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Field Physiology: Studying Organismal Function in the Natural Environment

Cassondra L. Williams, Allyson G. Hindle

10.1002/cphy.c200005

Source: Volume 11, Issue 3, July 2021

Published online: June 2021

Full Article on Wiley Online Library



Abstract

Continuous physiological measurements collected in field settings are essential to understand baseline, free‐ranging physiology, physiological range and variability, and the physiological responses of organisms to disturbances. This article presents a current summary of the available technologies to continuously measure the direct physiological parameters in the field at high‐resolution/instantaneous timescales from freely behaving animals. There is a particular focus on advantages versus disadvantages of available methods as well as emerging technologies “on the horizon” that may have been validated in captive or laboratory‐based scenarios but have yet to be applied in the wild. Systems to record physiological variables from free‐ranging animals are reviewed, including radio (VHF/UFH) telemetry, acoustic telemetry, and dataloggers. Physiological parameters that have been continuously measured in the field are addressed in seven sections including heart rate and electrocardiography (ECG); electromyography (EMG); electroencephalography (EEG); body temperature; respiratory, blood, and muscle oxygen; gastric pH and motility; and blood pressure and flow. The primary focal sections are heart rate and temperature as these can be, and have been, extensively studied in free‐ranging organisms. Predicted aspects of future innovation in physiological monitoring are also discussed. The article concludes with an overview of best practices and points to consider regarding experimental designs, cautions, and effects on animals. © 2021 American Physiological Society. Compr Physiol 11:1979‐2015, 2021.

Keywords: physiology; free ranging; telemetry; datalogger; oxygen; heart rate; temperature

