Introduction to the theme issue: Measuring physiology in free-living animals

Abstract

By describing where animals go, biologging technologies (i.e. animal attached logging of biological variables with small electronic devices) have been used to document the remarkable athletic feats of wild animals since the 1940s. The rapid development and miniaturization of physiologging (i.e. logging of physiological variables such as heart rate, blood oxygen content, lactate, breathing frequency and tidal volume on devices attached to animals) technologies in recent times (e.g. devices that weigh less than 2 g mass that can measure electrical biopotentials for days to weeks) has provided astonishing insights into the physiology of free-living animals to document how and why wild animals undertake these extreme feats. Now, physiologging, which was traditionally hindered by technological limitations, device size, ethics and logistics, is poised to benefit enormously from the on-going developments in biomedical and sports wearables technologies. Such technologies are already improving animal welfare and yield in agriculture and aquaculture, but may also reveal future pathways for therapeutic interventions in human health by shedding light on the physiological mechanisms with which free-living animals undertake some of the most extreme and impressive performances on earth.

This article is part of the theme issue ‘Measuring physiology in free-living animals (Part I)’.

1. Introduction

The field of ‘biologging’ (i.e. animal attached logging of biological variables with small electronic devices) has revealed how species of wild animals undertake remarkable feats of athleticism that set the benchmark for vertebrate performance. In the aerial environment, this includes non-stop endurance migratory flights of over 11 000 km by bar-tailed godwits (Limosa lapponica [1]), extreme long-distance migrations of more than 100 000 km by Arctic terns (Sterna paradisaea [2]), high-altitude flights of over 6000 m altitude by bar-headed geese (Anser indicus [3–6]) and non-stop flights for more than 10 months of the year by common swifts (Apus apus [7]). Similar remarkable feats have been recorded in the aquatic realm, including dives beyond 500 m deep by emperor penguins (Aptenodytes forsteri [8]), dives beyond 2 km deep by elephant seals (Mirounga sp.) resulting in near total venous blood oxygen depletion [9–11] and dives to nearly 3 km deep [12] for over 3 h [13] by Cuvier's beaked whales (Ziphius cavirostris). These astonishing feats highlight the fact that not only is it important to conserve wildlife for aesthetic and ethical reasons [14], but also because these athletic species may help to highlight medical pathways and approaches for some of the greatest health challenges for humans, including hypoxia (e.g. strokes and heart attacks), diabetes and obesity. The inspiration for this theme issue came from animal biologists attending conferences of Extreme and Expedition Medics, where researchers were engaged in medical studies in similar ecosystems (e.g. high altitude, [15,16]). While a few recent studies have made use of medical technologies designed for humans to study the diving capacity of humans and seals [17,18], medical studies generally have access to, and use, a wider and more sophisticated range of technology than what is available in the animal tracking sphere. Thus, this may be a critical time to bring together animal biology and medical technology, so that future research can draw inspiration across disciplines.

While biologging has largely focused on describing where animals go, the field of ‘physiologging’ (i.e. animal attached logging of physiological variables such as heart rate, blood oxygen content, lactate, breathing frequency and tidal volume) can provide crucial insights into how and why animals make the journeys they do. Many of the most important research questions in ecology (e.g. how does the environment drive movement? what sensory information do animals use to navigate? how will wildlife cope with anthropogenic-driven climate change?) critically need these how and why questions to be answered. However, physiologging technologies have evolved much more slowly than biologging technologies, with cutting edge developments generally coming from individual laboratory groups or research projects. From the 1960s onwards, a revolution in microelectronics, sports wearable technologies, nano-sensor devices and portable medical diagnostics for humans has provided a fertile opportunity for a step change in the study of physiology in free-living animals, which does not seem to have been exploited. For example, in 1962, Leyland C. Clark (the inventor of the oxygen electrode) invented the ‘enzyme electrode’, which used electrochemical detection of an immobilized enzyme by a metal electrode to measure the concentrations of various substances [19]. These ‘biosensors' are now extremely small, can cost as little as 2 cents a test, and can be mass produced in millions of units via screen-printing [20,21]. In a total biosensor market worth more than $13 billion, approximately 85% of the market is now focused on the measurement of blood glucose for diabetes [22]. Yet, these technologies appear to have been almost entirely untapped by the animal biologging field. We therefore propose that a ‘second age of biologging’ has arrived, which will operate on the boundaries between the disciplines of animal biology, medicine, sports and engineering, and will enable researchers to answer important questions in eco-physiology. This theme issue was driven by the recognition that animal biology requires a step change in the available technology to answer big research questions, and that the fields of animal biology and sports medical wearables and technology should now be integrated. The theme issue is divided into three sections.

2. Part 1: the past

In the mid-twentieth century, scientists contrived to monitor movements of marine megafauna under natural conditions. For example, Archie Carr used styrofoam floats and helium-filled balloons to track the movement of green turtles in the open sea [23], Per Scholander deployed capillary tubes on a fin whale to measure their maximum dive depth [24], and Arthur DeVries attached a Tsurumi Seiki depth recorder on female Weddell seals to show that these animals could dive down to at least 350 m [25] (figure 1). Following on from the research by Arthur DeVries, Gerald Kooyman then designed and built a time-depth recorder for deployment on Weddell seals to demonstrate that these animals can dive even deeper, as individuals reached depths beyond 600 m and for longer than 40 min [37]. In fact, this particular study may have been the genesis of the field of measuring physiology in free-living animals [38]. In 2003, the first international symposium on such research was held in Tokyo, and a new term ‘Bio-logging’ was proposed by the organizing committee. Biologging has now come to be defined as the ‘investigation of phenomena in or around free-living organisms that are beyond the boundary of our visibility or experience’ [39]. Since then, a biologging symposium has been held every two to three years in several locations around the world. The field of biologging traditionally focused on technologies that allowed researchers to follow the movements of animals via satellite, which resulted in the successful tracking of a diverse range of terrestrial and marine animals [40,41]. However, the field of physiologging did not keep pace, possibly owing to the invasive and logistically demanding nature of physiological research [42] and the size of traditional logging devices that precluded smaller animals from being studied.

