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Technology wish lists and the significance of temperature-sensing wildlife telemetry

Technology wish lists and the significance of temperature-sensing wildlife telemetry Telemetry has revolutionized studies in wildlife biology, ecology, physiology, and conservation. With the increased demand for telemetry, new technology has made great strides to enable long studies in harsh and remote areas on a wide variety of study species. As the climate crisis continues to impact animals, temperature-sensing telemetry has become a helpful technique for understanding the effects of climate change and how to protect wildlife from them. However, temperature-sensing telemetry and telemetry in general still pose technological challenges and accessibil- ity issues for the researchers who use it. Currently available telemetry technology is expensive, too large and heavy for many study species, and cannot measure all variables researchers want to study. These technological improvements have especially been neglected for temperature-sensing telemetry, which may be underutilized given the current climate crisis. To understand why innovation has stalled, and where it should be directed going forward, we gathered opinions from researchers who use telemetry and from manufacturers that create and supply telemetry equipment. Our goal was to broadly describe the current technological landscape, compare it to what we envision for the future, and make suggestions for how to reach that future. Keywords: Company, Innovation, Interview, Manufacturer, Survey, Technology, Telemetry, Temperature, Wildlife tracking Introduction become accessible to more researchers. During the cur- Wildlife studies were originally confined to live animal rent “golden age” of animal biotelemetry, advances in trapping, surveys, and transects that provided snapshot technology are allowing scientists to learn much more ecological and physiological data. Capture–mark–recap- about wild animals, using less invasive, and therefore, ture studies were possible for certain types of animals, more fruitful and relevant methods [1, 2]. but recapturing individuals to study how they change An especially promising advance is temperature-sens- over time remained challenging or impossible for most ing telemetry. Temperature-sensing telemetry (which animals until the advent of telemetry in the mid-1950s. senses temperature) combined with datalogging technol- Since then, advances in telemetry have revolutionized ogy (which records temperature data) in the transmit- studies in wildlife biology, ecology, physiology, and con- ters themselves, in receivers, or in separate dataloggers, servation. The number of publications using telemetry to allows researchers to remotely collect environmental or study animals has skyrocketed in the past 20 years (Fig. 1) body temperature data without spatial or temporal bias as technology continues to improve and as transmitters [3]. As the climate crisis continues to impact animal dis- tributions, movement, health, and interactions, among other factors, temperature-sensing telemetry will be *Correspondence: savannahjweaver@gmail.com pivotal. Altered temperature regimes are and will con- Biological Sciences Department, College of Science and Mathematics, tinue to be the driver of physiological stress and con- California Polytechnic State University, San Luis Obispo, CA 93407-0401, USA straints [4]. Measuring temperature using telemetry Full list of author information is available at the end of the article © The Author(s) 2021. 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The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Weaver et al. Anim Biotelemetry (2021) 9:29 Page 2 of 13 Fig. 1 The number of publications using animal biotelemetry has risen dramatically in the past 20 years. Data are from a Web of Science search conducted on 3 June 2021 for the following terms: wildlife telemetry, wildlife biotelemetry, wildlife tracking, animal telemetry, animal biotelemetry, and animal tracking will help describe changes in environmental tempera- undergone incredible miniaturization and cost reduction, ture and changes in behavior as a response. Ectotherms further improvements could still be made so the tech- have emerged as model organisms to study these effects nology is feasible for a greater suite of animals and more because environmental temperature plays such a direct researchers. Even basic very high-frequency (VHF) radio role in their physiology [4, 5]. These data are essential for telemetry remains out of reach for many researchers conservation efforts because continuous body and envi - with smaller budgets, including many researchers from ronmental temperature data can be used to predict the low-income countries. This amplifies scientific biases by effects of climate change on at-risk populations [6]. Tem - excluding certain researchers from being able to access perature-sensing telemetry can also be used to remotely telemetry equipment, increasing the likelihood of para- collect data on both ectothermic and endothermic ani- chute scientists conducting telemetry and thus perpetu- mals’ activity patterns, from terrestrial surface activity [7] ating problematic colonial science [9–11]. Furthermore, to marine diving behavior [8]. Clearly, temperature rep- scientists studying very small animals still face major resents a key variable for physiology, ecology, and behav- challenges with telemetry due to the tradeoff between ior, thus one might expect temperature-sensing telemetry battery life and transmitter size/weight. Challenges with to be a high priority for researchers and manufacturers. access to telemetry equipment and with the technology However, in our experience, temperature-sensing telem- itself therefore remain, and this commentary serves to etry is underutilized, and its technological advances summarize opinions on these challenges from both the appear to have stalled. While temperature-sensing trans- creators and users of the technology. mitters have enjoyed the same miniaturization as regu- Researchers who use telemetry to study the ecology lar transmitters, temperature datalogging technology in and physiology of a wide variety of animals, including receivers remains largely unchanged since the 1980s. endangered species and the effects of climate change, Additional areas of improvement include technology are greatly impacted by the technology available to them. capabilities, size/weight, and price. In some cases, telem- Many factors impact the design and price of telemetry etry may not be an improvement on capture–mark– transmitters, sensors, receivers, antennas, software, and recapture studies because telemetry devices cannot other equipment. Like all producers and consumers, the measure the variables of interest. Although devices have challenges and constraints faced by companies producing W eaver et al. Anim Biotelemetry (2021) 9:29 Page 3 of 13 telemetry gear and by scientists using it for research are Researcher surveys often different. For example, transmitters may be paired Methods with various sensors [12] that measure and log changes in Throughout November 2020, we distributed an online the animal’s behavior (e.g., by measuring speed or accel- Microsoft Form with a combination of free response, eration), physiology (e.g., muscular activity, sound pro- rank-choice, and Likert scale questions (Additional duction, temperature), or environmental conditions (e.g., file  1). In our survey questions, we used the terminol- dissolved oxygen, altitude). Many of these sensors repre- ogy “temperature-sensitive telemetry”, which we define sent niche equipment that are strongly desired by some the same way as “temperature-sensing telemetry”. We researchers but may not be worthwhile for manufactur- distributed the survey using social media (Twitter, Face- ers to produce en masse. Companies producing telemetry book) and via email to corresponding authors of papers equipment are typically private, for-profit businesses that published in the journal Animal Biotelemetry in the past must balance the price points of their equipment with 2 years and of papers publicized on telemetry company researcher demand and the ever-changing landscape of websites. Of the 84 telemetry users who responded to the research funding. Finally, manufacturers must respond survey, 23% were university faculty (n = 19), 20% were to, and indeed anticipate, the technological needs of postdoctoral researchers (n = 17), 20% were graduate stu- researchers, and in turn researchers are often con- dents pursuing either an MS or PhD (n = 17), 16% were strained by manufacturer investment choices, creating non-academic researchers such as those associated with an intricate dance between tech-users and tech-creators, government or nonprofit organizations (n = 13), and 20% the progress of which may have dire impacts for research responded as “other” (n = 17), with one non-response. on sensitive or endangered species in this current climate We recognize that our survey has distribution and par- crisis and associated mass extinction. ticipation biases. We present this commentary to advocate for what Survey responses were exported to Microsoft Excel telemetry advances could and should be made in the for count data. Respondents could choose more than future. We aim not to describe what is currently possi- one answer choice for each question, so the percentages ble, but what researchers want to be possible. We gath- of respondents choosing a given answer sums to greater ered opinions from researchers who use telemetry and than 100% for most questions. SJW coded written free from manufacturers that create and supply telemetry responses for keywords. We used X tests to determine equipment to broadly describe the current technological whether there was a significant difference in the fre - landscape and to compare it to what we envision for the quency of temperature-sensing telemetry use based on future. Telemetry technology includes Global Positioning study organism (endotherm versus ectotherm and by Systems (GPS), VHF radio, and Argos satellite tracking. clade), study habitat, or device attachment method. The A given telemetry system may consist of various sensors sample sizes vary for each test because respondents may that measure, transmitters that send, and receivers or log- have selected more than one option for a given question. gers that record the data of interest [13]. However, in this For the analysis of study organism, each survey respond- paper, we refer to telemetry broadly because the opinions ent was coded to study either endotherms, ectotherms, discussed apply to all telemetry systems. We surveyed 84 or both (n = 84). For analyses of clade, habitat, and total scientific researchers who use telemetry and interviewed device attachment method, we excluded those research- representatives of 9 companies that design, manufacture, ers who selected more than