skip to main content


Title: Advances in thermal physiology of diving marine mammals: The dual role of peripheral perfusion
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.  more » « less
Award ID(s):
1644256
NSF-PAR ID:
10299590
Author(s) / Creator(s):
; ;
Date Published:
Journal Name:
Temperature
ISSN:
2332-8940
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Mechanistic approaches for predicting the ranges of endotherms are needed to forecast their responses to environmental change. We test whether physiological constraints on maximum metabolic rate and the factor by which endotherms can elevate their metabolism (metabolic expansibility) influence cold range limits for mammal and bird species. We examine metabolic expansibility at the cold range boundary (MECRB) and whether species’ traits can predict variability in MECRBand then use MECRBas an initial approach to project range shifts for 210 mammal and 61 bird species. We find evidence for metabolic constraints: the distributions of metabolic expansibility at the cold range boundary peak at similar values for birds (2.7) and mammals (3.2). The right skewed distributions suggest some species have adapted to elevate or evade metabolic constraints. Mammals exhibit greater skew than birds, consistent with their diverse thermoregulatory adaptations and behaviors. Mammal and bird species that are small and occupy low trophic levels exhibit high levels of MECRB. Mammals with high MECRBtend to hibernate or use torpor. Predicted metabolic rates at the cold range boundaries represent large energetic expenditures (>50% of maximum metabolic rates). We project species to shift their cold range boundaries poleward by an average of 3.9° latitude by 2070 if metabolic constraints remain constant. Our analysis suggests that metabolic constraints provide a viable mechanism for initial projections of the cold range boundaries for endotherms. However, errors and approximations in estimating metabolic constraints (e.g., acclimation responses) and evasion of these constraints (e.g., torpor/hibernation, microclimate selection) highlight the need for more detailed, taxa‐specific mechanistic models. Even coarse considerations of metabolism will likely lead to improved predictions over exclusively considering thermal tolerance for endotherms.

     
    more » « less
  2. Penguins are the only extant family of flightless diving birds. They currently comprise at least 18 species, distributed from polar to tropical environments in the Southern Hemisphere. The history of their diversification and adaptation to these diverse environments remains controversial. We used 22 new genomes from 18 penguin species to reconstruct the order, timing, and location of their diversification, to track changes in their thermal niches through time, and to test for associated adaptation across the genome. Our results indicate that the penguin crown-group originated during the Miocene in New Zealand and Australia, not in Antarctica as previously thought, and thatAptenodytesis the sister group to all other extant penguin species. We show that lineage diversification in penguins was largely driven by changing climatic conditions and by the opening of the Drake Passage and associated intensification of the Antarctic Circumpolar Current (ACC). Penguin species have introgressed throughout much of their evolutionary history, following the direction of the ACC, which might have promoted dispersal and admixture. Changes in thermal niches were accompanied by adaptations in genes that govern thermoregulation and oxygen metabolism. Estimates of ancestral effective population sizes (Ne) confirm that penguins are sensitive to climate shifts, as represented by three different demographic trajectories in deeper time, the most common (in 11 of 18 penguin species) being an increasedNebetween 40 and 70 kya, followed by a precipitous decline during the Last Glacial Maximum. The latter effect is most likely a consequence of the overall decline in marine productivity following the last glaciation.

     
    more » « less
  3. Abstract

    An animal’s daily use of time (their “diel activity”) reflects their adaptations, requirements, and interactions, yet we know little about the underlying processes governing diel activity within and among communities. Here we examine whether community-level activity patterns differ among biogeographic regions, and explore the roles of top-down versus bottom-up processes and thermoregulatory constraints. Using data from systematic camera-trap networks in 16 protected forests across the tropics, we examine the relationships of mammals’ diel activity to body mass and trophic guild. Also, we assess the activity relationships within and among guilds. Apart from Neotropical insectivores, guilds exhibited consistent cross-regional activity in relation to body mass. Results indicate that thermoregulation constrains herbivore and insectivore activity (e.g., larger Afrotropical herbivores are ~7 times more likely to be nocturnal than smaller herbivores), while bottom-up processes constrain the activity of carnivores in relation to herbivores, and top-down processes constrain the activity of small omnivores and insectivores in relation to large carnivores’ activity. Overall, diel activity of tropical mammal communities appears shaped by similar processes and constraints among regions reflecting body mass and trophic guilds.

