, tags only collect and transmit data for a finite period, during which time they may be dislodged. For tags that are retained until battery power is depleted, release typically occurs through tag and/or tag attachment materials fatiguing or failing (e.g., via UV exposure or corrosion), growth of the study subject, or other factors [5].
In addition to the technical capacity of the available instruments, researchers are ethically bound to consider animal welfare implications associated with using telemetry instrumentation [2, 6]. There may be potential for injury, physical suffering, increased risk of predation, or fitness costs associated with capture, tag attachment, and tag retention; these have been assessed in many taxa (e.g., [7,8,9,10]). For this reason, preference should be given to tags that minimize detrimental impact on study subjects by optimizing the mass, shape, attachment location, and retention time of the instrument [2, 6].
Leatherback sea turtles (Dermochelys coriacea) have been the subject of numerous satellite-tagging studies spanning more than 20 years. In the Northwest Atlantic, this giant (up to 700 kg) marine reptile undertakes long migrations between subtropical and tropical nesting beaches and high-latitude foraging grounds, where it feeds on gelatinous zooplankton prey [11, 12]. The species is listed as endangered across much of its range (e.g., Species at Risk Act, Canada; Endangered Species Act, USA). Leatherbacks differ morphologically and physiologically from other sea turtles, most notably in the structure of their carapace, which is covered by smooth, oily skin [13,14,15,16,17]. As a result, satellite tags cannot be attached to leatherbacks using the fibreglass or epoxy resins that work well on the hard, keratinous scutes of cheloniid sea turtles [1, 13,14,15,16,17]; therefore, alternative methods have been pursued.
Traditionally, there was a focus on using non-invasive, indirect tag attachment methods for tracking leatherback turtles via satellite. Initial work used a custom-fitted harness system, structured like a backpack, to hold a satellite tag in place above the carapace [13, 18]. The first documented use of this approach (circa 1987) on a leatherback departing a nesting beach in French Guiana [19] was criticized, as the transmitter design was bulky and clearly lacked hydrodynamic efficiency [1]. Another nesting leatherback, this time in St. Croix, USVI, was equipped with a harness and transmitter circa 1993 [20]. The turtle was re-encountered nesting 18 days later. Chafing from the harness was observed on the animal, prompting researchers to remove the harness and transmitter [20]. Other early attempts at satellite tracking of leatherback turtles (circa 1996) used large, buoyant tags that were towed on a tether anchored through the caudal tip of the carapace [21]. Modern adaptations of this equipment using alternative tag types continue to be employed to this day [22].
Further refinements to the harness design and miniaturization of satellite tags, including platform terminal transmitters (PTTs) specifically, fuelled a suite of leatherback movement research projects using harness-attached tags (e.g., Fig. 1a), beginning around the year 2000 (e.g., [23,24,25,26,27,28,29]). These studies yielded substantial insights into leatherback movements and behaviour. However, in 2006 and 2008, detailed reports on the condition of two turtles observed nesting with harnesses attached for 635 days and 665 days generated concern about the potential for the harnesses to cause the animals discomfort and injury—including shoulder calluses, scarring, and deformation of the carapace [15, 16]. Fortunately, subsequent encounters with both turtles revealed healing of their injuries once the harnesses were removed [15, 16].
While these cases demonstrated rapid recovery from impacts of harness materials in contact with body parts, concerns about the possibility of physical injury and/or potential fitness costs related to harness hydrodynamic drag remained. This prompted increased interest in exploring the potential of directly attaching satellite tags to the carapace, an approach that had been then used in only a handful of short-term leatherback biotelemetry studies between 1999 and 2007 with limited success [14, 30, 31]. However, the direct attachment method, even at its most refined, is invasive, requiring drilling of the turtle's highly-vascularized cartilaginous carapace. Channels are drilled through the longitudinal carapacial ridges (e.g., Fig. 1b). Wire, ties, or other foreign materials are then laced through the drill channels to secure the instruments. This effectively precludes complete healing for as long as these materials are in place.
Reports of the first long-term deployments of PTT satellite tags directly attached to leatherbacks (2005–2009) included analyses of movements and dive behaviour [17, 25, 32]. They suggested that leatherbacks equipped with directly-attached tags had improved hydrodynamic performance and reduced energetic costs versus those with harness-attached tags. However, these preliminary studies comparing the effectiveness of harnesses versus direct attachment techniques and investigating potential tagging effects were limited to relatively short-term behavioural analyses with relatively small sample sizes (Fossette et al. [17], n = 2 directly attached, n = 3 harnessed; Byrne et al. [32], n = 2 directly attached, n = 6 harnessed; Sherrill-Mix and James [16], n = 0 directly attached, n = 42 harnessed), and did not provide insight into long-term outcomes for tagged turtles.
Direct attachment of satellite tags to leatherbacks is now a mainstream tagging technique. However, to date, there have been no long-term studies of leatherbacks equipped with satellite tags via direct attachment which assess individual survival, nesting success, tag retention, or the condition of the tag attachment site through time. Biologists implementing tagging studies, and particularly those focused on protected species, have a responsibility to ensure not only that such research contributes to the sound management of the species in question, but also that animal welfare concerns are clearly identified and effectively addressed. Thus, an evaluation of both the efficacy of direct carapacial attachment of satellite tags to leatherback turtles and its suitability from an animal welfare perspective is long overdue.
Here we reference the largest dataset of satellite-tagged leatherbacks in the Atlantic. We build upon evidence collected by Sherill-Mix and James [16] to assess and compare potential impacts to, and fates of, turtles subjected to harness or direct attachment tagging methods. All turtles were tagged during directed fieldwork in eastern Canada, a region that hosts one of the largest seasonal foraging populations of leatherbacks in the world [12, 25, 33], comprising turtles from nesting populations throughout South and Central America, southern USA, and the Caribbean [34]. In the present study, we evaluate satellite tag attachment methods, operational lifespan, and retention. We also describe subsequent observations of turtles equipped with satellite tags, including condition of the carapace at the attachment site following long-term tag retention and healing of impacted areas following release or removal of directly-attached tags.