one clade, study habitat, and sell telemetry equipment. We collected perceptions or attachment method because their incorporation of of telemetry equipment generally, but we also focused temperature may have only been related to one of the specifically on temperature-sensing telemetry to evaluate responses listed (n < 84 for each of these tests). Fig- total whether our perceived lack of user interest and manu- ure  2 shows the full dataset with no exclusions made, so facturer investment is evident, and to pursue reasons for it does not perfectly reflect the X test statistics and per- this. We describe current implementations of temper- centages presented in the results. We used R v4.0.3 [14] ature-sensing telemetry, assert the need for improved and tidyverse workflow [15] to create figures and analyze telemetry technology in general and increased focus on data. The survey and the use of data were approved by temperature-sensing telemetry, and make suggestions the California Polytechnic State University Institutional for how to achieve these key innovations. The informa - Review Board (Project 2020-183). tion presented here will be a resource in the coming years for researchers planning to acquire telemetry equipment Current telemetry applications and organizing new studies, as well as for manufacturers Most of the respondents (56%) reported studying endo- deciding which technological directions may optimize therms, 39% studied ectotherms, and 5% studied both. their investment. The number of study species listed by survey respondents Weaver et al. Anim Biotelemetry (2021) 9:29 Page 4 of 13 Fig. 2 Study organisms, habitats, and transmitter-animal pairing methods. Survey respondents (N = 84) indicated a their study organism(s), b their study organisms’ primary habitat(s), and c the mode(s) of device attachment to their study animals. All vertical axes represent count data totaled 255, although many were not listed to species- of study questions, including animal movement, habitat level. In order of popularity, birds (Aves), mammals use, behaviors, home range, survivorship, activity timing, (Mammalia), reptiles (Reptilia), ray-finned fishes (Actin - sociality, management needs/outcomes, and more (Addi- opterygii), and sharks and rays (Chondrichthyes) were tional file 2). the most common clades of study animals in our sample of researchers using telemetry (Fig.  2a); other telemetry Telemetry wish lists study species included amphibians, insects, and crayfish. Survey respondents were asked to rank their top priori- Terrestrial organisms are the most tracked animals based ties when selecting telemetry equipment, and the charac- on this survey (77% of respondents study them), followed teristics with the most first-choice rankings were weight, by freshwater (25%) and marine (17%, Fig.  2b). Most price, size, variables recorded, and battery life (Fig.  3). respondents (65%) reported that they use external attach- Durability, data storage, and receiver range were also pri- ment methods such as a collar, waistband, backpack, or orities but were comparably less important. similar; 42% reported that they use adhesives such as glue Researchers are only somewhat satisfied with the cur - or tape; 31% reported that they implant devices (Fig. 2c). rently available telemetry equipment they use. Most Researchers reported using telemetry for a wide array survey respondents are unable to measure everything W eaver et al. Anim Biotelemetry (2021) 9:29 Page 5 of 13 Fig. 3 Researchers’ most important telemetry product characteristics. Survey respondents (N = 84) ranked what factors are most important to them when selecting telemetry equipment desired with the equipment they use (Q11, Fig.  4). We telemetry to measure and record, fantasy equipment asked respondents what variables they want to be able refers to any and all telemetry product characteristics. to measure that cannot be measured/recorded by cur- The top ten fantasy equipment characteristics were rently available telemetry equipment (Additional file  1, smaller and lighter transmitters (60%), longer battery life Question 7). We used these responses to create a “wish (54%), more variables measured (52%), lower cost (23%), list” of variables that respondents wished their current more data storage (22%), better durability for rough envi- telemetry devices could measure and transmit/record. ronments, including waterproofing and for use with reck - Some of the additional variables with the highest demand less animals (21%), longer signal range (18%), remote data among survey respondents included assessing movement download ability (17%), higher measurement frequency and behaviors via accelerometry (12%), and measuring/ (13%), and more precise measurements (13%; Addi- recording environmental temperature (6%), heart rate tional file  2). Survey respondents suggested solar power (6%), internal body temperature (5%), and audio and/ to extend battery life and urged that including a battery or video recordings (5%). See Additional file  2 for a full indicator would be immensely helpful. In an ideal world list of variables respondents wished their equipment with no technological constraints, researchers hope for recorded. all these capabilities and more in ever-smaller devices. Respondents reported that their most time-consuming technical difficulties when using telemetry equipment for Temperature‑sensing telemetry studies included equipment running out of battery power 33% of respondents reported that they incorporate prematurely (19%), equipment failing or breaking (18%), either environmental or organismal temperature into issues with data or equipment retrieval (17%), and diffi - their telemetry (Q12, Fig.  4). Respondents who reported cult data formatting (13%; Additional file  2). Conversely, studying ectotherms incorporate temperature into we asked respondents to imagine there were no techno- their telemetry studies significantly more often (57%) logical limits and describe traits of their ideal, “fantasy” than respondents studying endotherms (15%; n = 84, equipment that would meet all of their research needs X = 17.0, df = 2, p < 0.001; Fig.  2a). The frequency of and interests if anything was possible (Additional file  1, temperature-sensing telemetry use was also significantly Question 13). Whereas the variable wish lists described different across study organism clades (n = 70, X = 19.3, above referred to what variables researchers wanted df = 5, p = 0.002; Fig.  2a): 16% of respondents studying Weaver et al. Anim Biotelemetry (2021) 9:29 Page 6 of 13 Fig. 4 Researchers’ opinions on the research application and affordability of current telemetry equipment. Survey respondents (N = 84) indicated their satisfaction with the variables measured by current telemetry equipment, whether or not they use temperature-sensing telemetry, and their opinions on the pricing of telemetry equipment. Questions abbreviated for the figure (e.g., temperature equipment refers to temperature-sensing telemetry equipment); see Additional file 1 for full questions birds incorporate temperature, with 13% for mammals, opinion as strongly (Q16 and Q18, Fig. 4), and may even 56% for reptiles, 20% for ray-finned fishes, 100% for be willing to pay more for better temperature-sensing sharks and rays, and 75% for “other” organisms, which telemetry technology (Q19, Fig. 4). consisted of ectothermic amphibians and invertebrates. Researchers studying marine organisms were most likely Company interviews to incorporate temperature (71%), followed by terrestrial Methods (30%), then freshwater (20%). The frequency of temper - To understand telemetry product development and pre- ature-sensing telemetry use was not significantly differ - dict future advances, we interviewed representatives ent among study animal habitats (n = 67, X = 5.6, df = 2, from companies that manufacture telemetry equipment p = 0.059; Fig.  2b) or major mode of device attachment over the phone or via email correspondence. We com- (n = 53, X = 4.7, df = 2, p = 0.096; Fig. 2c). piled a list of companies to interview that we already For respondents who do not use temperature-sensing knew of or that we found in a basic Google search prior telemetry, 37% said that temperature was unrelated to to distributing the researcher survey. Of the 17 compa- their research questions, 8% said it was unnecessary nies we contacted, 11 responded to our queries, and 9 because there was not sufficient temperature variation to followed through with the interview (Additional file  2): measure in their context, and 5% had never considered Advanced Telemetry Systems, Inc. (ATS; Isanti, Minne- the possibility of including temperature in their telemetry sota, United States), Cellular Tracking Technologies LLC studies. Some researchers may have wanted to include (CTT; Rio Grande, New Jersey, United States), Holo- temperature but were unable to do so due to cost (13%), hil Systems, Ltd. (Carp, Ontario, Canada), Innovasea logistics of product trade-offs and availability (12%), size/ Systems Inc. (Canada; Chile; Norway; United States), weight limitations (10%), and battery lifespan (2%; Fig. 5). mOOvement (Brisbane, Queensland, Australia), Micro- Respondents overall said that the current price of telem- wave Telemetry, Inc. (MTI; Columbia, Maryland, United etry equipment is too high (Q15 and Q17, Fig.  4), but States), TechnoSmart Europe SRL (Guidonia, Rome, temperature-sensing telemetry users do not share this Italy), Vectronic Aerospace Inc. (Coralville, Iowa, United W eaver et al. Anim Biotelemetry (2021) 9:29 Page 7 of 13 Fig. 5 Why researchers do not include temperature. Survey respondents who do not use temperature-sensing telemetry equipment (N = 56) indicated why they do not use it States), and Wildlife Computers, Inc. (Redmond, Wash- engage with researchers, but more companies reported ington, United States). that they rely on unsolicited feedback and casual con- Our aim was not to draw conclusions about the popu- versations with customers to gauge interest in new and larity of companies or to compare their products, but improved products. Approximately half of the com- rather to understand product development and to gauge panies we interviewed said that miniaturization and whether manufacturers’ perception of researchers’ improving reliability are the most important product desires align with the needs reported by survey respond- characteristics to improve, with extending battery life/ ents. We asked manufacturer representatives questions efficiency, improving durability, and lowering price also about their product development and market perception listed by several companies. Although they stated that generally, as well as questions directly related to temper- they are actively working on improving each of these, ature-sensing equipment (Additional file  3). The inter - miniaturization was of primary importance. However, views and the use of data from them were approved by companies feel inconsistent