     
    more » « less
  4. Synopsis Marine mammals exhibit some of the most dramatic physiological adaptations in their clade and offer unparalleled insights into the mechanisms driving convergent evolution on relatively short time scales. Some of these adaptations, such as extreme tolerance to hypoxia and prolonged food deprivation, are uncommon among most terrestrial mammals and challenge established metabolic principles of supply and demand balance. Non-targeted omics studies are starting to uncover the genetic foundations of such adaptations, but tools for testing functional significance in these animals are currently lacking. Cellular modeling with primary cells represents a powerful approach for elucidating the molecular etiology of physiological adaptation, a critical step in accelerating genome-to-phenome studies in organisms in which transgenesis is impossible (e.g., large-bodied, long-lived, fully aquatic, federally protected species). Gene perturbation studies in primary cells can directly evaluate whether specific mutations, gene loss, or duplication confer functional advantages such as hypoxia or stress tolerance in marine mammals. Here, we summarize how genetic and pharmacological manipulation approaches in primary cells have advanced mechanistic investigations in other non-traditional mammalian species, and highlight the need for such investigations in marine mammals. We also provide key considerations for isolating, culturing, and conducting experiments with marine mammal cells under conditions that mimic in vivo states. We propose that primary cell culture is a critical tool for conducting functional mechanistic studies (e.g., gene knockdown, over-expression, or editing) that can provide the missing link between genome- and organismal-level understanding of physiological adaptations in marine mammals. 
    more » « less
  5. Marine mammals such as northern elephant seals (NES) routinely experience hypoxemia and ischemia-reperfusion events to many tissues during deep dives with no apparent adverse effects. Adaptations to diving include increased antioxidants and elevated oxygen storage capacity associated with high hemoprotein content in blood and muscle. The natural turnover of heme by heme oxygenase enzymes (encoded by HMOX1 and HMOX2 ) produces endogenous carbon monoxide (CO), which is present at high levels in NES blood and has been shown to have cytoprotective effects in laboratory systems exposed to hypoxia. To understand how pathways associated with endogenous CO production and signaling change across ontogeny in diving mammals, we measured muscle CO and baseline expression of 17 CO-related genes in skeletal muscle and whole blood of three age classes of NES. Muscle CO levels approached those of animals exposed to high exogenous CO, increased with age, and were significantly correlated with gene expression levels. Muscle expression of genes associated with CO production and antioxidant defenses ( HMOX1 , BVR , GPX3 , PRDX1 ) increased with age and was highest in adult females, while that of genes associated with protection from lipid peroxidation ( GPX4 , PRDX6 , PRDX1 , SIRT1 ) was highest in adult males. In contrast, muscle expression of mitochondrial biogenesis regulators ( PGC1A , ESRRA , ESRRG ) was highest in pups, while genes associated with inflammation ( HMOX2 , NRF2 , IL1B ) did not vary with age or sex. Blood expression of genes involved in regulation of inflammation ( IL1B , NRF2 , BVR , IL10 ) was highest in pups, while HMOX1 , HMOX2 and pro-inflammatory markers ( TLR4 , CCL4 , PRDX1 , TNFA ) did not vary with age. We propose that ontogenetic upregulation of baseline HMOX1 expression in skeletal muscle of NES may, in part, underlie increases in CO levels and expression of genes encoding antioxidant enzymes. HMOX2 , in turn, may play a role in regulating inflammation related to ischemia and reperfusion in muscle and circulating immune cells. Our data suggest putative ontogenetic mechanisms that may enable phocid pups to transition to a deep-diving lifestyle, including high baseline expression of genes associated with mitochondrial biogenesis and immune system activation during postnatal development and increased expression of genes associated with protection from lipid peroxidation in adulthood. 
    more » « less