SPECIALTY GRAND CHALLENGE published: 30 March 2021 doi: 10.3389/fphys.2021.669158 The New Era of Physio-Logging and Their Grand Challenges Andreas Fahlman 1*, Kagari Aoki 2 , Gemma Bale 3 , Jeroen Brijs 4 , Ki H. Chon 5 , Colin K. Drummond 6 , Martin Føre 7 , Xavier Manteca 8 , Birgitte I. McDonald 9 , J. Chris McKnight 10 , Kentaro Q. Sakamoto 2 , Ippei Suzuki 11 , M. Jordana Rivero 12 , Yan Ropert-Coudert 13 and Danuta M. Wisniewska 14 1 Fundación Oceanográfic de la Comunitat Valenciana, Valencia, Spain, 2 Department of Marine Bioscience, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Japan, 3 Department of Physics and Department of Engineering, University of Cambridge, Cambridge, United Kingdom, 4 Hawai’i Institute of Marine Biology, University of Hawai’i at Manoa, Manoa, HI, United States, 5 Biomedical Engineering, University of Connecticut, Storrs, CT, United States, 6 Biomedical Engineering, Case Western Reserve University, Cleveland, OH, United States, 7 Department of Engineering Cybernetics, Norwegian University of Science and Technology, Trondheim, Norway, 8 Department of Animal and Food Science, Autonomous University of Barcelona, Barcelona, Spain, 9 Moss Landing Marine Labs at San Jose State University, Moss Landing, CA, United States, 10 Sea Mammal Research Unit, University of St. Andrews, Scotland, United Kingdom, 11 Akkeshi Marine Station, Field Science Center for Northern Biosphere, Hokkaido University, Akkeshi, Japan, 12 Rothamsted Research North Wyke, Okehampton, United Kingdom, 13 Centre D’Etudes Biologiques de Chizé, La Rochelle Université, UMR7372, CNRS, France, 14 Department of Biology, University of Southern Denmark, Odense, Denmark Keywords: bio-logging, bio-telemetry, physiology, heart rate, accelerometers, welfare, conservation Edited and reviewed by: INTRODUCTION George E. Billman, The Ohio State University, The field of bio-sensing refers to studies where the physiology of an animal, its behavior and United States movement, as well as the characteristics of the environment it moves in, is measured either by *Correspondence: electronic sensor-carrying devices that store the data (bio-logging), or those that transmit the data Andreas Fahlman directly (bio-telemetry).1 One of the first bio-sensing studies was conducted over 80 years ago with afahlman@whoi.edu the attachment of a capillary tube to a fin whale (Balaenoptera physalus) to assess the dive depth of a free-ranging marine mammal (Scholander, 1940). In humans, the stethoscope was developed Specialty section: by Rene Laennec in 1819 as the first non-invasive heart monitor, which solved the challenge of This article was submitted to listening to the heart by placing an ear on the patient’s chest (not always welcome in the Victorian Physio-logging, era) (Roguin, 2006). Quickly the system found new uses eventually leading to a shift from subjective a section of the journal Frontiers in Physiology to objective data about the internal body. The field of bio-sensing has since increased exponentially and revolutionized our understanding of animal ecology. With the technological development of Received: 18 February 2021 miniaturized sensors, numerous studies of movement ecology, behavior, and communication in a Accepted: 26 February 2021 Published: 30 March 2021 diverse range of animals (e.g., species of fish, reptiles, birds and mammals) have been reviewed in (Frost et al., 1997; Davis, 2008; Ropert-Coudert et al., 2009a; Rutz and Hays, 2009; Swain et al., Citation: 2011; Hussey et al., 2015; Wilmers et al., 2015; Endo and Wu, 2019; Börger et al., 2020; Wassmer Fahlman A, Aoki K, Bale G, Brijs J, Chon KH, Drummond CK, Føre M, et al., 2020). While determining the physiological limits and plasticity of a species is essential Manteca X, McDonald BI, for understanding its ecology and evolution, studies that measure the physiological responses McKnight JC, Sakamoto KQ, Suzuki I, of free-ranging animals (i.e., physio-logging) have not seen the same exponential increase, even Rivero MJ, Ropert-Coudert Y and though physiological questions were at the origin of the use of data loggers in seminal work Wisniewska DM (2021) The New Era done by field physiologists such as Gerry Kooyman, Paul Ponganis, Warren Zapol, and Patrick of Physio-Logging and Their Grand Butler (Butler and Woakes, 1979; Falke et al., 1985; Kooyman, 1985; Ponganis et al., 1991). Challenges. Front. Physiol. 