pressure to make these the California Polytechnic State University Institutional improvements. Some companies reported constant Review Board (Project 2020-183), and we received per- demand for new and improved products, while others mission from the interviewees that we could include their reported very little. company’s name and responses in our paper. According to manufacturers, the equipment charac- teristics that researchers desire tend to create trade- offs, where each innovation comes with a drawback. Current product development For example, measuring an additional variable uses Eight of the nine companies we interviewed said that more battery, makes the device larger and heavier, they use customer feedback and requests to determine and/or increases its cost. Additionally, a common sen- what directions to take for product development and timent from companies was that new and improved improvement. Other ways product development may be products are an endless cycle: before manufacturers directed included demand, predicting research trends, can even develop and refine one technology, research - and company goals and interests, each of which were ers have already come up with new research ques- listed by 2–3 companies. Several of the companies we tions that necessitate the development of another new interviewed reported that they rely on conferences to technology. Weaver et al. Anim Biotelemetry (2021) 9:29 Page 8 of 13 Temperature‑sensing telemetry responses, but they maintain reservations about creat- Company representatives reported that between 0 and ing new technology. Researchers can be eager to get new 15% of their customers are interested in incorporating technology on an urgent timeline, but seemingly simple temperature into their equipment, with most estimating innovations can take years to develop into something between 5 and 10%. Since the baseline demand for tem- actually effective. Researchers’ demand for improved perature-sensing telemetry equipment is so low, almost telemetry equipment has already pushed huge techno- all the manufacturers we interviewed reported that their logical advances [1, 2, 24, 25], and based on researcher perceived demand for new and improved temperature- demands and company plans, these improvements will sensing telemetry equipment was essentially nonexist- continue. Equipment manufacturers are indeed working ent. Some companies automatically include temperature hard to meet researchers’ most pressing needs, but the sensors in all products, and others can incorporate tem- technology will always lag behind the new applications perature sensors into any product. These sensors most desired. often record ambient temperature or animal surface body Certain innovations are unlikely because there is not temperature. Some companies also produce surgically enough demand, they would be too difficult to engi - implantable temperature-sensing transmitters that can neer, or the product would not be profitable enough. For yield data on animal core body temperature. For those example, researchers always want to get the same or bet- companies that produce temperature-sensing transmit- ter technology in an ever-smaller package, but there need ters and feel demand for improvement of temperature- to be better batteries available before that will be possi- sensing products specifically, they are currently working ble. Survey respondents had numerous wish list variables to make temperature measurements more precise and that they want telemetry equipment to be able to meas- the transmitters smaller and less expensive, although this ure; however, most variables were only listed by < 5% of applies to few companies. respondents (Additional file  2). The amount of product development necessary to create a niche product for a Technological trade‑offs single project is unlikely to be financially feasible for the After nearly a century of telemetry innovation, there is manufacturer or the user. Many innovations are simply now a wide array of telemetry devices with an even wider not feasible because the number of buyers would be so array of potential applications [1, 2, 12, 16]. Telemetry small. now enables studies on topics such as animal movement Even when certain product characteristics can be and migration [17–19], physiological processes [20, 21], achieved, there is usually an associated downside such as or social interactions [22], and our survey respondents shorter battery life, larger/heavier transmitters, loss of a compiled an even longer list of current applications different sensor, and especially increased product cost. (Additional file  2). However, the survey responses also Survey respondents wrote about having to make deci- show how many research interests still cannot yet be sat- sions based on these trade-offs with sample size, trans - isfactorily investigated using telemetry. mitter size/weight, and battery life. When it comes to Our survey of researchers who use telemetry to study telemetry equipment, there is not a single product that animals and interviews with the manufacturers that pro- will fit the needs of every study. This may be one rea - duce telemetry equipment revealed only partial align- son why researchers reported using such a diverse array ment between supply and demand. For example, both of manufacturers (n = 42, Additional file  2), some of researchers and manufacturers identified transmitter whom specialize in specific technologies. Unfortunately, miniaturization as a top priority. However, one over- it seems researchers are often unable to find the right looked issue brought up in the survey responses, and in company for a product that will most closely match their a recent review paper focusing on satellite telemetry [23], needs, as most of the respondents’ desired wish list vari- was difficult data formatting. This was the only issue that ables have been recorded using biotelemetry [2]. To navi- did not seem to be on any company’s radar in our inter- gate the vast array of telemetry manufacturers, products, views. An inability to understand data structure and ana- and applications, several reviews and guides are informa- lyze it could be a barrier to researchers wishing to begin tive [12, 16, 23, 26]. using telemetry or simply looking to switch telemetry manufacturers. A universal telemetry data structure, per- Financial obstacles haps agreed upon by a coalition of company representa- Telemetry, along with much scientific research, is gener - tives and data scientists, could go a long way to inspire ally dominated by well-funded projects and universities new telemetry users and applications. in wealthy nations. The cost of telemetry devices limits Overall, companies recognize most of the wish list vari- the number of variables that can be measured, animals ables and fantasy equipment traits compiled in the survey that can be tracked, and researchers who can use it. Even W eaver et al. Anim Biotelemetry (2021) 9:29 Page 9 of 13 if product costs were to fall, accessibility is likely to con- box? This could extend study lifetimes indefinitely with - tinue to be stratified. Many companies offer equipment out necessitating additional surgical procedures. Other refurbishment, which can decrease costs in subsequent promising technologies include powering transmitters years of telemetry, after getting started. Thus, one way via kinetic energy of the moving animal (e.g., [33, 34]). to make telemetry studies more equitable could be for Some companies prefer to remain within their product companies to sell refurbished equipment at discounted expertise, but many companies will work closely with prices, as some already do. researchers to develop relatively simple, small, pragmatic Despite already-high costs for telemetry equipment, product characteristics for certain projects. some survey respondents still indicated they are willing Alternatively, in the absence of a single product that to pay top dollar for a device that measures everything fulfills all their niche demands, several survey respond - they want it to. However, interview responses from com- ents reported using more than one datalogger/trans- panies suggest they disagree. Researchers state that they mitter to record all their variables of interest. This may are willing to pay more money for their ideal equipment, especially be a helpful option for well-funded projects on but companies argue that in the end, idealized equipment large animals. Integrating several technologies in this way is too expensive to be feasible. Companies are actively could further be improved with universal telemetry data working to improve many product characteristics, but formatting. there will likely be a standstill on many niche product characteristics, at least from the large telemetry compa- Temperature‑sensing telemetry nies, until there is enough demand to satisfy manufactur- Current status ers’ need for profit. This presents telemetry innovation Temperature can currently be incorporated into wildlife with a predicament: certain product characteristics are telemetry as a variable measured by the telemetry sys- unlikely to be developed unless they are mainstream tem and recorded on a separate data logger, and devices enough to garner widespread use and thus sales and may be attached to or implanted into animals. The most profitability, but how can those product characteristics common method that manufacturers use to introduce become mainstream before they are developed and avail- temperature sensors into a telemetry system is to create able for purchase? acoustic transmitters with a signal pulse rate calibrated against temperature measurements, such that the inter- Potential product development pulse interval of the telemetry signals of field-active ani - One solution is to put the responsibility of product devel- mals can be recorded over time, usually by a receiver, opment on the researchers. Several survey respondents and then later converted to temperature data. Surgically reported that they use “DIY” equipment to measure their implanted transmitters facilitate the collection of inter- desired variables on a reasonable budget. While some nal body temperature data of free-ranging animals [3, 5], researchers actually engineer their own transmitters or allowing researchers to study the relationship between other equipment, others modify existing technology. One body temperature and various physiological processes example of this is user-modifications to reduce the size and behavioral habits in a natural, ecologically relevant and weight of Thermochron iButton temperature loggers, setting. Externally attached transmitters can yield esti- which are often used with telemetry for thermal ecology mates of animal body surface temperature [5, 6]. Alter- studies [27–29]. In addition, for two of the most preva- natively, temperature-sensing telemetry devices may be lent telemetry equipment problems—data download used to outfit wild animals as “bioprobes”, to record data