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Advances in thermal physiology of diving marine mammals: The dual role of peripheral perfusion

Citation

Favilla, Arina; Horning, Markus; Costa, Daniel (2021), Advances in thermal physiology of diving marine mammals: The dual role of peripheral perfusion, Dryad, Dataset, https://doi.org/10.7291/D1M09M

Abstract

The ability to maintain a high core body temperature is a defining characteristic of all mammals, yet their diverse habitats present disparate thermal challenges that have led to specialized adaptations. Marine mammals inhabit a highly conductive environment. Their thermoregulatory capabilities far exceed our own despite having limited avenues of heat transfer. Additionally, marine mammals must balance their thermoregulatory demands with those associated with diving (i.e., oxygen conservation), both of which rely on cardiovascular adjustments. This review presents the progress and novel efforts in investigating marine mammal thermoregulation, with a particular focus on the role of peripheral perfusion. Early studies in marine mammal thermal physiology were primarily performed in the laboratory and provided foundational knowledge through in vivo experiments and ex vivo measurements. However, the ecological relevance of these findings remains unknown because comparable efforts on free-ranging animals have been limited. We demonstrate the utility of biologgers for studying their thermal adaptations in the context in which they evolved. Our preliminary results from freely diving northern elephant seals (Mirounga angustirostris) reveal blubber’s dynamic nature and the complex interaction between thermoregulation and the dive response due to the dual role of peripheral perfusion. Further exploring the potential use of biologgers for measuring physiological variables relevant to thermal physiology in other marine mammal species will enhance our understanding of the relative importance of morphology, physiology, and behavior for thermoregulation and overall homeostasis.

Methods

As one of the deepest diving pinnipeds, northern elephant seals (Mirounga angustirostris) are an ideal model species to study the thermal physiology of diving marine mammals. Translocating juvenile elephant seals from Año Nuevo State Park (San Mateo County, CA) has proven valuable for short at-sea studies using physiological biologgers that must be recovered (Oliver et al. 1998). Año Nuevo is ideally situated north of Monterey Bay, where the bathymetry allows for deep dives, similar to the average dives of adults (e.g., Costa et al. 2002, Maresh et al. 2014).

Juvenile elephant seals (1-2 years old) were sedated following standard protocols (Le Boeuf et al. 2000), instrumented, and transported to Monterey where they were released into the bay. The instruments were recovered to access the data stored onboard once the seals returned to land generally within 1 week.

In addition to a satellite tag and VHF transmitter to facilitate tracking and relocating the seal upon its return, the seals were equipped with two heat flux biologgers that measure diving depth, acceleration, water temperature and the following physiological variables: heat flux at four locations (neck, axilla, flank, swimming muscle), skin temperature, and the temperature gradient within the blubber layer with three subcutaneous thermistors. The heat flux biologgers were custom-built by Wildlife Computers (Redmond, WA) for a prior study on Weddell seals in Antarctica (Hindle et al. 2015) using heat flux sensors first validated for use in diving animals on Steller sea lions (Willis and Horning 2005). They were refurbished and reconfigured to integrate the subcutaneous thermistors for this project, which was necessary to investigate the underlying physiological mechanisms of their thermal responses while diving.

Heat flux was measured using small disc sensors (24.5 mm diameter, Concept Engineering, Old Saybrook, CT) that were attached to the seal’s shaved skin using custom-made PVC ring holders. A thin layer (1 mm) of a two-part thermally conductive epoxy (1.8 Wm-1K-1, Epo-Tek® T905BN, Epoxy Technology, Billerica, MA) was applied on the sensor which provides some adhesive quality after curing so that minimal superglue (Loctite Super Glue Gel Control) was used around the periphery of the PVC ring to ensure proper attachment. The sensor has directionality and was oriented on the seal such that positive heat flux indicates the animal is gaining heat and negative heat flux indicates the animal is losing heat. One of the four heat flux sensors also has an embedded thermistor to measure skin temperature at the flank. To account for the additional thermal resistance provided by the sensor itself and attachment mechanism, a correction factor was experimentally determined following Willis and Horning (2005) and used to multiply the raw voltage output. The manufacturer’s calibration constant was used to convert from mV to W m-2, and further corrections will be applied pending post-deployment calibrations.

Three thermistors (NTC 2.252kΩ at 25°C) were encapsulated in epoxy (Epo-Tek® 302-3M, Epoxy Technology, Billerica, MA) within stainless steel capillary tubes and connected to the biologgers with Kevlar® cable. To place the thermistors in the blubber layer, a small incision was made in the flank. A muscle biopsy cannula was used to create a channel where the thermistor was then inserted. A portable ultrasound (Philips Lumify L12-4 linear array transducer) was used to measure blubber depth prior to insertion and provided guidance while inserting the thermistors to the appropriate depths. The thermistor cable was secured using a box-stitch suture at the incision site. Antibiotics (1 g Cefazolin) were administered IV at deployment and recovery as a preventative measure, but there was no sign of infection in any of the seals.

Usage Notes

The files contain data from one juvenile northern elephant seal (male, 172 kg) whose trip at-sea was ~7 days. Two sections of data are provided with the variables listed below that were used to create the figures in Favilla et al. 2021 Temperature. All variables listed were sampled at 1 Hz.

Data-0502204000_0503083000.csv & Data-0508013000_0509013000.csv

Columns and relevant descriptions:

  • DateTime: GMT date and time
  • Depth: meters
  • WaterTemp: degrees Celsius, temperatures during surface interval (where the tag may have been out of the water) was corrected by replacing surface ‘air’ values with average value within top 2 meters
  • HeatFlux: W m2, corrected for additional thermal resistance from sensor and attachment mechanism and manufacturer’s calibration constant, measured at flank
  • BlubberDeep: degrees Celsius, thermistor placed near muscleblubber interface
  • BlubberMid: degrees Celsius, thermistor placed near the middle of the blubber layer
  • BlubberShallow: degrees Celsius, thermistor placed subcutaneously in blubber layer

DiveStat-No530_601.csv

Columns and relevant descriptions:

  • DiveNumber
  • StartTime: GMT date and time of dive start
  • MaxDepth: meters
  • DiveDuration: H:M:S, time elapsed between beginning of dive descent and end of ascent
  • SurfaceDuration: H:M:S, time elapsed between end of dive ascent and beginning of subsequent dive
  • SolarEl: degrees, solar elevation determined using geolocation and date and time
  • TimeOfDay: defined by SolarEl, where elevation > 0° is ‘Day’ and elevation ≤ 0° is ‘Night’