Public Release: 

A message from nature to muskrats: 'Don't chill out'

A comprehensive study finds that muskrats, unlike other aquatic mammals, receive no metabolic benefit from hypothermia.

American Physiological Society

San Diego, CA -- Muskrats are mainly vegetarians but will eat animals as well. These small animals consume about one-third of their weight every day. Their digestive system is designed for green vegetation. In the summer they eat the roots of aquatic plants. In the winter, they swim under the surface ice to get to the plants. To the distress of farmers, muskrats also eat agricultural crops.

Since muskrats forage underwater they should exhibit traits that maximize their breath-hold capacity. It is generally acknowledged that an animal's dive time is limited by finite on-board oxygen supply and that its aerobic dive limit (ADL) defines the maximum dive duration that can be supported by an oxygen-based metabolism (accessible body oxygen stores divided by the rate at which these stores are depleted underwater). In order to maximize time spent underwater, animals must acquire strategies that enhance their ADL, their capacity for recovery from diving, or their ability to continue diving beyond the ADL (i.e. their capacity for anaerobic metabolism).

One strategy that many assume the muskrat adopts for increased diving time is related to a well-established finding that a drop in temperature reduces rates of cellular reactions ("Q10 effect") and this phenomenon may account for the hypometabolic state of cooled tissues. Essentially, this effect depresses metabolism of cooled body tissues, thereby conserving energy. Cooling the body to increase diving time is known as "adaptive hypothermia" hypothesis.

A depression in diving metabolic rate (DMR) could partially explain the breath-hold capacity of some divers. Calculated DMR based on known body oxygen stores as well as diving patterns and behaviour, has been predicted to be equivalent to, or lower than resting metabolic rates in several penguin species (gentoo, king, emperor), as well as southern elephant seals. Since oxygen affinity of mammalian hemoglobin is typically increased in cold, a reduced sensitivity to temperature may serve to maintain the unloading of oxygen to cooled tissues during diving.

The semi-aquatic muskrat (Ondatra zibethicus) is an excellent model for investigating the adaptive hypothermia hypothesis, since it routinely cools during voluntary swimming and diving and apparently does not engage thermogenic pathways underwater. Both heart rate and Tb of muskrats decline during voluntary diving, and active rewarming via brown adipose tissue (BAT) does not appear to occur until surfacing. Given these observations, the researchers hypothesized that hypothermia in diving muskrats may enhance their dive performance by lowering diving metabolic rate.

The authors of "Does Natural Hypothermia Improve the Dive Performance of Muskrats?" are Allyson G. Hindle, Robert W. Senkiw, and Robert A. MacArthur, all from the Department of Zoology, University of Manitoba, Winnipeg, Manitoba. They will present their findings at "The Power of Comparative Physiology: Evolution, Integration and Application," an American Physiological Society (APS) meeting scheduled for August 24-28, 2002 at the Town & Country Hotel, San Diego, CA. To learn more about the program and presentations, log on to: http://www.the-aps.org/meetings/aps/san_diego/home.htm

Based on the premise that DMR is depressed with hypothermia, the research team predicted a parallel reduction in diving heart rate. Beat-to-beat changes in heart rate during submergence were also analyzed to determine if the pattern of bradycardia normally observed during diving is affected by hypothermia. To validate metabolic inferences derived from telemetered heart rate, concurrent measurements of (oxygen consumption) and heart rate were gathered for muskrats engaged in varying intensities of diving and surface activities.

Methodology

Muskrats were surgically implanted with either temperature-sensitive radio transmitters, or with electrocardiogram (ECG)/Tb transmitters. Rates of O2 consumption in the metabolic chamber were determined using a negative-pressure, open-circuit respirometry setup. Prior to dive trials, muskrats were placed in a "chilling tank" where they were immersed to a depth of 15 cm in 6 ± 1C water for up to one hour in order to induce mild hypothermia.