and battery life—survey respondents proposed poten- about environments humans have difficulty accessing tial fixes using drones and rechargeability. For example, [35]. using drones as mobile telemetry receivers could remove We found that most survey respondents do not use limitations due to poor signal range, animals in inac- temperature-sensing telemetry, which explains why com- cessible environments, and other challenges [30, 31]. panies perceive a low demand for it. The application of Alternatively, if receivers were smaller and many could temperature-sensing telemetry has previously been lim- be purchased for a given project, they could be placed ited to niche studies on ectotherms, whose physiology, throughout the study species’ range to help track move- movement, and behavior are directly linked to tempera- ment and habitat use where GPS cannot be implemented ture [5, 6, 36–38]. In accordance with this idea, survey for size or signal limitations. For transmitters attached respondents who reported studying ectotherms were to organisms externally, solar power is already a known significantly more likely to have used temperature-sens - avenue for battery rechargeability [32]. Could internally ing telemetry than those studying endotherms, with use implanted transmitters be recharged wirelessly by placing of this technology particularly prevalent in studies on the animal with the implanted device inside a charging sharks and rays, reptiles, amphibians, and invertebrates. Weaver et al. Anim Biotelemetry (2021) 9:29 Page 10 of 13 It may seem that collecting internal or surface tempera- also be expensive and suffer from several serious limita - ture data is not as applicable to studies on endotherms, tions, including that study animals must remain within which also typically maintain relatively stable body tem- the range of the stationary array, and that the array can peratures, known as homeothermy. However, endo- be damaged by livestock, wildlife, bad weather, or people. thermy and homeothermy do not disconnect animals Further information on specific challenges and solutions from the physiological, ecological, and behavioral effects to measuring and logging body temperature in free-rang- of temperature [39]. Some researchers using externally ing ectotherms can be found in [5]. These deterrents as attached transmitters like radio-collars to study endo- well as the lack of modernization of equipment likely therms may benefit from adding temperature sensors to contribute to researchers’ avoidance of temperature- their transmitters, as data on the ambient temperature sensing telemetry unless they are specifically interested of the animal’s microhabitat may be useful to remotely in temperature. As thermal studies increase to study the estimate activity patterns [7]. For example, the tem- effects of climate change, we expect increased demand perature fluctuations detected by a temperature-sensing for improvements of temperature-sensing telemetry transmitter on a small mammal as it moves to and from products. its burrow could allow researchers to remotely construct activity budgets for the species [40]. For large animals, Future possibilities this may be more easily recorded using small tempera- Most animals, ectotherms and endotherms alike, suffer ture dataloggers (e.g., HOBO Tidbit, Thermochron in extreme heat. As climate change brings increasingly iButton) in combination with regular, non-temperature- hot summers along with intermittent heat waves, collect- sensing transmitters. As reported by our survey respond- ing temperature data has become informative for more ents, using several pieces of equipment in this way is a researchers studying animals in all habitats. Studies that common solution. However, for small animals, adding track temperature-related habitat use inform conserva- temperature sensitivity to the transmitter may be more tion efforts to provide thermal refugia [6]. Understand - efficient because it adds less weight than would adding ing thermal preferences and limitations and predicting a separate datalogger. Temperature-sensing transmitters how animals will struggle physiologically due to climate implanted internally in endotherms may elucidate partial change are important considerations now so that conser- ectothermy [41] or be used to track feeding effects [42], vation mitigation can be optimally guided going forward. health [43, 44], and thermal stress due to climate change There is incredible potential for improved temperature- [45]. Temperature-sensing telemetry may be especially sensing telemetry to promote research in physiology, helpful when studying species with regional or temporal ecology, and conservation. For the survey respondents heterothermy [46–49]. There is literature discussing the that reported using temperature-sensing telemetry, there merits and potential methods to implement temperature- was overwhelming agreement that researchers would be sensing telemetry and biologging in endotherms [50, 51], willing to pay more for temperature-sensing technology yet such applications are severely lacking. that incorporated more of their fantasy equipment char- Another reason for the relatively low reported use of acteristics (Q19, Fig. 4), yet equipment manufacturers do temperature-sensing telemetry is that researchers are not feel the pressure to improve or create these products. unlikely to use this technology unless their research goals What is lacking? Some survey responses revealed that explicitly include studying the thermal ecology of the researchers are seemingly unaware of currently available study species. Temperature-sensing transmitters incur temperature-sensing telemetry equipment, which could additional costs to the price, weight, size, and/or bat- explain the lack of demand companies reported as the tery life of the transmitter. Most temperature-sensing primary reason for their lack of investment in tempera- transmitters, whether internal or external, send temper- ture-sensing telemetry technology. Just as the implemen- ature measurements to a receiver and do not store the tation of telemetry in general exploded as it became more data. Researchers can log the temperature of the animal visible, perhaps temperature-sensing telemetry needs when they track them in the field, but this point-sam - more publicity. As soon as awareness and implementa- pling leads to temporally biased body temperature data tion of temperature-sensing telemetry increases, costs [3]. For researchers aiming to collect continuous body to both users and manufacturers will go down, but there temperature, they can build their own data storage sys- must be better and easier-to-use temperature-sensing tems [52] or invest in a manufacturer-produced receiver technology for it to expand its use among the research and antenna array with data acquisition (e.g., Telonics or community. Once temperature-sensing telemetry equip- Lotek both produce such systems). Although these sys- ment overcomes the current technological, develop- tems can facilitate continuous body temperature data mental, and accessibility hurdles, a whole new realm of that are very valuable for many studies, these options can scientific questions will become possible. Studies that W eaver et al. Anim Biotelemetry (2021) 9:29 Page 11 of 13 Authors’ contributions seek to understand thermal ecology and physiology and SJW is credited for preparation and administration of the survey and inter- the effects of climate change have already become more views, analysis and visualization of the responses, and preparation of the man- feasible with the advent of temperature-sensing telem- uscript. MFW is credited for sponsorship of this research, coordination of the studies of an endangered lizard that led to the conception of this paper, and etry, and further innovation would in turn expand the feedback on manuscript drafts. ENT is credited for conception and preparation potential questions that researchers may attempt to of the manuscript. All the authors read and approved the final manuscript. answer. Funding No funding sources to declare. Conclusions Availability of data and materials Telemetry has facilitated a robust and growing field of The datasets created from the survey and interviews are not publicly available wildlife research, which survey responses show can be to maintain privacy of participants’ individual responses and opinions. All analyses and figures were done in R v4.0.3. The original Microsoft Forms survey used to answer a breadth of scientific research questions. used is included with this publication as Additional file 1, and count data for However, researchers have a lengthy and ever-growing the survey responses are included in Additional file 2. list of technological advances awaiting fulfillment by manufacturers. As manufacturers respond to researchers’ Declarations demands for new and improved products, the breadth of Ethics approval and consent to participate potential telemetry studies will widen and gain depth as The survey and interviews we conducted were approved by the California well. One useful telemetry application is the integration Polytechnic State University Institutional Review Board (Project 2020–183). All of thermal sensors, which may inform how the climate survey and interview participants were informed about the risks and benefits associated with their participation. Survey participants certified their eligibility crisis is affecting animals’ behavior, physiology, ecology, and consent by completing and submitting the survey. Interview participants and much more. Given the current progression of cli- explicitly signed an informed consent form to participate and allow their mate change, increased application and improvement of responses to be included in this paper. temperature-sensing telemetry equipment is especially Consent for publication urgent. Not applicable. A primary obstacle to telemetry innovation and imple- Competing interests mentation is funding. The future of telemetry is in coop - The authors report no competing interests. erative use of devices and government funding for the development of new and improved products. For exam- Author details Biological Sciences Department, College of Science and Mathematics, ple, two research teams using telemetry in opposite sea- California Polytechnic State University, San Luis Obispo, CA 93407-0401, USA. sons could share devices. Increased government funding Central Coast Field Office, US Bureau of Land Management, 940 2nd Ave., for telemetry product development could help compa- Marina, CA 93933, USA. nies overcome the initial costs deterring them from mak- Received: 19 February 2021 Accepted: 2 July 2021 ing new products, especially ones that would be widely used once engineered. In conjunction, these strategies could increase the number of researchers using telemetry as well as the range and quality of technology available References for their use. 1. 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Technology wish lists and the significance of temperature-sensing wildlife telemetry

