Using heart rate and acceleration biologgers to estimate winter activity costs in free-swimming largemouth bass.

Winter is a critical period for largemouth bass (Micropterus nigricans) with winter severity and duration limiting their population growth at northern latitudes. Unfortunately, we have an incomplete understanding of their winter behaviour and energy use in the wild. More winter-focused research is needed to better understand their annual energy budget, improve bioenergetics models, and establish baselines to assess the impacts of climate warming; however, winter research is challenging due to ice cover. Implantable tags show promise for winter-focused research as they can be deployed prior to ice formation. Here, using swim tunnel respirometry, we calibrated heart rate and acceleration biologgers to enable estimations of metabolic rate (MO2) and swimming speed in free-swimming largemouth bass across a range of winter-relevant temperatures. In addition, we assessed their aerobic and swim performance. Calculated group thermal sensitivities of most performance metrics indicated the passive physicochemical effects of temperature, suggesting little compensation in the cold; however, resting metabolic rate and critical swimming speed showed partial compensation. We found strong relationships between acceleration and swimming speed, as well as between MO2 and heart rate, acceleration, or swimming speed. Jackknife validations indicated that these modeled relationships accurately estimate swimming speed and MO2 from biologger recordings. However, there were relatively few reliable heart rate recordings to model the MO2 relationship. Recordings of heart rate were high-quality during holding but dropped during experimentation, potentially due to interference from aerobic muscles during swimming. The models informed by acceleration or swimming speed appear to be best suited for field applications.

Body temperature patterns during pregnancy and parturition in moose.

Gestation and lactation have high energetic requirements. Up to three-fourths of the gestation period in moose (Alces alces) overlaps with the food-scarce period in winter. During this period, moose deal with the limited forage resources available through hypometabolism with decreased heart rate and body temperature (Tb). Body temperature is also an indicator of oestrus, pregnancy and parturition, which is well documented in several domestic species. In this study, we sought to determine if moose displayed a similar Tb pattern during pregnancy and parturition to domesticated ruminants, and if we could detect parturition by combining Tb and activity data. We studied the Tb pattern of 30 free-ranging adult female moose (≥1.5 years old), equipped with ruminal temperature loggers and GPS collars. We documented a 0.13-0.19°C higher Tb in pregnant compared to non-pregnant moose, depending on the study area with the Tb difference increasing along a south-north gradient, and a drop in Tb and in activity when parturition was imminent. Detection of parturition was highly successful when combining Tb and activity data with an accuracy of 91.5%. Our findings demonstrate that Tb responses to pregnancy and parturition in a wild capital-breeding ruminant are similar to those of domesticated ruminants.

Exploring relationships between oxygen consumption and biologger-derived estimates of heart rate in two warmwater piscivores.

Estimating metabolic rate in wild, free-swimming fish is inherently challenging. Here, we explored using surgically implanted heart rate biologgers to estimate metabolic rate in two warmwater piscivores, bowfin Amia calva (Linneaus 1766) and largemouth bass Micropterus salmoides (Lacepède 1802). Fish were surgically implanted with heart rate loggers, allowed to recover for 24 h, exposed to a netting and air exposure challenge, and then placed into respirometry chambers so that oxygen consumption rate (MO2 ) could be measured in parallel to heart rate (fH ) for a minimum of 20 h (ca. 20 estimates of MO2 ). Heart rate across the duration of the experiment (at 19°C) was significantly higher in largemouth bass (mean ± s.d., 45 ± 14 beats min-1 , range 18-86) than in bowfin (27 ± 9 bpm, range 16-98). Standard metabolic rate was also higher in largemouth bass (1.06 ± 0.19 mg O2  kg-1  min-1 , range 0.46-1.36) than in bowfin (0.89 ± 0.17 mg O2  kg-1  min-1 , range 0.61-1.28). There were weak relationships between fH and MO2 , with heart rate predicting 28% of the variation in oxygen consumption in bowfin and 23% in largemouth bass. The shape of the relationship differed somewhat between the two species, which is perhaps unsurprising given their profound differences in physiology and life history, illustrating the need to carry out species-specific validations. Both species showed some potential for a role of fH in efforts to estimate field metabolic rates, although further validation experiments with a wider range of conditions (e.g., digestive states, swimming activity) would likely help improve the strength of the MO2 -fH relationship for use in field applications.