Figure 1. Figure 1. Methods of collecting physiological data from free‐living animals. An internal device (gray bar) or an external device with sensors attached (black bar) may (i) archive data in onboard memory for subsequent recovery (biologger) and (ii) transmit data over acoustic or VHF/UHF radio frequencies to a receiver (transmitter).
Figure 2. Figure 2. Five‐second ECG traces for a typical mammal (A), bird (B), and reptile (C) obtained using intravascular bipolar catheters or external subcutaneous electrodes. An ECG profile of a resting northern elephant seal from a bipolar pacing catheter inserted in the extradural vein (A) and sampled at 100 Hz, with the R‐R interval identified. ECG tracing from a diving emperor penguin recorded at 50 Hz using subcutaneous electrodes (B), demonstrating the inversion of the QRS complex in avian ECGs. An ECG tracing of a green marine turtle from a bipolar pacing catheter inserted in the jugular vein (C) and sampled at 50 Hz, illustrating the sinus venosus (SV) wave prior to the P wave. (D) ECG profile of a loggerhead turtle obtained using an intravascular bipolar catheter modified to collect ECG data. (E) ECG profile of loggerhead turtle obtained using external electrodes inserted subcutaneously. The gray areas in D and E indicate an interval when the turtle was moving. Data collected with the bipolar catheter was less sensitive to muscle artifact, with clear R peaks compared to external electrodes 342. This was particularly relevant during periods when the animal was moving; R peaks could not be identified during these periods when using external electrodes 342.
Figure 3. Figure 3. Heart rates of three terrestrial species under different conditions, illustrating biological insights gained from heart rate studies. (A) Heart rate of a fruit‐eating bat under three types of daily activities demonstrates a high natural scope of cardiovascular physiology in this species. Heart rate exceeded 800 beats/min during foraging and flying but dropped below 300 beats/min during episodes of bradycardia while resting during the day. Reprinted, with permission, from O'Mara MT, et al., 2017 218, CC BY 4.0, DOI: 10.7554/eLife.26686. (B and C) Heart rate profiles of a fox squirrel during disturbances while in captivity (B) and free‐ranging after release (C) indicate that experimental setting can profoundly affect physiology and responses. Heart rate increased during a disturbance while in captivity but decreased during a disturbance when in its natural environment. (B and C) Reprinted, with permission, from Smith EN and Johnson C, 1984 285 from Elsevier, Copyright 1984. Movement rate (D) and heart rate profile (E) of a black bear before, during, and after an unmanned aerial vehicle (UAV) flew overhead shows that responses may be detected in physiological measures that are not clear from behavioral measurements alone. Heart rate (E) increased in the presence of the UAV, even though there was no change in movement rate (D). (D and E) Reprinted, with permission, from Ditmer MA, et al., 2015 71 from Elsevier, Copyright 2015.
Figure 4. Figure 4. (A) EMG telemetry setup for measuring jaw muscle activity during feeding in wild mantled howlers 318. Electrodes placed in the masseter and temporalis muscles were attached to the telemetry unit contained in a jacket worn by the howler. Researchers within 100 m of the animal could start and stop recording and inspect EMG profiles during deployments via Bluetooth. This was an improvement over an earlier radio telemetry EMG device that recorded continuously, depleting the battery within 33 h 344. Reprinted, with permission, from Vinyard CJ, et al., 2012 318. (B) EMG data during tooth grinding by a resting howler using radio telemetry EMG. Reprinted, with permission, from Williams SH, et al., 2008 344, Springer Nature: Springer, International Journal of Primatology, Copyright, 2008.
Figure 5. Figure 5. EEG surface electrodes on owl head clipped of feathers (A) placed above specific brain areas (B) attached to a Neurologger (C) successfully recorded sleep and wakefulness in adult barn owls. (A, B, and C) Reprinted, with permission, from Scriba MF, et al., 2013 273, Springer Nature: Springer, Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, Copyright 2013. A flying great frigatebird carrying a Neurologger mounted on the head and a GPS tag attached to its back (D). To record EEG, epidural electrodes were placed above the hyperpallium of each hemisphere (E), which were attached to the logger shown as a black rectangle (E). Data collected during flight shows (F) acceleration of the head (sway, surge, and heave) on the top and left and right EEG activity below. The red arrow indicate an instance of apparent REM sleep. Wakefulness, characterized by low‐amplitude and high‐frequency waves, is enlarged in the green box. Red lines indicate wing flapping, and * indicates solitary high‐amplitude, slow waves. Unihemispheric sleep is shown in the blue box, with the EEG of the left hemisphere demonstrating continuous, high‐amplitude slow waves, characteristic of slow wave sleep. (D, E, and F) Reprinted, with permission, from Rattenborg NC, et al., 2016 251, CC BY 4.0, doi.org/10.1038/ncomms12468.
Figure 6. Figure 6. (A) A Weddell seal carrying two dataloggers to record skin surface heat flux (each logger recorded heat flux and temperature from two sites). This adult female carries heat flux sensors affixed to her head, neck, axilla, and flank 135. (B) Thermal image of an adult female Weddell seal carrying a datalogger recording digital ECG (the left‐side surface ECG electrode, secured by a neoprene patch, is visible in this image).
Figure 7. Figure 7. Polar endotherms experience dramatic regional temperature variation, making site selection key for experiments collecting temperature measurements. (A) Regional temperatures of Weddell seals at the surface and during diving range from near‐freezing skin surface temperatures 135 to relatively stable temperature in locomotory muscle 238. Core temperature, measured in the aorta, also fluctuates substantially during diving. Reused, with permission, from Hill RD, et al., 1987 131. (B) Mean regional temperatures measured in emperor penguins are high at rest (3 h measurements overnight) but range over 37.2 °C during diving 244. Modified, with permission, from Ponganis PJ, et al., 2003 244.
Figure 8. Figure 8. (A) The partial pressure of oxygen (PO2) and temperature were measured in the arterial, venous, and air sac systems of diving emperor penguins 222,270. Reprinted, with permission, from Ostrowski S, et al., 2003 222. (B) The Clark type PO2 electrode (Licox, Integra LifeSciences, Plainsboro, NJ, USA) and a thermistor (model 554; Yellow Springs Instruments, Yellow Springs, OH, USA) were connected by an underwater cable to a (C) microprocessor board (UFI, Inc., Morro Bay, CA, USA) within an underwater housing unit rated to 1000 m. (B and C) Adapted, with permission, from Ponganis PJ, et al., 2009 241. (D) Muscle O2 saturation was near zero in some dives near the aerobic dive limit of emperor penguins 317. (E) Measurements were made using a custom‐made near‐infrared spectroscopy (NIR) probe implanted on the pectoral muscle of diving emperor penguins that was attached to a (F) microprocessor board (UFI, Inc., Morro Bay, CA, USA) within an underwater housing unit rated to 1000 m 317. The NIR probe is identified in Panel F with a black rectangle. (D, E, and F) Reprinted, with permission, from Williams CL, et al., 2011 340.
Figure 9. Figure 9. pH logger and example of first pH recordings of a foraging albatross. (A) pH‐logging unit, from left to right, measured 11 cm length, contained in a titanium housing, with electronic on one side and a pressure equalization system on the other (far right). Reprinted from Peters G, 1997 233. (B) GPS tracks of 40 free‐ranging, foraging wandering albatrosses from Crozet archipelago with extensive foraging on the perimeter of the Crozet plateau (inset). Reprinted from Grémillet D, et al., 2012 111, CC‐BY, doi.org/10.1371/journal.pone.0037834.g001. (C) Stomach temperature and pH records from a wandering albatross at sea over a seven‐day period demonstrate extremely low stomach pH during a foraging trip. Reprinted from Grémillet D, et al., 2012 111, CC‐BY, doi.org/10.1371/journal.pone.0037834.g002.
Figure 10. Figure 10. (A) A baboon wearing form‐fitting backpack designed to carry telemetry equipment to record and transmit blood flow and blood pressure data in free‐ranging animals. Baboons appeared to tolerate the backpacks well and participated in routine activities with their troops for two or more weeks. Reprinted from Watson NW, et al., 1968 329. (B) The system, consisting of blood flowmeter, blood pressure sensor, FM telemetry system, remote control assembly, and anesthesia cartridge contained in backpacks. Transmitting different signals was used to remotely turn the system on or off, switch between vessels measured, stimulate the brain, or activate the anesthetic capsule to anesthetize the animal for recovery. Reprinted from Van Citters RL and Franklin D, 1969 313. (C) The blood pressure transducer. Modified from Sarazan RD and Schweitz KT, 2009 263. (D) After use with the baboons, pressure transducers were then implanted into the right carotid artery of free‐ranging giraffes. For transducer implantation, the vessel was isolated and then sutured around the exiting transducer cable. Reprinted from Van Citters RL and Franklin D, 1966 312. (E) The components were taken out of the backpack and wrapped around the giraffe's neck 315. Blood pressure was recorded during different activities of two free‐ranging giraffes, including galloping where blood pressure was 230/125 mmHg. The drop in blood pressure coincided with the giraffe's front feet hitting the ground. Reprinted, with permission, from Van Citters RL, et al., 1969 315.