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Abstract

Telemetry has revolutionized studies in wildlife biology, ecology, physiology, and conservation. With the increased demand for telemetry, new technology has made great strides to enable long studies in harsh and remote areas on a wide variety of study species. As the climate crisis continues to impact animals, temperature-sensing telemetry has become a helpful technique for understanding the effects of climate change and how to protect wildlife from them. However, temperature-sensing telemetry and telemetry in general still pose technological challenges and accessibil- ity issues for the researchers who use it. Currently available telemetry technology is expensive, too large and heavy for many study species, and cannot measure all variables researchers want to study. These technological improvements have especially been neglected for temperature-sensing telemetry, which may be underutilized given the current climate crisis. To understand why innovation has stalled, and where it should be directed going forward, we gathered opinions from researchers who use telemetry and from manufacturers that create and supply telemetry equipment. Our goal was to broadly describe the current technological landscape, compare it to what we envision for the future, and make suggestions for how to reach that future. Keywords: Company, Innovation, Interview, Manufacturer, Survey, Technology, Telemetry, Temperature, Wildlife tracking Introduction become accessible to more researchers. During the cur- Wildlife studies were originally confined to live animal rent “golden age” of animal biotelemetry, advances in trapping, surveys, and transects that provided snapshot technology are allowing scientists to learn much more ecological and physiological data. Capture–mark–recap- about wild animals, using less invasive, and therefore, ture studies were possible for certain types of animals, more fruitful and relevant methods [1, 2]. but recapturing individuals to study how they change An especially promising advance is temperature-sens- over time remained challenging or impossible for most ing telemetry. Temperature-sensing telemetry (which animals until the advent of telemetry in the mid-1950s. senses temperature) combined with datalogging technol- Since then, advances in telemetry have revolutionized ogy (which records temperature data) in the transmit- studies in wildlife biology, ecology, physiology, and con- ters themselves, in receivers, or in separate dataloggers, servation. The number of publications using telemetry to allows researchers to remotely collect environmental or study animals has skyrocketed in the past 20 years (Fig. 1) body temperature data without spatial or temporal bias as technology continues to improve and as transmitters [3]. As the climate crisis continues to impact animal dis- tributions, movement, health, and interactions, among other factors, temperature-sensing telemetry will be *Correspondence: savannahjweaver@gmail.com pivotal. Altered temperature regimes are and will con- Biological Sciences Department, College of Science and Mathematics, tinue to be the driver of physiological stress and con- California Polytechnic State University, San Luis Obispo, CA 93407-0401, USA straints [4]. Measuring temperature using telemetry Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Weaver et al. Anim Biotelemetry (2021) 9:29 Page 2 of 13 Fig. 1 The number of publications using animal biotelemetry has risen dramatically in the past 20 years. Data are from a Web of Science search conducted on 3 June 2021 for the following terms: wildlife telemetry, wildlife biotelemetry, wildlife tracking, animal telemetry, animal biotelemetry, and animal tracking will help describe changes in environmental tempera- undergone incredible miniaturization and cost reduction, ture and changes in behavior as a response. Ectotherms further improvements could still be made so the tech- have emerged as model organisms to study these effects nology is feasible for a greater suite of animals and more because environmental temperature plays such a direct researchers. Even basic very high-frequency (VHF) radio role in their physiology [4, 5]. These data are essential for telemetry remains out of reach for many researchers conservation efforts because continuous body and envi - with smaller budgets, including many researchers from ronmental temperature data can be used to predict the low-income countries. This amplifies scientific biases by effects of climate change on at-risk populations [6]. Tem - excluding certain researchers from being able to access perature-sensing telemetry can also be used to remotely telemetry equipment, increasing the likelihood of para- collect data on both ectothermic and endothermic ani- chute scientists conducting telemetry and thus perpetu- mals’ activity patterns, from terrestrial surface activity [7] ating problematic colonial science [9–11]. Furthermore, to marine diving behavior [8]. Clearly, temperature rep- scientists studying very small animals still face major resents a key variable for physiology, ecology, and behav- challenges with telemetry due to the tradeoff between ior, thus one might expect temperature-sensing telemetry battery life and transmitter size/weight. Challenges with to be a high priority for researchers and manufacturers. access to telemetry equipment and with the technology However, in our experience, temperature-sensing telem- itself therefore remain, and this commentary serves to etry is underutilized, and its technological advances summarize opinions on these challenges from both the appear to have stalled. While temperature-sensing trans- creators and users of the technology. mitters have enjoyed the same miniaturization as regu- Researchers who use telemetry to study the ecology lar transmitters, temperature datalogging technology in and physiology of a wide variety of animals, including receivers remains largely unchanged since the 1980s. endangered species and the effects of climate change, Additional areas of improvement include technology are greatly impacted by the technology available to them. capabilities, size/weight, and price. In some cases, telem- Many factors impact the design and price of telemetry etry may not be an improvement on capture–mark– transmitters, sensors, receivers, antennas, software, and recapture studies because telemetry devices cannot other equipment. Like all producers and consumers, the measure the variables of interest. Although devices have challenges and constraints faced by companies producing W eaver et al. Anim Biotelemetry (2021) 9:29 Page 3 of 13 telemetry gear and by scientists using it for research are Researcher surveys often different. For example, transmitters may be paired Methods with various sensors [12] that measure and log changes in Throughout November 2020, we distributed an online the animal’s behavior (e.g., by measuring speed or accel- Microsoft Form with a combination of free response, eration), physiology (e.g., muscular activity, sound pro- rank-choice, and Likert scale questions (Additional duction, temperature), or environmental conditions (e.g., file  1). In our survey questions, we used the terminol- dissolved oxygen, altitude). Many of these sensors repre- ogy “temperature-sensitive telemetry”, which we define sent niche equipment that are strongly desired by some the same way as “temperature-sensing telemetry”. We researchers but may not be worthwhile for manufactur- distributed the survey using social media (Twitter, Face- ers to produce en masse. Companies producing telemetry book) and via email to corresponding authors of papers equipment are typically private, for-profit businesses that published in the journal Animal Biotelemetry in the past must balance the price points of their equipment with 2 years and of papers publicized on telemetry company researcher demand and the ever-changing landscape of websites. Of the 84 telemetry users who responded to the research funding. Finally, manufacturers must respond survey, 23% were university faculty (n = 19), 20% were to, and indeed anticipate, the technological needs of postdoctoral researchers (n = 17), 20% were graduate stu- researchers, and in turn researchers are often con- dents pursuing either an MS or PhD (n = 17), 16% were strained by manufacturer investment choices, creating non-academic researchers such as those associated with an intricate dance between tech-users and tech-creators, government or nonprofit organizations (n = 13), and 20% the progress of which may have dire impacts for research responded as “other” (n = 17), with one non-response. on sensitive or endangered species in this current climate We recognize that our survey has distribution and par- crisis and associated mass extinction. ticipation biases. We present this commentary to advocate for what Survey responses were exported to Microsoft Excel telemetry advances could and should be made in the for count data. Respondents could choose more than future. We aim not to describe what is currently possi- one answer choice for each question, so the percentages ble, but what researchers want to be possible. We gath- of respondents choosing a given answer sums to greater ered opinions from researchers who use telemetry and than 100% for most questions. SJW coded written free from manufacturers that create and supply telemetry responses for keywords. We used X tests to determine equipment to broadly describe the current technological whether there was a significant difference in the fre - landscape and to compare it to what we envision for the quency of temperature-sensing telemetry use based on future. Telemetry technology includes Global Positioning study organism (endotherm versus ectotherm and by Systems (GPS), VHF radio, and Argos satellite tracking. clade), study habitat, or device attachment method. The A given telemetry system may consist of various sensors sample sizes vary for each test because respondents may that measure, transmitters that send, and receivers or log- have selected more than one option for a given question. gers that record the data of interest [13]. However, in this For the analysis of study organism, each survey respond- paper, we refer to telemetry broadly because the opinions ent was coded to study either endotherms, ectotherms, discussed apply to all telemetry systems. We surveyed 84 or both (n = 84). For analyses of clade, habitat, and total scientific researchers who use telemetry and interviewed device attachment method, we excluded those research- representatives of 9 companies that design, manufacture, ers who selected more than one clade, study habitat, and sell telemetry equipment. We collected perceptions or attachment method because their incorporation of of telemetry equipment generally, but we also focused temperature may have only