Heart rates of Atlantic salmon Salmo salar during a critical swim speed test and subsequent recovery.

In this study, heart rate (HR) bio-loggers were implanted in the abdominal cavity of 12 post-smolt Atlantic salmon Salmo salar weighing 1024 ± 31 g and acclimated to 12°C sea water. One week after the surgical procedure, a critical swim speed (Ucrit ) test was performed on tagged and untagged conspecifics, whereafter tagged fish were maintained in their holding tanks for another week. The Ucrit was statistically similar between tagged and untagged fish (2.67 ± 0.04 and 2.74 ± 0.05 body lengths s-1 , respectively) showing that the bio-logger did not compromise the swimming performance. In the pre-swim week, a diurnal cycle was apparent with HR peaking at 65 beats min-1 during the day and approaching 40 beats min-1 at night. In the Ucrit test, HR increased approximately exponentially with swimming speed until a plateau was reached at the final speed before fatigue with a maximum of 85.2 ± 0.7 beats min-1 . During subsequent recovery tagged fish could be divided into a surviving group (N = 8) and a moribund group (N = 4). In surviving fish HR had fully recovered to pre-swim levels after 24 h, including reestablishment of a diurnal HR cycle. In moribund fish HR never recovered and remained elevated at c. 80 beats min-1 for 4 days, whereafter they started dying. We did not identify a proximal cause of death in moribund fish, but possible explanations are discussed. Tail beat frequency (TBF) was also measured and showed a more consistent response to increased swimming speeds. As such, when exploring correlations between HR, TBF and metabolic rates at different swimming speeds, TBF provides better predictions. On the contrary, HR measurements in free swimming fish over extended periods of time are useful for other purposes such as assessing the accumulative burden of various stressors and recovery trajectories from exhaustive exercise.

Glucocorticoids and activity in free-living arctic ground squirrels: Interrelationships between weather, body condition, and reproduction.

The dynamic relationship between glucocorticoids and behavior are not well understood in wild mammals. We investigated how weather, body condition, and reproduction interact to affect cortisol levels and activity patterns in a free-living population of arctic ground squirrels (Urocitellus parryii). As a proxy for foraging and escape behaviors, collar-mounted accelerometers and light loggers were used to measure above-ground activity levels and the amount of time squirrels spent below the surface, respectively. Fecal cortisol metabolites (FCMs) were quantified to assess glucocorticoid secretion in squirrels. Male and female squirrels differed in above-ground activity levels and time spent below-ground across the active season, with males being most active during mating and females most active during lactation. We also found that female, but not male, squirrels exhibited seasonal variation in FCM levels, with concentrations highest during mid-lactation and lowest after the lactation period. In female squirrels, the seasonal relationships between breeding stage, activity, and FCM levels were also consistent with changes in maternal investment and the preparative role that glucocorticoids are hypothesized to play in energy mobilization. Body condition was not associated with FCM levels in squirrels. As predicted, deteriorating weather also influenced FCM levels and activity patterns in squirrels. FCM concentrations were affected by an interaction between temperature and wind speed when seasonal temperatures were lowest. In addition, above-ground activity, but not time spent below-ground, positively correlated with FCM levels. These results suggest that, although ground squirrels avoid inclement weather by remaining below-ground, activation of the stress axis may stimulate foraging activity.

Temperature and depth profiles of Chinook salmon and the energetic costs of their long-distance homing migrations.

