Introduction

Biotelemetry devices (“biologgers”) can monitor behavioral and physiological indicators of welfare status in real time, and couple these data with precise information about environmental context (Brown et al. 2013). Biologgers consist of a suite of sensors attached to an animal. The different sensors typically record location, motion, or other biological and environmental features multiple times a day (Cooke et al. 2004). The data collection is remote, meaning that the human observer does not operate in the field except to capture the animals and attach the devices. 

In one such study, ornithologists outfitted a female white-tailed sea eagle (Haliaeetus albicilla) with a biologger that recorded her movement, circadian rhythm, behavioral profile, and body temperature (Krone et al. 2009). In this article, I use this case study to illustrate biotelemetry’s potential to offer insights on wild animals’ welfare. 

The biologger in this case comprised two radio transmitters, a battery pack, and sensors monitoring location, temperature, vertical motion, and horizontal motion. (Figure 1). At 170 g, the device weighed 3.5% as much as the eagle. The study ended after only five months when the eagle unexpectedly died.

As with many biotelemetry studies, this one focused on a rare species (the white-tailed sea eagle) and collected data to inform its conservation.  Although welfare was not the focus of the project, it nonetheless proved data highly relevant to individual welfare because it documented the eagle’s dying process in unprecedented detail. This illustrates how biologgers could be used to understand the welfare burdens of different causes of death.

Welfare-relevant conclusions from biotelemetry

Cause of death

GPS data enabled the researchers to identify both the immediate cause of death and the broader environmental context for it.

Because the biologger transmitted location data every 5 minutes, the researchers were able to determine the precise time and location of the eagle’s death and to recover her corpse as soon as possible — overcoming major challenges in cause-of-death research. Through necropsy, they determined she died of lead poisoning (Krone et al. 2009).

Because the data stream was continuous for 5 months, there was strong evidence that  the eagle had ingested lead while foraging within her territory. Even though the eagle had a high-quality habitat that was protected in a conservation reserve, she was still at risk of lead exposure because of legal hunting in her environment (Krone et al. 2009).

Welfare while dying

The biologger fitted to this eagle also included accelerometers, which provided a high-resolution behavioral profile. Activity readings were taken 8 times per second for the entire duration of the study. This frequency enabled researchers to characterize the eagle’s usual circadian rhythm, as well as the start of her sickness period and her dying period. The sickness and dying periods each lasted 11 days (Krone et al. 2009).

With an understanding of the animal’s typical daily rhythms, it was clear when she started showing abnormal behaviors that indicated disease: changes to the timing of flight and rest and increases in the frequency of rest periods (Veissier et al. 1989, Scheibe et al. 1999). The eagle eventually ceased all activity. This extreme lethargy signalled the beginning of her dying process (Krone et al. 2009). Her body temperature also dropped a total of 15℃, coinciding with the decreases in activity (Krone et al. 2009). This physiological and behavioral profile provides a basis for inferring welfare status during the dying process (Figure 2).

I compared the eagle’s behavioural and physiological profiles over time to her baseline readings in order to estimate her mental state (Beausoleil et al. 2018). Although it may be hard to ever know with certainty how physiological conditions relate to subjective feelings in other species, we can make reasonable guesses given similarities between our own and other animals’ needs. 

The eagle’s lethargy could be associated with negative feelings of malaise. The sickness and dying phases spanned 22 days, so the eagle would have also had increasing feelings of hunger, as she was not eating during this time (Mellor and Beausoliel 2015). The necropsy showed total depletion of fat reserves (Krone et al. 2009). Since eagles eagles ideally eat about 5% of their body weight daily to maintain peak body condition, (Fevold and Craighead 1958), it is reasonable to assume that this loss of reserves and lack of hunting activity would lead to feelings of severe hunger and discomfort. Lastly, the 15º C drop in body temperature would likely lead to extreme discomfort associated with coldness (Mellor and Beausoliel 2015).

Advantages of biologgers for wild animal welfare studies

Recovering corpses

For studying death in the wild, the traditional methods such as short-duration video or corpse-recovery surveys have well-known limitations. Corpses are encountered by chance (Dell et al. 2014). Most are not recovered because they are decomposed or scavenged, making it incredibly difficult to estimate the relative frequencies of different causes of death in a population (Tavecchia et al. 2011). 

Biotelemetry has major advantages for cause-of-death research because it provides detailed information on when and where animals die (Klaassen et al. 2014). As a result, most of the deaths can be attributed to a specific cause (Figure 3). The positional data can also help researchers rapidly and systematically recover corpses (Calvete et al. 2002).

Knowing the prevalence and severity of different causes of death is important, because the amount of suffering that an animal experiences while dying is largely determined by the cause and manner of death (Beausoleil et al. 2016). Vehicle collisions, hunting with firearms, or electrocution may cause near-instantaneous death, whereas disease, starvation, or intoxication may weaken the animal over an extended period (22 days in our eagle case study). 

Beyond simply identifying the cause of death, comparative studies could allow us to infer the experiences of animals that die from different causes, and how the prevalence of these causes varies by life stage or environment. Such knowledge would allow wild animal welfare advocates to prioritize preventing the most painful manners of death.