been related to one of the specifically on temperature-sensing telemetry to evaluate responses listed (n < 84 for each of these tests). Fig- total whether our perceived lack of user interest and manu- ure  2 shows the full dataset with no exclusions made, so facturer investment is evident, and to pursue reasons for it does not perfectly reflect the X test statistics and per- this. We describe current implementations of temper- centages presented in the results. We used R v4.0.3 [14] ature-sensing telemetry, assert the need for improved and tidyverse workflow [15] to create figures and analyze telemetry technology in general and increased focus on data. The survey and the use of data were approved by temperature-sensing telemetry, and make suggestions the California Polytechnic State University Institutional for how to achieve these key innovations. The informa - Review Board (Project 2020-183). tion presented here will be a resource in the coming years for researchers planning to acquire telemetry equipment Current telemetry applications and organizing new studies, as well as for manufacturers Most of the respondents (56%) reported studying endo- deciding which technological directions may optimize therms, 39% studied ectotherms, and 5% studied both. their investment. The number of study species listed by survey respondents Weaver et al. Anim Biotelemetry (2021) 9:29 Page 4 of 13 Fig. 2 Study organisms, habitats, and transmitter-animal pairing methods. Survey respondents (N = 84) indicated a their study organism(s), b their study organisms’ primary habitat(s), and c the mode(s) of device attachment to their study animals. All vertical axes represent count data totaled 255, although many were not listed to species- of study questions, including animal movement, habitat level. In order of popularity, birds (Aves), mammals use, behaviors, home range, survivorship, activity timing, (Mammalia), reptiles (Reptilia), ray-finned fishes (Actin - sociality, management needs/outcomes, and more (Addi- opterygii), and sharks and rays (Chondrichthyes) were tional file 2). the most common clades of study animals in our sample of researchers using telemetry (Fig.  2a); other telemetry Telemetry wish lists study species included amphibians, insects, and crayfish. Survey respondents were asked to rank their top priori- Terrestrial organisms are the most tracked animals based ties when selecting telemetry equipment, and the charac- on this survey (77% of respondents study them), followed teristics with the most first-choice rankings were weight, by freshwater (25%) and marine (17%, Fig.  2b). Most price, size, variables recorded, and battery life (Fig.  3). respondents (65%) reported that they use external attach- Durability, data storage, and receiver range were also pri- ment methods such as a collar, waistband, backpack, or orities but were comparably less important. similar; 42% reported that they use adhesives such as glue Researchers are only somewhat satisfied with the cur - or tape; 31% reported that they implant devices (Fig. 2c). rently available telemetry equipment they use. Most Researchers reported using telemetry for a wide array survey respondents are unable to measure everything W eaver et al. Anim Biotelemetry (2021) 9:29 Page 5 of 13 Fig. 3 Researchers’ most important telemetry product characteristics. Survey respondents (N = 84) ranked what factors are most important to them when selecting telemetry equipment desired with the equipment they use (Q11, Fig.  4). We telemetry to measure and record, fantasy equipment asked respondents what variables they want to be able refers to any and all telemetry product characteristics. to measure that cannot be measured/recorded by cur- The top ten fantasy equipment characteristics were rently available telemetry equipment (Additional file  1, smaller and lighter transmitters (60%), longer battery life Question 7). We used these responses to create a “wish (54%), more variables measured (52%), lower cost (23%), list” of variables that respondents wished their current more data storage (22%), better durability for rough envi- telemetry devices could measure and transmit/record. ronments, including waterproofing and for use with reck - Some of the additional variables with the highest demand less animals (21%), longer signal range (18%), remote data among survey respondents included assessing movement download ability (17%), higher measurement frequency and behaviors via accelerometry (12%), and measuring/ (13%), and more precise measurements (13%; Addi- recording environmental temperature (6%), heart rate tional file  2). Survey respondents suggested solar power (6%), internal body temperature (5%), and audio and/ to extend battery life and urged that including a battery or video recordings (5%). See Additional file  2 for a full indicator would be immensely helpful. In an ideal world list of variables respondents wished their equipment with no technological constraints, researchers hope for recorded. all these capabilities and more in ever-smaller devices. Respondents reported that their most time-consuming technical difficulties when using telemetry equipment for Temperature‑sensing telemetry studies included equipment running out of battery power 33% of respondents reported that they incorporate prematurely (19%), equipment failing or breaking (18%), either environmental or organismal temperature into issues with data or equipment retrieval (17%), and diffi - their telemetry (Q12, Fig.  4). Respondents who reported cult data formatting (13%; Additional file  2). Conversely, studying ectotherms incorporate temperature into we asked respondents to imagine there were no techno- their telemetry studies significantly more often (57%) logical limits and describe traits of their ideal, “fantasy” than respondents studying endotherms (15%; n = 84, equipment that would meet all of their research needs X = 17.0, df = 2, p < 0.001; Fig.  2a). The frequency of and interests if anything was possible (Additional file  1, temperature-sensing telemetry use was also significantly Question 13). Whereas the variable wish lists described different across study organism clades (n = 70, X = 19.3, above referred to what variables researchers wanted df = 5, p = 0.002; Fig.  2a): 16% of respondents studying Weaver et al. Anim Biotelemetry (2021) 9:29 Page 6 of 13 Fig. 4 Researchers’ opinions on the research application and affordability of current telemetry equipment. Survey respondents (N = 84) indicated their satisfaction with the variables measured by current telemetry equipment, whether or not they use temperature-sensing telemetry, and their opinions on the pricing of telemetry equipment. Questions abbreviated for the figure (e.g., temperature equipment refers to temperature-sensing telemetry equipment); see Additional file 1 for full questions birds incorporate temperature, with 13% for mammals, opinion as strongly (Q16 and Q18, Fig. 4), and may even 56% for reptiles, 20% for ray-finned fishes, 100% for be willing to pay more for better temperature-sensing sharks and rays, and 75% for “other” organisms, which telemetry technology (Q19, Fig. 4). consisted of ectothermic amphibians and invertebrates. Researchers studying marine organisms were most likely Company interviews to incorporate temperature (71%), followed by terrestrial Methods (30%), then freshwater (20%). The frequency of temper - To understand telemetry product development and pre- ature-sensing telemetry use was not significantly differ - dict future advances, we interviewed representatives ent among study animal habitats (n = 67, X = 5.6, df = 2, from companies that manufacture telemetry equipment p = 0.059; Fig.  2b) or major mode of device attachment over the phone or via email correspondence. We com- (n = 53, X = 4.7, df = 2, p = 0.096; Fig. 2c). piled a list of companies to interview that we already For respondents who do not use temperature-sensing knew of or that we found in a basic Google search prior telemetry, 37% said that temperature was unrelated to to distributing the researcher survey. Of the 17 compa- their research questions, 8% said it was unnecessary nies we contacted, 11 responded to our queries, and 9 because there was not sufficient temperature variation to followed through with the interview (Additional file  2): measure in their context, and 5% had never considered Advanced Telemetry Systems, Inc. (ATS; Isanti, Minne- the possibility of including temperature in their telemetry sota, United States), Cellular Tracking Technologies LLC studies. Some researchers may have wanted to include (CTT; Rio Grande, New Jersey, United States), Holo- temperature but were unable to do so due to cost (13%), hil Systems, Ltd. (Carp, Ontario, Canada), Innovasea logistics of product trade-offs and availability (12%), size/ Systems Inc. (Canada; Chile; Norway; United States), weight limitations (10%), and battery lifespan (2%; Fig. 5). mOOvement (Brisbane, Queensland, Australia), Micro- Respondents overall said that the current price of telem- wave Telemetry, Inc. (MTI; Columbia, Maryland, United etry equipment is too high (Q15 and Q17, Fig.  4), but States), TechnoSmart Europe SRL (Guidonia, Rome, temperature-sensing telemetry users do not share this Italy), Vectronic Aerospace Inc. (Coralville, Iowa, United W eaver et al. Anim Biotelemetry (2021) 9:29 Page 7 of 13 Fig. 5 Why researchers do not include temperature. Survey respondents who do not use temperature-sensing telemetry equipment (N = 56) indicated why they do not use it States), and Wildlife Computers, Inc. (Redmond, Wash- engage with researchers, but more companies reported ington, United States). that they rely on unsolicited feedback and casual con- Our aim was not to draw conclusions about the popu- versations with customers to gauge interest in new and larity of companies or to compare their products, but improved products. Approximately half of the com- rather to understand product development and to gauge panies we interviewed said that miniaturization and whether manufacturers’ perception of researchers’ improving reliability are the most important product desires align with the needs reported by survey respond- characteristics to improve, with extending battery life/ ents. We asked manufacturer representatives questions efficiency, improving durability, and lowering price also about their product development and market perception listed by several companies. Although they stated that generally, as well as questions directly related to temper- they are actively working on improving each of these, ature-sensing equipment (Additional file  3). The inter - miniaturization was of primary importance. However, views and the use of data from them were approved by companies feel inconsistent pressure to make these the California Polytechnic State University Institutional improvements. Some companies reported constant Review Board (Project 2020-183), and we received per- demand for new and improved