River warming poses an existential threat to many Pacific salmon (Oncorhynchus spp) populations. However, temperature-mediated risks to salmon are often complex and addressing them requires species- and population-specific data collected over large spatial and temporal scales. In this study, we combined radiotelemetry with archival depth and temperature sensors to collect continuous thermal exposure histories of 21 adult spring- and summer-run Chinook salmon (O. tshawytscha) as they migrated hundreds of kilometers upstream in the Columbia River basin. Salmon thermal histories in impounded reaches of the Columbia and Snake rivers were characterized by low daily temperature variation but frequent and extensive vertical movements. Dives were associated with slightly cooler salmon body temperatures (~ 0.01 to 0.02 °C/m), but there was no evidence for use of cool-water thermal refuges deep in reservoirs or at tributary confluences along the migration route. In tributaries, salmon were constrained to relatively shallow water, and they experienced ~ 2-5 °C diel temperature fluctuations. Differences in migration timing and among route-specific thermal regimes resulted in substantial among-individual variation in migration temperature exposure. Bioenergetics models using the collected thermal histories and swim speeds ranging from 1.0 to 1.5 body-lengths/s predicted median energetic costs of ~ 24-40% (spring-run) and ~ 37-60% (summer-run) of initial reserves. Median declines in total mass were ~ 16-24% for spring-run salmon and ~ 19-29% for summer-run salmon. A simulated + 2 °C increase in water temperatures resulted in 4.0% (spring-run) and 6.3% (summer-run) more energy used per fish, on average. The biotelemetry data provided remarkable spatial and temporal resolution on thermal exposure. Nonetheless, substantial information gaps remain for the development of robust bioenergetics and climate effects models for adult Chinook salmon.

Importance of the coronary circulation for cardiac and metabolic performance in rainbow trout (Oncorhynchus mykiss).

Cardiac oxygenation is achieved via both coronary arterial and luminal venous oxygen supply routes in many fish species. However, the relative importance of these supplies for cardiac and aerobic metabolic performance is not fully understood. Here, we investigated how coronary artery ligation in rainbow trout (Oncorhynchus mykiss), implanted with heart rate loggers, affected cardiorespiratory performance in vivo While coronary ligation significantly elevated resting heart rate, the standard metabolic rate was unchanged compared to sham-treated controls. However, coronary ligation reduced the maximum metabolic rate while heart rate remained unchanged following enforced exercise. Thus, coronary ligation reduced metabolic and heart rate scopes by 29% and 74%, respectively. Our findings highlight the importance of coronary oxygen supply for overall cardiorespiratory performance in salmonid fish, and suggest that pathological conditions that impair coronary flow (e.g. coronary arteriosclerosis) constrain the ability of fish to cope with metabolically demanding challenges such as spawning migrations and environmental warming.

A field test of the use of pop-off data storage tags in freshwater fishes.

In the present study, pop-off data storage tags (pDST) without any transmitting capabilities were attached to 118 adult salmonids in a 19 000 km2 freshwater system (Lake Ontario). The 9·3 cm long cylindrical tags were externally attached to fishes using a backpack-style harness, set to record pressure (dBar ≈ depth in m) and temperature every 70 s (and at some key times, every 5 s) and programmed to release from the harness and float to the surface after c. 1 year. Recapture of the bright-orange tags for data retrieval relied on members of the public finding tags on shore, or on anglers capturing fishes with tags attached and using the contact information displayed on each tag to mail tags to the research team in exchange for a monetary reward. Thirty-seven tags were found and returned from the 118 released (31%), while 26 of the 118 tags (22%) remained scheduled to pop-off in summer 2017. Of the 37 tags returned, 23 were from wild-caught fishes (out of 88 wild-caught and tagged fishes; 26%) and yielded useful data whereas 14 were from hatchery-reared fishes that were opportunistically tagged and appear to have been unable to acclimate to life in the wild and died days to weeks after release. The field study described here thus demonstrated that pDSTs can be a viable option for collecting large amounts of high-resolution depth and temperature data for salmonids in freshwater systems. Technical challenges, limitations and unknowns related to the use of pDSTs with freshwater fishes are discussed. In addition, pDSTs are compared with alternate electronic tagging technologies and assessed for their potential as a more widespread tool in research on freshwater fishes.

Integrating physiology, behavior, and energetics: Biologging in a free-living arctic hibernator.