12:669158. 1 Recent advances combine the logging and transmission of data using AI and machine learning approaches to process data doi: 10.3389/fphys.2021.669158 on-board the logger and transmit either subsets of data or information derived from the primary data recorded. Frontiers in Physiology | www.frontiersin.org 1 March 2021 | Volume 12 | Article 669158 Fahlman et al. New Era of Physio-Logging The slower growth of the physio-logging field could be due to difficult to assess the magnitude of potential confounding factors the commercial unavailability of physiological sensors, or that the such as stress or manipulation on the measured physiological available sensors were too large, based on static-technologies, or variable. In recent years, there has been a focus on measuring required specialized surgical training and extensive knowledge physiology in free-ranging animals. For example, trained animals of the anatomy and physiology of the animal for successful that are desensitized to the experimental procedures have been implantation. Despite these challenges, studies using bio-sensing used to study diving energetics, cardiorespiratory and vascular tools have renewed the interest in physio-logging and attempted physiology, and cerebrovascular physiology (Elsner, 1965; Olsen to understand the physiology of an animal through inference et al., 1969; Ridgway and Howard, 1979; Williams et al., 1993; from their behavior (Wilson et al., 2002; Hooker et al., 2009; Hurley and Costa, 2001; Fahlman et al., 2008, 2019, 2020a,b; Goldbogen et al., 2011, 2019b; Kolarevic et al., 2016; Føre et al., Mortola and Sequin, 2009; Rosen and Trites, 2013; Worthy et al., 2018b; Quick et al., 2020). 2013; Elmegaard et al., 2016, 2019; Takei et al., 2016; McKnight Physio-loggers have recently been used on farmed animals et al., 2019; Meir et al., 2019; Pedersen et al., 2020; Blawas et al., (livestock) to record physiological variables (e.g., body 2021). As bio-logging technologies have advanced, physiological temperature, respiration and heart rates) in order to monitor parameters such as heart rate, respiration rate, and blood O2 water intake, the occurrence of diseases, energy expenditure in have even been measured in free-ranging fish, reptiles, birds, and grazing activities, and effect of diet on body temperature under mammals (Falke et al., 1985; Ponganis et al., 1991; Thompson and cold and warm conditions (Brosh et al., 2006; Eigenberg et al., Fedak, 1993; Southwood et al., 1999; Andrews et al., 2000; Froget 2008; AlZahal et al., 2011; Arias et al., 2011; Aharoni et al., et al., 2004; Ropert-Coudert et al., 2006, 2009b; Meir et al., 2009; 2013; Cantor et al., 2018). In the human arena – where early bio- Yamamoto et al., 2009; Meir and Ponganis, 2010; McDonald and telemetry approaches were born – technological advances such as Ponganis, 2013, 2014; Sakamoto et al., 2013; Duriez et al., 2014; movement sensors initially allowed anyone with a “smartphone” Goldbogen et al., 2019a; McKnight et al., 2019, 2021a,b; Sumich, or “smartwatch” to assess their daily energy consumption, 2021). There is a parallel shift in the paradigm of physiological leading to the so-called “quantified health” movement (Scully monitoring of humans. Whereas once health monitoring was et al., 2012). Indeed, subsequent development of non-invasive exclusively a physician-based in-patient activity, the emergence sensing (photoplethysmography) enabled new and exciting of health and fitness wearables has led to the so-called “quantified possibilities to track health and fitness in a large number of self ” movement, where patients are producing data in support of people (Dörr et al., 2019; Seshadri et al., 2020). In addition, diagnostics (Patel and Tarakji, 2021). recent developments in wearable medical and nanotechnology, with increased battery life, storage capacity and a range of sensors have increased our ability to study physiological function TECHNOLOGICAL DEVELOPMENT both non-invasively and continuously over months and years (Kang et al., 2016; Kaidarova et al., 2018, 2019; Lee et al., 2019; Progress on medical sensing technology has increased Lazaro et al., 2020). Thus, tools capable of measuring a range significantly. A wide range of physiological monitoring of important and informative physiological parameters are now technologies are now available and are setting the stage from