Observing behavior

Currently, most welfare assessments are done by in-person human observation (Bailey et al. 2018). But biotelemetry allows continuous data collection from almost any location an animal may occupy — even where people cannot follow (Ropert-Coudert and Wilson 2005).

The ability to record quantitative behavioral profiles anywhere the animal goes allows for much more informed welfare estimates. For example, behavioral profiles can show sickness behaviors or other abnormal trends in function and condition (Brown et al. 2013, Adelman et al. 2014). This multidimensional information allows us to understand an animal’s welfare status in the context of events and environmental variables that matter at the scale of an individual’s preferences and perceptions (Bisson et al. 2009, Martins et al. 2014, McClune et al. 2015, Clemente al. 2016).

Observing community interactions

Because biologgers minimally distort behavior and can transmit data from any location, they are particularly well-suited to observing individuals’ interactions with their communities. For example, animals in different environments could be monitored as they cope with the various habitats that they encounter. This analysis would provide an animal’s-eye view on habitat quality and show to what extent an animal’s welfare might be improved or diminished by altering the environment (Lima and Zollner 1996, Nicol et al. 2020).  

By pairing biotelemetry with an understanding of community interactions, it may be possible to show how community structure degrades or enhances the average welfare of each animal community-member. For example, in a community with two species that cooperate beneficially, biotelemetry could monitor the degree to which stress is reduced when animals have the opportunity to interact (Hammers et al. 2019).  

Concerns about biotelemetry research

Technological limitations

Cost is the largest barrier to scaling wildlife biotelemetry research. Devices typically range from hundreds to thousands of dollars per unit (Cooke et al. 2004). Because of the high cost, sample sizes of biotelemetry studies are typically insufficient to predict a welfare outcome before it occurs, even though the data itself is reflective of welfare status (Lindberg and Walker 2007, Costantini and Møller 2013, Naef-Daenzer and Grüebler 2014).

Additionally, while biologgers have been shrinking in size due to advances in battery technology, they are still most commonly only usable on larger animals (Cooke et al. 2004). Unless the weight barriers can be overcome, the vast majority of animals — small invertebrates — are impossible to study with biotelemetry. 

Among marine invertebrates, biotelemetry is generally only feasible for individuals weighing more than 400 g. If this threshold were decreased to 40 g, then ten times more species could be studied, as could larvae and juveniles (O’Dor 2002). In terrestrial insects, biotelemetry studies have been limited to a few large arthropods, such as locusts or hawkmoths. Insect biologgers usually weigh less than 1 g, but their battery life is 3 hours or less (Sato and Maharbiz 2010). This temporal limitation nearly eliminates the ability to research invertebrate welfare through biologgers.

Welfare harms

Biologgers harm the animals wearing them (Hawkins 2004). Death during the tagging process can occur either at capture, directly after release, or from physical attrition over the course of the study (Casas et al. 2015, Weiser et al. 2016, Lameris et al. 2018). For example, the eagle in our case study was caught with a noose, a particularly stressful and risky method for capturing birds (Kautz and Seamans et al. 1980). 

Even in cases with no tag-related mortality (for example, Goldsmith et al. 2017), the devices can have sublethal impacts such as exhaustion, injury, reduced body condition, and the disruption of social activities and pair bonding (Weiser et al. 2016, Brlík et al. 2020, Hamelin and James 2018, Lameris et al. 2018; but see Niles et al. 2010 which found no sublethal impacts). 

The eagle in our case study appeared to have no negative symptoms from the biologger (Krone et al. 2009). However, the authors noted several instances where the bird was at rest during abnormal periods of the day. The authors theorized that stresses such as hunters, tourists, inclement weather, or even sub-lethal lead exposures, may have disrupted the eagle (Krone et al. 2009). But back-mounted biologgers such as the one worn by this eagle (Figure 4) have been documented to cause significant drag that impairs flight (Irvine et al. 2007, Meyer et al. 2015). Therefore, the device itself could have periodically exhausted the bird and necessitated abnormal rest periods.  

Conclusions

Biotelemetry’s scientific applications are promising for wild animal welfare research. For example, biologgers can be used to understand the prevalence of different causes of death. Biologgers provide behavioral and physiological profiles at such an extraordinary level of detail that they can potentially be used to infer animals’ mental states. As this study illustrates, these details can be discovered not only throughout an animal’s life, but uniquely, during their sickness and dying process, potentially revealing important information about the harms associated with different causes of death. Finally, by linking physiological and behavioral data with precise location data, biotelemetry gives unprecedented insight into the links between animals and their environment in real time.

The shift from direct human observation to remote monitoring is not without costs to the animals themselves. Biologgers’ weight and drag is substantial, and there are many documented instances of welfare harms and tag-related deaths. Therefore, it remains unclear whether biologgers in their current forms are justifiable or necessary for conducting wild animal welfare research. We plan to conduct further work to identify the costs and benefits associated with biologgers, best practices for determining when such work is necessary (if ever), and what can be done (if anything) to eliminate welfare harms during remote monitoring studies.