The use of animal-borne instruments (ABIs), including biologgers and biotransmitters, has played an integral role in advancing our understanding of adjustments made by animals in their physiology and behavior across their annual and daily cycles and in response to weather and environmental change. Here, we review our research employing body temperature (Tb), light, and acceleration biologgers to measure patterns of physiology and behavior of a free-living, semi-fossorial hibernator, the arctic ground squirrel (Urocitellus parryii). We have used these devices to address a variety of physiological, ecological, and evolutionary questions within the fields of hibernation physiology, phenology, behavioral ecology, and chronobiology. We have also combined biologging with other approaches, such as endocrinology and tracking the thermal environment, to provide insights into the physiological mechanisms that underlie fundamental questions in biology including physiological performance trade-offs, timing and functional energetics. Finally, we explore the practical and methodological considerations that need to be addressed in biologging studies of free-living vertebrates and discuss future technological advancements that will increase the power and potential of biologging as a tool for assessing physiological function in dynamic and changing environments.

Thermal exposure of adult Chinook salmon in the Willamette River basin.

Radiotelemetry and archival temperature loggers were used to reconstruct the thermal experience of adult spring Chinook salmon (Oncorhynchus tshawytscha) in the highly regulated Willamette River system in Oregon. The study population is threatened and recovery efforts have been hampered by episodically high prespawn mortality that is likely temperature mediated. Over three years, 310 salmon were released with thermal loggers and 68 were recovered in spawning tributaries, primarily at hatchery trapping facilities downstream from high-head dams. More than 190,000 internal body temperature records were collected (mean ~2800 per fish) and associated with 14 main stem and tributary reaches. Most salmon experienced a wide temperature range (minima ~8-10 °C; maxima ~13-22 °C) and 65% encountered potentially stressful conditions (≥18 °C). The warmest salmon temperatures were in lower Willamette River reaches, where some fish exhibited short-duration behavioral thermoregulation. Cumulative temperature exposure, measured by degree days (DD) above 0 °C, varied more than seven-fold among individuals (range=208-1498 DDs) and more than two-fold among sub-basin populations, on average. Overall, ~72% of DDs accrued in tributaries and ~28% were in the Willamette River main stem. DD differences among individuals and populations were related to migration distance, migration duration, and salmon trapping protocols (i.e., extended pre-collection holding in tributaries versus hatchery collection shortly after tributary entry). The combined data provide spatially- and temporally-referenced information on both short-duration stressful temperature exposure and the biologically important total exposure. Thermal exposure in this population complex proximately influences adult salmon physiology, maturation, and disease processes and ultimately affects prespawn mortality and fitness. The results should help managers develop more effective salmon recovery plans in basins with marginal thermal conditions.

Evaluation of Post-Surgical Recovery in Olive Flounder (Paralichthys olivaceus) by Assessing Behavior, Heart Rate, and Wound Healing.

This study examined the post-surgery recovery of olive flounder (Paralichthys olivaceus) following tag insertion by analyzing behavior, heart rate, and wound healing. The experiments used 30 individuals (length: 38.67 ± 2.12 cm; weight: 742.48 ± 116.41 g). Heart rate was measured using a DST milli-HRT (Star-Oddi) bio-logger. To assess the influence of water temperature on the recovery process after surgical tag insertion, behavioral analyses, heart rate, and wound healing were conducted in two experimental groups: Experiment 1 (22 °C, optimal water temperature); Experiment 2 (28 °C, high water temperature); and control group (22 °C, non-operated fish). The experiment was repeated twice over a 7-day period for each experimental group. Compared to the non-operated fish, the operated fish exhibited stable levels after the 3rd to 4th day in Experiment 1. Statistical analyses based on heart rate in Experiment 1 indicated that the appropriate post-surgery recovery time point was approximately 3 days, representing the point at which behavioral fluctuations stabilized. In the case of Experiment 2, abnormal behavioral patterns (e.g., tilted swimming) and changes in average swimming time and daily heart rate were found to stabilize after 4 days post-surgery.

Ecological inference using data from accelerometers needs careful protocols.