Figure 1.

Timeline of (top) electronic and microprocessor development from the 1940s to the present day; and (bottom) key events in the field of physiologging. (Online version in colour.)

3. Part II: the present state-of-the-art

Owing to the recent and rapid development of physiologging technologies, it is currently possible to monitor fine-scale physiological changes in free-living animals not only with custom-made biologging devices [43], but also with state-of-the-art miniaturized commercial technologies developed for use in humans [44] or for farmed terrestrial and aquatic animals (e.g. dairy cattle [45,46] and fishes [47,48]). For example, the portable and commercially available near infraRed spectroscopy data logging devices introduced in 2006 were originally designed for measuring muscle oximetry in sports athletes [49], but have now also been used to show anticipatory adjustments of blood flow prior to diving in seals [18,50,51]. A wide range of variables can be measured with current physiologging technologies, which includes heart rate [52–56], brain activity [57,58], tissue oxygenation [50,51], respiratory rhythms [59,60] and body temperature [61,62]. When measured simultaneously with other parameters (e.g. time, depth, altitude, etc.), these variables can provide substantial insights into how wild animals undertake their remarkable feats of athleticism.

In addition to investigating the eco-physiology of wild animals, studies of animals in managed care provide rich opportunities for developing physiologging technologies, validating sensors, developing automated analytical approaches, and for comprehensively understanding the physiological responses of farmed animals and their longer-term consequences. For example, the global aquaculture industry is valued at several hundred billion dollars and thus optimizing the health and mass gain of fishes and shellfish is of paramount importance. Consequently, tools to monitor aquatic animal movement and physiology have been developed to maximize yield [47,48]. Likewise, automated analysis of physiological and movement data from dairy cows can help to identify and treat lameness before milk production suffers [45]. Furthermore, measurements of physiological parameters in cetaceans that are housed in aquaria and research facilities provide an opportunity to validate algorithms and/or indices for use on free-living animals [59]. Emerging technologies using implanted biosensors with carbon nanotubes [36] or glue-on ‘marine skin’ devices [64] have not yet been able to make measurements of biological phenomena, but have paved the way for future research.

4. Part III: the future

At present, with few exceptions, the application of physiologging in wild animal research is generally restricted to a handful of laboratories that have in-house engineers designing custom-made devices for their studies [36,63,64]. By introducing the field of biologging to medical biotechnology and sports wearables, as well as technology used in managed animals (agriculture and aquaculture), the hope is that the field can be opened up to allow more researchers to ask the sorts of questions that are required to tackle the most important threats to wild animals (e.g. disease transmission, climate change, [65]). Moreover, because devices developed for the medical biotechnology, agricultural and sports industries are underlined by enormous market opportunity, they are generally better tested and thus have a lower failure rate (e.g. from leaking or breaking, to hardware and software failures). This means that animal researchers employing these technologies could get more accurate and reliable data over longer periods of time, which would undoubtedly improve wildlife management, threat mitigation and our understanding of species resilience. This would represent a considerable step forward for wild animal research [65,66]. At the same time, automated analytical and software approaches will increase the power of analyses while also transforming potentially complex physiologging technologies into more user-friendly systems [67]. This may also have the advantage of helping to alleviate some of the problems that can be encountered when processing the long-term and/or high-resolution datasets obtained with physiologging technologies (e.g. the sampling of an electrocardiogram signal at 200 Hz for an entire year would produce 6.3 billion data points) [68]. The development of small and robust devices for measuring the physiology of wild animals also represents an exciting engineering challenge that could be used in the microelectronics realm to drive device development and testing in a broader sense. Finally, lessons learned from how animals cope with extreme environments and undertake (at least what we perceive to be) extreme athletic feats may yield lessons for the treatment of human conditions [69,70]. For example, the study of hypoxia in high-flying birds has been of interest to medics studying ischemia and hypoxaemia in humans [71].

5. Concluding remarks

The study of free-living animals and wildlife continues to provide a rich ground for scientific discovery and technical development (e.g. the ICARUS global tracking initiative [72]). Excitingly, biologging and its sub-discipline physiologging are poised to greatly benefit from the rapid advancements in medical biotechnology and wearable biosensors. With an ever-increasing access to technologies capable of determining real-time physiological changes in free-living animals, a ‘second age of biologging’ has well and truly arrived for eco-physiologists. This age will undoubtedly create new and exciting opportunities for measuring biological phenomena in free-living animals. Such information will not only provide important information about basic function and physiology, but will be critical to predict how major forces such as disease and climate change may impact the performance, health and welfare of both individuals and populations of free-living animals.

Data accessibility

This article has no additional data.

Competing interests

We declare we have no competing interests.

Funding

We received no funding for this study.