The experiments consisted of:

Experiment 1: Cost of Thermal Recovery from Chilling: This experiment enabled the quantification of post-immersion rewarming costs of hypothermic muskrats in the absence of diving. Average was determined, as it reflects the combined costs of recovery from chilling and post-immersion grooming and comfort movements within the metabolic chamber.

Experiment 2: Free Diving during Continuous Immersion: Pre-chilled and non-chilled muskrats were introduced into tanks where submerged screens prevented diving muskrats from surfacing at any point other than in a purpose-built metabolic chamber (14.6 L) situated at one end of the covered tank. Several behavioural indices of dive performance were measured during this aquatic phase, including dive frequency, average and total dive time, and dive: surface ratio (ratio of surface recovery time to duration of preceding dive).

Experiment 3: Dives of Controlled Duration: Pre-chilled or non-chilled control muskrats entered the water directly from the metabolic chamber and dive duration was controlled by blocking the entrance to the metabolic chamber once the muskrat had initiated a dive. Following each dive, muskrats were confined to the metabolic chamber and post-dive excess was calculated for that specific dive.

Experiment 4: Dive Trials on Juvenile Muskrats: Diving metabolic rates of normothermic and hypothermic juveniles were calculated in the same manner as for adults. However, due to time constraints associated with working on young, rapidly growing animals, juveniles did not participate in the same number of treatments as adults.

Experiment 5: Heart Rate During Diving and Post-Immersion Recovery: All eight adults instrumented with ECG/Tb transmitters participated in each "pre-chill" and "non-chill" trial. Three replicate trials assigned in random order were conducted on each subject to ensure the animal performed several long dives at each Tb.

Results

Pre-chilling elicited no overt behavioural changes to diving in adult muskrats. Both diving and average rates of oxygen consumption () of adults were unaffected by hypothermia when animals were tested in 30ºC water. However, significant interactions between water and body temperatures (Tb) were observed for diving (P = 0.045) and average (P = 0.040) , resulting in significantly higher (P = 0.045-0.017) values for hypothermic adults diving from the water surface in 10C water. Hypothermia reduced diving heart rate only in dives < 25 s (P = 0.007), and did not appear to affect the onset or temporal pattern of diving bradycardia. These study indicates that hypothermia does influence the dive response in a way that could potentially extend dive time through oxygen conservation.

However, the bradycardia response of hypothermic and normothermic muskrats quickly becomes indistinguishable as dive length increases. Consequently, the observed cardiac response to hypothermia was not strong enough to yield a relationship between mean diving heart rate and degree of pre-chilling (Tb). As well, heart rates of muskrats resting at the surface did not differ between hypothermic animals floating in cold (6ºC) water and normothermic animals resting in warm (30ºC) water. Presumably hypothermic muskrats experienced a greater vasoconstrictor response since abdominal Tb was lower. If so, failure to detect an attendant reduction in heart rate implies muskrats may readily tolerate hypertension during immersion.

Conclusions

This study documented few behavioural or metabolic changes in dive performance related to hypothermia in adult muskrats. While implying there is no energetic benefit to muskrats diving with a reduced Tb, this finding also suggests an impressive resistance to the effects of hypothermia in these animals. An elevation in average for hypothermic individuals implies that adult muskrats may defer rewarming to surface intervals.

The overriding conclusion to emerge from this study is that hypothermia in muskrats exerts a negligible effect on dive performance, as it influences neither submergence nor post-immersion metabolic costs.

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The American Physiological Society (APS) is one of the world's most prestigious organizations for physiological scientists. These researchers specialize in understanding the processes and functions by which animals live, and thus ultimately underlie human health and disease. Founded in 1887 the Bethesda, MD-based Society has more than 10,000 members and publishes 3,800 articles in its 14 peer-reviewed journals each year.

EDITOR'S NOTE: For further information or to schedule an interview, contact Donna Krupa at 703.967.2751 (cell), or at the APS Newsroom at: 619.908.5069 or 619.291.7131 ext. 3941, or by email at djkrupa1@aol.com. To view the program and abstracts, log on to http://www.the-aps.org/meetings/aps/san_diego/CP2002%20PROGRAM.PDF.

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