Accelerometers in animal-attached tags are powerful tools in behavioural ecology, they can be used to determine behaviour and provide proxies for movement-based energy expenditure. Researchers are collecting and archiving data across systems, seasons and device types. However, using data repositories to draw ecological inference requires a good understanding of the error introduced according to sensor type and position on the study animal and protocols for error assessment and minimisation.Using laboratory trials, we examine the absolute accuracy of tri-axial accelerometers and determine how inaccuracies impact measurements of dynamic body acceleration (DBA), a proxy for energy expenditure, in human participants. We then examine how tag type and placement affect the acceleration signal in birds, using pigeons Columba livia flying in a wind tunnel, with tags mounted simultaneously in two positions, and back- and tail-mounted tags deployed on wild kittiwakes Rissa tridactyla. Finally, we present a case study where two generations of tag were deployed using different attachment procedures on red-tailed tropicbirds Phaethon rubricauda foraging in different seasons.Bench tests showed that individual acceleration axes required a two-level correction to eliminate measurement error. This resulted in DBA differences of up to 5% between calibrated and uncalibrated tags for humans walking at a range of speeds. Device position was associated with greater variation in DBA, with upper and lower back-mounted tags varying by 9% in pigeons, and tail- and back-mounted tags varying by 13% in kittiwakes. The tropicbird study highlighted the difficulties of attributing changes in signal amplitude to a single factor when confounding influences tend to covary, as DBA varied by 25% between seasons.Accelerometer accuracy, tag placement and attachment critically affect the signal amplitude and thereby the ability of the system to detect biologically meaningful phenomena. We propose a simple method to calibrate accelerometers that can be executed under field conditions. This should be used prior to deployments and archived with resulting data. We also suggest a way that researchers can assess accuracy in previously collected data, and caution that variable tag placement and attachment can increase sensor noise and even generate trends that have no biological meaning.

Seasonal patterns in behavior and glucocorticoid secretion of a specialist Holarctic tree squirrel (Sciurus aberti).

Seasonally breeding mammals must make constant adjustments in behavior and physiology to manage energetic trade-offs between survival and reproduction. Despite encountering high levels of climate and resource variability across the year, specialist Abert's squirrels (Sciurus aberti), lack the capacity to express hibernation or pronounced morphological adaptations to seasonality. Using accelerometer and GPS devices, we assessed how abiotic environmental factors, reproduction, and resource abundance influenced levels of activity and daily range size in a rural and food-supplemented suburban population of squirrels. We also quantified fecal cortisol metabolites (FCM) in squirrels to assess patterns of glucocorticoid secretion. While changes in weather predicted activity levels in both populations, seasonal variation in activity levels were reduced in food-supplemented compared to rural squirrels. In contrast to activity, daily range size was not affected by weather but was a better predictor of sex-specific reproductive investment. Comparisons between populations suggest that food-supplemented squirrels forage more efficiently within smaller areas. Across both sexes and populations, squirrels showed no sexual dimorphism in body size, no major patterns of seasonal weight change, and no associations between body mass and FCM concentrations; however, FCMs were lower in the food-supplemented compared to rural population during late-spring. Taken together, activity levels and FCM concentrations appear primarily influenced by weather and seasonal fluctuations in food availability, whereas daily range size reflects sexual asymmetries in seasonal reproductive investment. Overall, squirrels appear to rely largely on behavioral adjustments to cope with novel environmental heterogeneity, rather than changes in morphology or GC secretion.

Pigeon leadership hierarchies are not dependent on environmental contexts or individual phenotypes.

Remaining cohesive on the move can be beneficial for animal groups. As such, animal groups have evolved coordination mechanisms such as leadership to resolve navigational conflicts of interest. Consistent "leaders" may have an intrinsic advantage over "followers" which compromise on their preferred route to retain cohesion, which highlights the question of the inter-individual variation (phenotype) that can predict leadership. Studies in both birds and fish have revealed that intrinsically faster individuals can lead movements, and leading movements propagate from the front edge of the flock/shoal. However, these experiments are generally conducted in relatively "familiar" environments, where the degree of compromise between the "leaders" and "followers" is low. We suggested that inter-individual differences in route efficiency, while not explanatory of leadership from familiar locations, may emerge as predictors of leadership from unfamiliar locations. We tested this prediction - and the potential impact of multiple other behavioral, morphological and "in-flight" phenotypes on leadership - using two groups of homing pigeons (Columba livia) (N = 16), a classic model species of leadership. We recorded N = 966 unique GPS trajectories from birds in (i) solo and familiar, and (ii) solo and unfamiliar contexts to measure solo speed and solo route efficiency; and (iii) group and familiar, and (iv) group and unfamiliar contexts to assess group leadership. Pigeon leadership hierarchies were similar across environmental context (i.e., familiarity). However, we found that no covariates could consistently predict leadership score in either context.