products, while others mission from the interviewees that we could include their reported very little. company’s name and responses in our paper. According to manufacturers, the equipment charac- teristics that researchers desire tend to create trade- offs, where each innovation comes with a drawback. Current product development For example, measuring an additional variable uses Eight of the nine companies we interviewed said that more battery, makes the device larger and heavier, they use customer feedback and requests to determine and/or increases its cost. Additionally, a common sen- what directions to take for product development and timent from companies was that new and improved improvement. Other ways product development may be products are an endless cycle: before manufacturers directed included demand, predicting research trends, can even develop and refine one technology, research - and company goals and interests, each of which were ers have already come up with new research ques- listed by 2–3 companies. Several of the companies we tions that necessitate the development of another new interviewed reported that they rely on conferences to technology. Weaver et al. Anim Biotelemetry (2021) 9:29 Page 8 of 13 Temperature‑sensing telemetry responses, but they maintain reservations about creat- Company representatives reported that between 0 and ing new technology. Researchers can be eager to get new 15% of their customers are interested in incorporating technology on an urgent timeline, but seemingly simple temperature into their equipment, with most estimating innovations can take years to develop into something between 5 and 10%. Since the baseline demand for tem- actually effective. Researchers’ demand for improved perature-sensing telemetry equipment is so low, almost telemetry equipment has already pushed huge techno- all the manufacturers we interviewed reported that their logical advances [1, 2, 24, 25], and based on researcher perceived demand for new and improved temperature- demands and company plans, these improvements will sensing telemetry equipment was essentially nonexist- continue. Equipment manufacturers are indeed working ent. Some companies automatically include temperature hard to meet researchers’ most pressing needs, but the sensors in all products, and others can incorporate tem- technology will always lag behind the new applications perature sensors into any product. These sensors most desired. often record ambient temperature or animal surface body Certain innovations are unlikely because there is not temperature. Some companies also produce surgically enough demand, they would be too difficult to engi - implantable temperature-sensing transmitters that can neer, or the product would not be profitable enough. For yield data on animal core body temperature. For those example, researchers always want to get the same or bet- companies that produce temperature-sensing transmit- ter technology in an ever-smaller package, but there need ters and feel demand for improvement of temperature- to be better batteries available before that will be possi- sensing products specifically, they are currently working ble. Survey respondents had numerous wish list variables to make temperature measurements more precise and that they want telemetry equipment to be able to meas- the transmitters smaller and less expensive, although this ure; however, most variables were only listed by < 5% of applies to few companies. respondents (Additional file  2). The amount of product development necessary to create a niche product for a Technological trade‑offs single project is unlikely to be financially feasible for the After nearly a century of telemetry innovation, there is manufacturer or the user. Many innovations are simply now a wide array of telemetry devices with an even wider not feasible because the number of buyers would be so array of potential applications [1, 2, 12, 16]. Telemetry small. now enables studies on topics such as animal movement Even when certain product characteristics can be and migration [17–19], physiological processes [20, 21], achieved, there is usually an associated downside such as or social interactions [22], and our survey respondents shorter battery life, larger/heavier transmitters, loss of a compiled an even longer list of current applications different sensor, and especially increased product cost. (Additional file  2). However, the survey responses also Survey respondents wrote about having to make deci- show how many research interests still cannot yet be sat- sions based on these trade-offs with sample size, trans - isfactorily investigated using telemetry. mitter size/weight, and battery life. When it comes to Our survey of researchers who use telemetry to study telemetry equipment, there is not a single product that animals and interviews with the manufacturers that pro- will fit the needs of every study. This may be one rea - duce telemetry equipment revealed only partial align- son why researchers reported using such a diverse array ment between supply and demand. For example, both of manufacturers (n = 42, Additional file  2), some of researchers and manufacturers identified transmitter whom specialize in specific technologies. Unfortunately, miniaturization as a top priority. However, one over- it seems researchers are often unable to find the right looked issue brought up in the survey responses, and in company for a product that will most closely match their a recent review paper focusing on satellite telemetry [23], needs, as most of the respondents’ desired wish list vari- was difficult data formatting. This was the only issue that ables have been recorded using biotelemetry [2]. To navi- did not seem to be on any company’s radar in our inter- gate the vast array of telemetry manufacturers, products, views. An inability to understand data structure and ana- and applications, several reviews and guides are informa- lyze it could be a barrier to researchers wishing to begin tive [12, 16, 23, 26]. using telemetry or simply looking to switch telemetry manufacturers. A universal telemetry data structure, per- Financial obstacles haps agreed upon by a coalition of company representa- Telemetry, along with much scientific research, is gener - tives and data scientists, could go a long way to inspire ally dominated by well-funded projects and universities new telemetry users and applications. in wealthy nations. The cost of telemetry devices limits Overall, companies recognize most of the wish list vari- the number of variables that can be measured, animals ables and fantasy equipment traits compiled in the survey that can be tracked, and researchers who can use it. Even W eaver et al. Anim Biotelemetry (2021) 9:29 Page 9 of 13 if product costs were to fall, accessibility is likely to con- box? This could extend study lifetimes indefinitely with - tinue to be stratified. Many companies offer equipment out necessitating additional surgical procedures. Other refurbishment, which can decrease costs in subsequent promising technologies include powering transmitters years of telemetry, after getting started. Thus, one way via kinetic energy of the moving animal (e.g., [33, 34]). to make telemetry studies more equitable could be for Some companies prefer to remain within their product companies to sell refurbished equipment at discounted expertise, but many companies will work closely with prices, as some already do. researchers to develop relatively simple, small, pragmatic Despite already-high costs for telemetry equipment, product characteristics for certain projects. some survey respondents still indicated they are willing Alternatively, in the absence of a single product that to pay top dollar for a device that measures everything fulfills all their niche demands, several survey respond - they want it to. However, interview responses from com- ents reported using more than one datalogger/trans- panies suggest they disagree. Researchers state that they mitter to record all their variables of interest. This may are willing to pay more money for their ideal equipment, especially be a helpful option for well-funded projects on but companies argue that in the end, idealized equipment large animals. Integrating several technologies in this way is too expensive to be feasible. Companies are actively could further be improved with universal telemetry data working to improve many product characteristics, but formatting. there will likely be a standstill on many niche product characteristics, at least from the large telemetry compa- Temperature‑sensing telemetry nies, until there is enough demand to satisfy manufactur- Current status ers’ need for profit. This presents telemetry innovation Temperature can currently be incorporated into wildlife with a predicament: certain product characteristics are telemetry as a variable measured by the telemetry sys- unlikely to be developed unless they are mainstream tem and recorded on a separate data logger, and devices enough to garner widespread use and thus sales and may be attached to or implanted into animals. The most profitability, but how can those product characteristics common method that manufacturers use to introduce become mainstream before they are developed and avail- temperature sensors into a telemetry system is to create able for purchase? acoustic transmitters with a signal pulse rate calibrated against temperature measurements, such that the inter- Potential product development pulse interval of the telemetry signals of field-active ani - One solution is to put the responsibility of product devel- mals can be recorded over time, usually by a receiver, opment on the researchers. Several survey respondents and then later converted to temperature data. Surgically reported that they use “DIY” equipment to measure their implanted transmitters facilitate the collection of inter- desired variables on a reasonable budget. While some nal body temperature data of free-ranging animals [3, 5], researchers actually engineer their own transmitters or allowing researchers to study the relationship between other equipment, others modify existing technology. One body temperature and various physiological processes example of this is user-modifications to reduce the size and behavioral habits in a natural, ecologically relevant and weight of Thermochron iButton temperature loggers, setting. Externally attached transmitters can yield esti- which are often used with telemetry for thermal ecology mates of animal body surface temperature [5, 6]. Alter- studies [27–29]. In addition, for two of the most preva- natively, temperature-sensing telemetry devices may be lent telemetry equipment problems—data download used to outfit wild animals as “bioprobes”, to record data and battery life—survey respondents proposed poten- about environments humans have difficulty accessing tial fixes using drones and rechargeability. For example, [35]. using drones as mobile telemetry receivers