available, and are continuously being improved and adapted to which physiological bio-sensing could profit immensely. For work on an increasing range of species. These developments will instance, virtually anyone with a “smartphone” or “smartwatch” revolutionize the capacity to measure and assess the physiology can now assess their daily calorie expenditure as sensors within of animals and humans over extended periods of time, which the phone can estimate the number of steps taken or distance will allow a comprehensive evaluation of the physiological moved. Similarly, researchers have applied this principle to function of animals in their natural environment. This new free-ranging animals and are able to derive an estimate of era of physio-logging will enable long-term studies to better energy expended in the wild via a measure of dynamic body understand fundamental physiological function, health, welfare movements measured by animal-embarked accelerometers or well-being of animals and humans, as well as their responses (Wilson et al., 2006, 2020; Gleiss et al., 2011) that correlates to environmental and/or anthropogenic changes. well with other direct measures of energy expended even in wild animals (Elliott et al., 2013; Jeanniard-Du-Dot et al., 2017; Hicks et al., 2020). Phonospirometry (i.e., the use of the breath THE PARADIGM SHIFT CHALLENGE sound to estimate respiratory flow) is being used to perform lung function testing in both humans and animals (Sumich and Much of what we know about animal physiology has been May, 2009; Larson et al., 2012; Sumich, 2021; Van Der Hoop obtained by measuring physiological parameters on captive, et al., 2021). In addition, the ongoing development of wearable semi-captive, or restrained animals including measures of heart medical sensors that can detect glucose levels, estimate heart rate rate, blood flow, blood chemistry, blood gases, and metabolic via waterproof ECG electrodes (Reyes et al., 2014; Noh et al., rate (Berkson, 1967; Kooyman et al., 1970; Kooyman and 2016) or assess blood flow/volume changes and/or blood oxygen Campbell, 1972; Kooyman and Sinnett, 1982; Lutcavage et al., saturation changes provide a particularly exciting avenue for 1989; Ponganis et al., 1990; Reed et al., 1994, 2000; Gräns et al., future research (Bockstaele et al., 2014; McKnight et al., 2019, 2010; Kang et al., 2016; Brijs et al., 2018; Berenbrink, 2021; 2021a,b). These technological advancements open up enormous Svendsen et al., 2021). Unfortunately, in such situations, it is possibilities as they will enable investigating the physiological Frontiers in Physiology | www.frontiersin.org 2 March 2021 | Volume 12 | Article 669158 Fahlman et al. New Era of Physio-Logging function in freely moving, and even free-ranging animals, animals, largely focusing on describing where they go and with minimal disturbances. Further, the development of fully what they do there. Animal tracking studies have substantially bioresorbable microchip technologies capable of measuring a improved the knowledge of movement patterns and drivers of variety of physiological parameters (Kang et al., 2016) could offer movement in marine, terrestrial and avian species. However, opportunities to measure new, fine-scale physiological metrics in the rapid development and miniaturization of bio-sensing free-moving and free-ranging animals. Thus, long-term data sets electronics capable of measuring a raft of physiological variables on movement, married with physiological data could become present innovative and exciting tools that will revolutionize this available, contributing essential components to frameworks that field of research and usher in a new era of physio-logging. These assess the consequences of environmental and/or anthropogenic technologies will allow us to comprehensively evaluate how and impacts such as Population Consequences of Disturbance why animals make the journeys they do (e.g., bar-headed geese (PCoD, Booth et al., 2014; Pirotta et al., 2018), as well as to flying over the Himalayas, Cuvier’s beaked whales diving to develop a fundamental understanding of the physiology of a 3000 m for over 3 h; Hawkes et al., 2013; Quick et al., 2020). diverse range of species. Such studies will provide a foundation for understanding how animals may respond to alterations in the environment and the ANALYTICAL DEVELOPMENT physiological boundaries