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Benign neonatal deep hypothermia in rodents and its relations to hibernation

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The neonates of many rodent species survive deep hypothermia (T b?=?0-8??C). In key respects, this hypothermia is more akin to hibernation than was thought during much of the twentieth century, indicating that studies of neonatal hypothermia may usefully supplement studies of hibernation in understanding evolved tissue adaptations to near-freezing T b. To clarify evolutionary diversity in neonatal survival of deep hypothermia, neonates of six species or strains were subjected to a standardized procedure: exposure for 2.5?h to test T bs followed by autoresuscitation. Mus and Peromyscus differed dramatically, the lowest T b survived by all ages studied (3-10 days) being 7-8??C in Mus and 0-1??C in Peromyscus. There was, however, no evidence of intrageneric plasticity because feral and laboratory Mus were identical, and Peromyscus species with cold- and warm-climate distribution ranges were identical. When neonates survive deep hypothermia, a key question is whether the experience is benign, meaning neonates tolerate hypothermia. To test the benign nature of deep hypothermia, neonates of Peromyscus leucopus were exposed four times (3?h each) to T b?=?1-2??C when 3-10 days old; controls were same-sex siblings not hypothermia exposed. When 74 such sibling pairs were exposed after weaning to predation by screech owls, the hypothermia-treated and control siblings did not differ in which was caught first. Based on study of deaths in 253 sibling pairs prior to weaning while under parental care, parents cared for hypothermia-treated siblings as attentively as controls. The results indicate that the experience of multiple neonatal deep-hypothermic episodes is benign in P. leucopus.
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J Comp Physiol B (2017) 187:705–713
DOI 10.1007/s00360-017-1070-0
ORIGINAL PAPER
Benign neonatal deep hypothermia inrodents andits relations
tohibernation
RichardW.Hill1
Received: 1 September 2016 / Revised: 4 December 2016 / Accepted: 26 February 2017 / Published online: 27 March 2017
© Springer-Verlag Berlin Heidelberg 2017
Based on study of deaths in 253 sibling pairs prior to wean-
ing while under parental care, parents cared for hypother-
mia-treated siblings as attentively as controls. The results
indicate that the experience of multiple neonatal deep-
hypothermic episodes is benign in P. leucopus.
Keywords Body temperature· Daily torpor·
Heterothermy· Tolerance· Diversity· Predation
avoidance· Owl predation
Introduction
This paper focuses on mammalian hypothermia: a state in
which core body temperature (Tb) is distinctly lower than
the range of Tb typical of homeothermic thermoregulation.
More specifically, the paper focuses on deep hypothermia,
defined for purposes here to be core Tb = 0–8 °C.
It has long been known that the neonates of rodents
tolerate lower Tbs than the adults of their species (Adolph
1951). In fact, the early-age neonates of many rodent spe-
cies tolerate several hours of exposure to deep hypothermia
(even in some cases Tbs very close to freezing), recovering
spontaneously when rewarmed. Unfortunately, this neona-
tal tolerance to deep hypothermia became viewed as a phe-
nomenon fundamentally different from hibernation or daily
torpor in the twentieth century because neonates in deep
hypothermia were generally thought then to be anoxic. In a
series of influential papers published in the 1940s to 1960s,
Adolph and colleagues concluded that the heart stops
beating during neonatal deep hypothermia (Adolph 1951,
1963). Because inhalation and exhalation stop (Adolph
1963; Hill 2000; Tattersall and Milsom 2003), the belief
that circulation also stops seemed to create a definitive case
that the tissues became anoxic, and discussions of neonatal
Abstract The neonates of many rodent species survive
deep hypothermia (Tb = 0–8 °C). In key respects, this hypo-
thermia is more akin to hibernation than was thought dur-
ing much of the twentieth century, indicating that studies
of neonatal hypothermia may usefully supplement studies
of hibernation in understanding evolved tissue adaptations
to near-freezing Tb. To clarify evolutionary diversity in
neonatal survival of deep hypothermia, neonates of six spe-
cies or strains were subjected to a standardized procedure:
exposure for 2.5h to test Tbs followed by autoresuscitation.
Mus and Peromyscus differed dramatically, the lowest Tb
survived by all ages studied (3–10 days) being 7–8 °C in
Mus and 0–1 °C in Peromyscus. There was, however, no
evidence of intrageneric plasticity because feral and labo-
ratory Mus were identical, and Peromyscus species with
cold- and warm-climate distribution ranges were identical.
When neonates survive deep hypothermia, a key question is
whether the experience is benign, meaning neonates toler-
ate hypothermia. To test the benign nature of deep hypo-
thermia, neonates of Peromyscus leucopus were exposed
four times (3h each) to Tb = 1–2 °C when 3–10 days old;
controls were same-sex siblings not hypothermia exposed.
When 74 such sibling pairs were exposed after weaning
to predation by screech owls, the hypothermia-treated and
control siblings did not differ in which was caught first.
Communicated by F. van Breukelen.
This manuscript is part of the special issue Hibernation --Guest
Editors: Frank van Breukelen and Jenifer C. Utz.
* Richard W. Hill
hillr@msu.edu
1 Department ofIntegrative Biology, Michigan State
University, EastLansing, MI48824, USA
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... In more recent decades, comparative studies of the stages of development have become more detailed, and they have addressed a wide diversity of animals and levels of organization. To illustrate with a few examples, Hill (1976) detailed the radical changes in metabolic rate and thermoregulatory competence that take place as newborn mice (Peromyscus leucopus) mature to adulthood-including the remarkable fact (Hill 2017) that early-age nestlings employ apneic pulmonary O 2 uptake to survive periods when they lapse into profound hypothermia. Fuiman and Batty (1997) demonstrated that the swimming performance of herring (Clupea harengus) is strongly affected by temperature-dependent changes in water viscosity when the fish are 1 month old, although unaffected when they are adult. ...
... Of all the properties of individual animals of interest to comparative physiologists, age and stage of development are among the most consequential (Hill 1976(Hill , 2017Fuiman and Batty 1997;Matoba et al. 2000;Mortola 2001;Fuiman and Werner 2002;Lestyk et al. 2009). For environmental physiologists and others interested in natural populations of a species, the survivorship curve provides invaluable information because it reveals the relative abundances of ages and stages of development. ...
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Chapter
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Chapter
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