could remove We found that most survey respondents do not use limitations due to poor signal range, animals in inac- temperature-sensing telemetry, which explains why com- cessible environments, and other challenges [30, 31]. panies perceive a low demand for it. The application of Alternatively, if receivers were smaller and many could temperature-sensing telemetry has previously been lim- be purchased for a given project, they could be placed ited to niche studies on ectotherms, whose physiology, throughout the study species’ range to help track move- movement, and behavior are directly linked to tempera- ment and habitat use where GPS cannot be implemented ture [5, 6, 36–38]. In accordance with this idea, survey for size or signal limitations. For transmitters attached respondents who reported studying ectotherms were to organisms externally, solar power is already a known significantly more likely to have used temperature-sens - avenue for battery rechargeability [32]. Could internally ing telemetry than those studying endotherms, with use implanted transmitters be recharged wirelessly by placing of this technology particularly prevalent in studies on the animal with the implanted device inside a charging sharks and rays, reptiles, amphibians, and invertebrates. Weaver et al. Anim Biotelemetry (2021) 9:29 Page 10 of 13 It may seem that collecting internal or surface tempera- also be expensive and suffer from several serious limita - ture data is not as applicable to studies on endotherms, tions, including that study animals must remain within which also typically maintain relatively stable body tem- the range of the stationary array, and that the array can peratures, known as homeothermy. However, endo- be damaged by livestock, wildlife, bad weather, or people. thermy and homeothermy do not disconnect animals Further information on specific challenges and solutions from the physiological, ecological, and behavioral effects to measuring and logging body temperature in free-rang- of temperature [39]. Some researchers using externally ing ectotherms can be found in [5]. These deterrents as attached transmitters like radio-collars to study endo- well as the lack of modernization of equipment likely therms may benefit from adding temperature sensors to contribute to researchers’ avoidance of temperature- their transmitters, as data on the ambient temperature sensing telemetry unless they are specifically interested of the animal’s microhabitat may be useful to remotely in temperature. As thermal studies increase to study the estimate activity patterns [7]. For example, the tem- effects of climate change, we expect increased demand perature fluctuations detected by a temperature-sensing for improvements of temperature-sensing telemetry transmitter on a small mammal as it moves to and from products. its burrow could allow researchers to remotely construct activity budgets for the species [40]. For large animals, Future possibilities this may be more easily recorded using small tempera- Most animals, ectotherms and endotherms alike, suffer ture dataloggers (e.g., HOBO Tidbit, Thermochron in extreme heat. As climate change brings increasingly iButton) in combination with regular, non-temperature- hot summers along with intermittent heat waves, collect- sensing transmitters. As reported by our survey respond- ing temperature data has become informative for more ents, using several pieces of equipment in this way is a researchers studying animals in all habitats. Studies that common solution. However, for small animals, adding track temperature-related habitat use inform conserva- temperature sensitivity to the transmitter may be more tion efforts to provide thermal refugia [6]. Understand - efficient because it adds less weight than would adding ing thermal preferences and limitations and predicting a separate datalogger. Temperature-sensing transmitters how animals will struggle physiologically due to climate implanted internally in endotherms may elucidate partial change are important considerations now so that conser- ectothermy [41] or be used to track feeding effects [42], vation mitigation can be optimally guided going forward. health [43, 44], and thermal stress due to climate change There is incredible potential for improved temperature- [45]. Temperature-sensing telemetry may be especially sensing telemetry to promote research in physiology, helpful when studying species with regional or temporal ecology, and conservation. For the survey respondents heterothermy [46–49]. There is literature discussing the that reported using temperature-sensing telemetry, there merits and potential methods to implement temperature- was overwhelming agreement that researchers would be sensing telemetry and biologging in endotherms [50, 51], willing to pay more for temperature-sensing technology yet such applications are severely lacking. that incorporated more of their fantasy equipment char- Another reason for the relatively low reported use of acteristics (Q19, Fig. 4), yet equipment manufacturers do temperature-sensing telemetry is that researchers are not feel the pressure to improve or create these products. unlikely to use this technology unless their research goals What is lacking? Some survey responses revealed that explicitly include studying the thermal ecology of the researchers are seemingly unaware of currently available study species. Temperature-sensing transmitters incur temperature-sensing telemetry equipment, which could additional costs to the price, weight, size, and/or bat- explain the lack of demand companies reported as the tery life of the transmitter. Most temperature-sensing primary reason for their lack of investment in tempera- transmitters, whether internal or external, send temper- ture-sensing telemetry technology. Just as the implemen- ature measurements to a receiver and do not store the tation of telemetry in general exploded as it became more data. Researchers can log the temperature of the animal visible, perhaps temperature-sensing telemetry needs when they track them in the field, but this point-sam - more publicity. As soon as awareness and implementa- pling leads to temporally biased body temperature data tion of temperature-sensing telemetry increases, costs [3]. For researchers aiming to collect continuous body to both users and manufacturers will go down, but there temperature, they can build their own data storage sys- must be better and easier-to-use temperature-sensing tems [52] or invest in a manufacturer-produced receiver technology for it to expand its use among the research and antenna array with data acquisition (e.g., Telonics or community. Once temperature-sensing telemetry equip- Lotek both produce such systems). Although these sys- ment overcomes the current technological, develop- tems can facilitate continuous body temperature data mental, and accessibility hurdles, a whole new realm of that are very valuable for many studies, these options can scientific questions will become possible. Studies that W eaver et al. Anim Biotelemetry (2021) 9:29 Page 11 of 13 Authors’ contributions seek to understand thermal ecology and physiology and SJW is credited for preparation and administration of the survey and inter- the effects of climate change have already become more views, analysis and visualization of the responses, and preparation of the man- feasible with the advent of temperature-sensing telem- uscript. MFW is credited for sponsorship of this research, coordination of the studies of an endangered lizard that led to the conception of this paper, and etry, and further innovation would in turn expand the feedback on manuscript drafts. ENT is credited for conception and preparation potential questions that researchers may attempt to of the manuscript. All the authors read and approved the final manuscript. answer. Funding No funding sources to declare. Conclusions Availability of data and materials Telemetry has facilitated a robust and growing field of The datasets created from the survey and interviews are not publicly available wildlife research, which survey responses show can be to maintain privacy of participants’ individual responses and opinions. All analyses and figures were done in R v4.0.3. The original Microsoft Forms survey used to answer a breadth of scientific research questions. used is included with this publication as Additional file 1, and count data for However, researchers have a lengthy and ever-growing the survey responses are included in Additional file 2. list of technological advances awaiting fulfillment by manufacturers. As manufacturers respond to researchers’ Declarations demands for new and improved products, the breadth of Ethics approval and consent to participate potential telemetry studies will widen and gain depth as The survey and interviews we conducted were approved by the California well. One useful telemetry application is the integration Polytechnic State University Institutional Review Board (Project 2020–183). All of thermal sensors, which may inform how the climate survey and interview participants were informed about the risks and benefits associated with their participation. Survey participants certified their eligibility crisis is affecting animals’ behavior, physiology, ecology, and consent by completing and submitting the survey. Interview participants and much more. Given the current progression of cli- explicitly signed an informed consent form to participate and allow their mate change, increased application and improvement of responses to be included in this paper. temperature-sensing telemetry equipment is especially Consent for publication urgent. Not applicable. A primary obstacle to telemetry innovation and imple- Competing interests mentation is funding. The future of telemetry is in coop - The authors report no competing interests. erative use of devices and government funding for the development of new and improved products. For exam- Author details Biological Sciences Department, College of Science and Mathematics, ple, two research teams using telemetry in opposite sea- California Polytechnic State University, San Luis Obispo, CA 93407-0401, USA. sons could share devices. Increased government funding Central Coast Field Office, US Bureau of Land Management, 940 2nd Ave., for telemetry product development could help compa- Marina, CA 93933, USA. nies overcome the initial costs deterring them from mak- Received: 19 February 2021 Accepted: 2 July 2021 ing new products, especially ones that would be widely used once engineered. In conjunction, these strategies could increase the number of researchers using telemetry as well as the range and quality of technology available References for their use. 1. 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Journal

Animal BiotelemetrySpringer Journals

Published: Aug 18, 2021

Keywords: Company; Innovation; Interview; Manufacturer; Survey; Technology; Telemetry; Temperature; Wildlife tracking

References