Training in the Dark: Using Target Training for Non-Invasive Application and Validation of Accelerometer Devices for an Endangered Primate (Nycticebus bengalensis).

Accelerometers offer unique opportunities to study the behaviour of cryptic animals but require validation to show their accuracy in identifying behaviours. This validation is often undertaken in captivity before use in the wild. While zoos provide important opportunities for trial field techniques, they must consider the welfare and health of the individuals in their care and researchers must opt for the least invasive techniques. We used positive reinforcement training to attach and detach a collar with an accelerometer to an individual Bengal slow loris (Nycticebus bengalensis) at the Shaldon Wildlife Trust, U.K. This allowed us to collect accelerometer data at different periods between January-June 2020 and January-February 2021, totalling 42 h of data with corresponding video for validation. Of these data, we selected 54 min where ten behaviours were present and ran a random forest model. We needed 39 15-min sessions to train the animal to wear/remove the collar. The accelerometer data had an accuracy of 80.7 ± SD 9.9% in predicting the behaviours, with 99.8% accuracy in predicting resting, and a lower accuracy (but still >75% for all of them apart from suspensory walk) for the different types of locomotion and feeding behaviours. This training and validation technique can be used in similar species and shows the importance of working with zoos for in situ conservation (e.g., validation of field techniques).

Bears habituate to the repeated exposure of a novel stimulus, unmanned aircraft systems.

Unmanned aircraft systems (UAS; i.e. 'drones') provide new opportunities for data collection in ecology, wildlife biology and conservation. Yet, several studies have documented behavioral or physiological responses to close-proximity UAS flights. We experimentally tested whether American black bears (Ursus americanus) habituate to repeated UAS exposure and whether tolerance levels persist during an extended period without UAS flights. Using implanted cardiac biologgers, we measured heart rate (HR) of five captive bears before and after the first of five flights each day. Spikes in HR, a measure of stress, diminished across the five flights within each day and over the course of 4 weeks of twice-weekly exposure. We halted flights for 118 days, and when we resumed, HR responses were similar to that at the end of the previous trials. Our findings highlight the capacity of a large mammal to become and remain habituated to a novel anthropogenic stimulus in a relatively short time (3-4 weeks). However, such habituation to mechanical noises may reduce their wariness of other human threats. Also, whereas cardiac effects diminished, frequent UAS disturbances may have other chronic physiological effects that were not measured. We caution that the rate of habituation may differ between wild and captive animals: while the captive bears displayed large initial spikes in HR change (albeit not as large as wild bears), these animals were accustomed to regular exposure to humans and mechanical noises that may have hastened habituation to the UAS.

The utility of accelerometers to predict stroke rate in captive fur seals and sea lions.

The energy expenditure of free-living fur seals and sea lions is difficult to measure directly, but may be indirectly derived from flipper stroke rate. We filmed 10 captive otariids swimming with accelerometers either attached to a harness (Daily Diary: sampling frequency 32 Hz, N=4) or taped to the fur (G6a+: 25 Hz, N=6). We used down sampling to derive four recording rates from each accelerometer (Daily Diary: 32, 16, 8, 4 Hz; G6a+: 25, 20, 10, 5 Hz). For each of these sampling frequencies, we derived 20 combinations of two parameters (RMW, the window size used to calculate the running mean; and m, the minimum number of points smaller than a local maxima used to detect a peak) from the dynamic acceleration of x, z and x+z, to estimate stroke rate from the accelerometers. These estimates differed by up to ∼20% in comparison to the actual number of foreflipper strokes counted from videos. RMW and the choice of axis used to make the calculations (x, z or x+z) had little effect on the overall differences, though the variability was reduced when using x+z. The best m varied depending on the axis used and the sampling frequency; a larger m was needed for higher sampling frequencies. This study demonstrates that when parameters are appropriately tuned, accelerometers are a simple yet valid tool for estimating the stroke rates of swimming otariids.