for survival. Physio-logging can also provide the necessary tools for conservation management, which The collection of long-term and/or high-resolution data sets will contribute toward reducing the impacts of anthropogenic is likely to result in analytical challenges. For example, ECG disturbances on species, communities and even ecosystems. collection sampled at 200 Hz over a whole year results in 6.3 For example, assessment of stress levels, such as measuring billion data points. While ECG could be reduced to instantaneous corticosterone or heart rate may help evaluate the impact of heart rate (if H ) (Sakamoto et al., 2021), normal statistical tools, anthropogenetic disturbance (Miksis et al., 2001). Furthermore, such as comparison of means or medians are not applicable and physio-logging is also likely to provide an important diagnostic are likely to result in erroneous conclusions. More sophisticated tool for evaluating the well-being and welfare of farmed terrestrial analytical methods, including signal processing or time-series and aquatic animals. These technologies can provide a unique analysis, will have to be developed and introduced to deal with opportunity for health monitoring via an “animal-eye” view a growing number of studies that focus on physiological function of the conditions that farmed animals experience in human and eco-physiology. There has recently been a rapid growth in care on a day-to-day basis, enabling a better understanding of analytical techniques in bioinformatics, where new tools and how to address the challenges faced by industries attempting databases have been developed to handle the large data sets that to produce a profitable, ethical and environmentally sustainable result from sequencing the genome of various species and to product (Berckmans, 2004; Føre et al., 2018a; Brijs et al., 2021). evaluate gene networks and differential changes in molecular Many of the responses evaluated in these managed settings products. A similar exponential growth has been seen within could also be translated to wild animals given the clear link data processing methods based on Artificial Intelligence (AI) between physiology and welfare (Gregory, 2004; Baird et al., and Machine Learning (ML). These methods are used in several 2016; Føre et al., 2018a; Svendsen et al., 2021). Finally, physio- different fields today, especially when data sets are too large logging is likely to promote improved health and wellness and/or complex to handle through conventional means, and it in humans, where early detection of disease allows improved is likely that they prove useful for processing datasets from bio- treatment outcome. sensors. Although many AI/ML methods are “a black box,” in the As we enter a new age in the study of physiology of sense that they do not describe the mechanistic links between animals and humans living in complex environments, the Physio- input and output (e.g., environmental and/or anthropogenic logging journal aims to provide a forum where scientists, and changes and sensor output in this case), they could be useful conservation practitioners among others, can share knowledge for compressing and condensing large data sets and identifying on how modern sensing technology and analytical approaches unknown relationships between inputs and measured features can be used to understand physiological function and health of (Rasheed et al., 2020). animals and humans. 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Sci. 51, 167–175. doi: 10.1071/AN10255 This is an open-access article distributed under the terms of the Creative Commons Takei, Y., Suzuki, I., Wong, M. K. S., Milne, R., Moss, S., Sato, K., et al. (2016). Attribution License (CC BY). The use, distribution or reproduction in other forums Development of an animal-borne blood sample collection device and its is permitted, provided the original author(s) and the copyright owner(s) are credited deployment for the determination of cardiovascular and stress hormones in and that the original publication in this journal is cited, in accordance with accepted phocid seals. Am. J. Physiol. Regul. Integr. Comp. Physiol. 311, R788–R796. academic practice. No use, distribution or reproduction is permitted which does not doi: 10.1152/ajpregu.00211.2016 comply with these terms. Frontiers in Physiology | www.frontiersin.org 6 March 2021 | Volume 12 | Article 669158