Figure 1. Methods of collecting physiological data from free‐living animals. An internal device (gray bar) or an external device with sensors attached (black bar) may (i) archive data in onboard memory for subsequent recovery (biologger) and (ii) transmit data over acoustic or VHF/UHF radio frequencies to a receiver (transmitter).


Figure 2. Five‐second ECG traces for a typical mammal (A), bird (B), and reptile (C) obtained using intravascular bipolar catheters or external subcutaneous electrodes. An ECG profile of a resting northern elephant seal from a bipolar pacing catheter inserted in the extradural vein (A) and sampled at 100 Hz, with the R‐R interval identified. ECG tracing from a diving emperor penguin recorded at 50 Hz using subcutaneous electrodes (B), demonstrating the inversion of the QRS complex in avian ECGs. An ECG tracing of a green marine turtle from a bipolar pacing catheter inserted in the jugular vein (C) and sampled at 50 Hz, illustrating the sinus venosus (SV) wave prior to the P wave. (D) ECG profile of a loggerhead turtle obtained using an intravascular bipolar catheter modified to collect ECG data. (E) ECG profile of loggerhead turtle obtained using external electrodes inserted subcutaneously. The gray areas in D and E indicate an interval when the turtle was moving. Data collected with the bipolar catheter was less sensitive to muscle artifact, with clear R peaks compared to external electrodes 342. This was particularly relevant during periods when the animal was moving; R peaks could not be identified during these periods when using external electrodes 342.


Figure 3. Heart rates of three terrestrial species under different conditions, illustrating biological insights gained from heart rate studies. (A) Heart rate of a fruit‐eating bat under three types of daily activities demonstrates a high natural scope of cardiovascular physiology in this species. Heart rate exceeded 800 beats/min during foraging and flying but dropped below 300 beats/min during episodes of bradycardia while resting during the day. Reprinted, with permission, from O'Mara MT, et al., 2017 218, CC BY 4.0, DOI: 10.7554/eLife.26686. (B and C) Heart rate profiles of a fox squirrel during disturbances while in captivity (B) and free‐ranging after release (C) indicate that experimental setting can profoundly affect physiology and responses. Heart rate increased during a disturbance while in captivity but decreased during a disturbance when in its natural environment. (B and C) Reprinted, with permission, from Smith EN and Johnson C, 1984 285 from Elsevier, Copyright 1984. Movement rate (D) and heart rate profile (E) of a black bear before, during, and after an unmanned aerial vehicle (UAV) flew overhead shows that responses may be detected in physiological measures that are not clear from behavioral measurements alone. Heart rate (E) increased in the presence of the UAV, even though there was no change in movement rate (D). (D and E) Reprinted, with permission, from Ditmer MA, et al., 2015 71 from Elsevier, Copyright 2015.


Figure 4. (A) EMG telemetry setup for measuring jaw muscle activity during feeding in wild mantled howlers 318. Electrodes placed in the masseter and temporalis muscles were attached to the telemetry unit contained in a jacket worn by the howler. Researchers within 100 m of the animal could start and stop recording and inspect EMG profiles during deployments via Bluetooth. This was an improvement over an earlier radio telemetry EMG device that recorded continuously, depleting the battery within 33 h 344. Reprinted, with permission, from Vinyard CJ, et al., 2012 318. (B) EMG data during tooth grinding by a resting howler using radio telemetry EMG. Reprinted, with permission, from Williams SH, et al., 2008 344, Springer Nature: Springer, International Journal of Primatology, Copyright, 2008.


Figure 5. EEG surface electrodes on owl head clipped of feathers (A) placed above specific brain areas (B) attached to a Neurologger (C) successfully recorded sleep and wakefulness in adult barn owls. (A, B, and C) Reprinted, with permission, from Scriba MF, et al., 2013 273, Springer Nature: Springer, Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, Copyright 2013. A flying great frigatebird carrying a Neurologger mounted on the head and a GPS tag attached to its back (D). To record EEG, epidural electrodes were placed above the hyperpallium of each hemisphere (E), which were attached to the logger shown as a black rectangle (E). Data collected during flight shows (F) acceleration of the head (sway, surge, and heave) on the top and left and right EEG activity below. The red arrow indicate an instance of apparent REM sleep. Wakefulness, characterized by low‐amplitude and high‐frequency waves, is enlarged in the green box. Red lines indicate wing flapping, and * indicates solitary high‐amplitude, slow waves. Unihemispheric sleep is shown in the blue box, with the EEG of the left hemisphere demonstrating continuous, high‐amplitude slow waves, characteristic of slow wave sleep. (D, E, and F) Reprinted, with permission, from Rattenborg NC, et al., 2016 251, CC BY 4.0, doi.org/10.1038/ncomms12468.


Figure 6. (A) A Weddell seal carrying two dataloggers to record skin surface heat flux (each logger recorded heat flux and temperature from two sites). This adult female carries heat flux sensors affixed to her head, neck, axilla, and flank 135. (B) Thermal image of an adult female Weddell seal carrying a datalogger recording digital ECG (the left‐side surface ECG electrode, secured by a neoprene patch, is visible in this image).


Figure 7. Polar endotherms experience dramatic regional temperature variation, making site selection key for experiments collecting temperature measurements. (A) Regional temperatures of Weddell seals at the surface and during diving range from near‐freezing skin surface temperatures 135 to relatively stable temperature in locomotory muscle 238. Core temperature, measured in the aorta, also fluctuates substantially during diving. Reused, with permission, from Hill RD, et al., 1987 131. (B) Mean regional temperatures measured in emperor penguins are high at rest (3 h measurements overnight) but range over 37.2 °C during diving 244. Modified, with permission, from Ponganis PJ, et al., 2003 244.


Figure 8. (A) The partial pressure of oxygen (PO2) and temperature were measured in the arterial, venous, and air sac systems of diving emperor penguins 222,270. Reprinted, with permission, from Ostrowski S, et al., 2003 222. (B) The Clark type PO2 electrode (Licox, Integra LifeSciences, Plainsboro, NJ, USA) and a thermistor (model 554; Yellow Springs Instruments, Yellow Springs, OH, USA) were connected by an underwater cable to a (C) microprocessor board (UFI, Inc., Morro Bay, CA, USA) within an underwater housing unit rated to 1000 m. (B and C) Adapted, with permission, from Ponganis PJ, et al., 2009 241. (D) Muscle O2 saturation was near zero in some dives near the aerobic dive limit of emperor penguins 317. (E) Measurements were made using a custom‐made near‐infrared spectroscopy (NIR) probe implanted on the pectoral muscle of diving emperor penguins that was attached to a (F) microprocessor board (UFI, Inc., Morro Bay, CA, USA) within an underwater housing unit rated to 1000 m 317. The NIR probe is identified in Panel F with a black rectangle. (D, E, and F) Reprinted, with permission, from Williams CL, et al., 2011 340.


Figure 9. pH logger and example of first pH recordings of a foraging albatross. (A) pH‐logging unit, from left to right, measured 11 cm length, contained in a titanium housing, with electronic on one side and a pressure equalization system on the other (far right). Reprinted from Peters G, 1997 233. (B) GPS tracks of 40 free‐ranging, foraging wandering albatrosses from Crozet archipelago with extensive foraging on the perimeter of the Crozet plateau (inset). Reprinted from Grémillet D, et al., 2012 111, CC‐BY, doi.org/10.1371/journal.pone.0037834.g001. (C) Stomach temperature and pH records from a wandering albatross at sea over a seven‐day period demonstrate extremely low stomach pH during a foraging trip. Reprinted from Grémillet D, et al., 2012 111, CC‐BY, doi.org/10.1371/journal.pone.0037834.g002.


Figure 10. (A) A baboon wearing form‐fitting backpack designed to carry telemetry equipment to record and transmit blood flow and blood pressure data in free‐ranging animals. Baboons appeared to tolerate the backpacks well and participated in routine activities with their troops for two or more weeks. Reprinted from Watson NW, et al., 1968 329. (B) The system, consisting of blood flowmeter, blood pressure sensor, FM telemetry system, remote control assembly, and anesthesia cartridge contained in backpacks. Transmitting different signals was used to remotely turn the system on or off, switch between vessels measured, stimulate the brain, or activate the anesthetic capsule to anesthetize the animal for recovery. Reprinted from Van Citters RL and Franklin D, 1969 313. (C) The blood pressure transducer. Modified from Sarazan RD and Schweitz KT, 2009 263. (D) After use with the baboons, pressure transducers were then implanted into the right carotid artery of free‐ranging giraffes. For transducer implantation, the vessel was isolated and then sutured around the exiting transducer cable. Reprinted from Van Citters RL and Franklin D, 1966 312. (E) The components were taken out of the backpack and wrapped around the giraffe's neck 315. Blood pressure was recorded during different activities of two free‐ranging giraffes, including galloping where blood pressure was 230/125 mmHg. The drop in blood pressure coincided with the giraffe's front feet hitting the ground. Reprinted, with permission, from Van Citters RL, et al., 1969 315.
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Further Reading
 1.Andrews RD, Enstipp MR. Diving physiology of seabirds and marine mammals: Relevance, challenges and some solutions for field studies. Comp Biochem Physiol Part A Mol Integr Physiol 202: 38‐52, 2016.
 2.Cooke SJ, Brownscombe JW, Raby GD, Broell F, Hinch SG, Clark TD, Semmens JM. Remote bioenergetics measurements in wild fish: Opportunities and challenges. Comp Biochem Physiol Part A Mol Integr Physiol 202: 23‐37, 2016.
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 4.Goldstein DL, Pinshow B. Taking physiology to the field: Using physiological approaches to answer questions about animals in their environments. Physiol Biochem Zool 79: 237‐241, 2006.
 5.Wilson AD, Wikelski M, Wilson RP, Cooke SJ. Utility of biological sensor tags in animal conservation. Conserv Biol 29: 1065‐1075, 2015.

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Article Title: Field Physiology: Studying Organismal Function in the Natural Environment
 

How to Cite

Cassondra L. Williams, Allyson G. Hindle. Field Physiology: Studying Organismal Function in the Natural Environment. Compr Physiol 2021, 11: 1979-2015. doi: 10.1002/cphy.c200005