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FRONTIERS IN BIOSCIENCE 15: 564-594 (2010

)

The circadian rhythm of body temperature

Roberto Refinetti1
1
Circadian Rhythm Laboratory, University of South Carolina, 807 Hampton Street, Walterboro, SC 29488, USA

TABLE OF CONTENTS

1. Abstract
2. Introduction
3. Rhythmicity under standard conditions
3.1. Pattern of oscillation
3.2. Intra- and interspecies differences
4. Influence of environmental factors
4.1. Ambient temperature
4.2. Food availability
5. Influence of biological factors
5.1. Locomotor activity
5.2. Maturation and aging
5.3. Body size
5.4. Reproductive state
6. Rhythmicity and homeostasis
6.1. Regulatory process
6.2. Heat-exchange process
7. Perspective
8. References

1. ABSTRACT 2. INTRODUCTION

This article reviews the literature on the circadian Repeated measurements of body temperature
rhythm of body temperature. It starts with a description of over time -- allowing the study of 24-hour rhythmicity --
the typical pattern of oscillation under standard laboratory have been conducted in animals and human subjects since
conditions, with consideration being given to intra- and at least the mid-1800s (1-6). A few literature reviews, often
interspecies differences. It then addresses the influence of with limited scopes, have been published occasionally in
environmental factors (principally ambient temperature and the last quarter of a century (7-10). The topic is important
food availability) and biological factors (including for at least two reasons: 1) the body temperature rhythm is
locomotor activity, maturation and aging, body size, and a convenient marker of the circadian clock for studies on
reproductive state). A discussion of the interplay of biological rhythms and sleep, and 2) the rhythm reflects a
rhythmicity and homeostasis (including both regulatory and constant conflict between homeostasis and circadian
heat-exchange processes) is followed by concluding rhythmicity in the control of core temperature in mammals
remarks. and birds.

Circadian rhythm of body temperature

it is important to point out that the expression lacks technical
precision. First, the word "circadian" is used in the non-
technical sense equivalent to "cycling every 24 hours." In
contrast, those who study circadian rhythms reserve the term
"circadian" to a rhythm that has been shown to free-run with a
period (cycle length) of 18 to 30 hours in the absence of
environmental cycles and to be capable of synchronization by
environmental cycles with 24-hour periods (11). Of course,
once a species has been shown to exhibit a CRT, it is
reasonable to assume the existence of a CRT in all members of
the species studied thereafter. It is not that clear, however,
whether the demonstration of a CRT in one mouse species, for
Figure 1. Mean pattern of daily oscillation of intra- example, justifies the use of the expression in other mouse
abdominal temperature of an Anatolian ground squirrel species. Most researchers would say that this generalization is
obtained by averaging data from 10 consecutive days in 15- not justified. What about different breeds, or different age
min intervals. The animal was housed in an individual cage cohorts, of the same species? Such cases remain debatable, and
in the laboratory with food freely available. The horizontal they highlight the problem at hand. Careful researchers will, of
rectangles denote the dark and light phases of the course, always avoid unjustified assumptions.
prevailing light-dark cycle. Data from Gur, Refinetti, and
Gur, 2008 (18). The second imprecision in the expression
"circadian rhythm of body temperature" has to do with the
This review will start with the description of daily phrase "body temperature." It is traditional usage in thermal
rhythmicity of body temperature in organisms kept under physiology to reserve the phrase "body temperature" to an
standard laboratory conditions, which usually include: 1) a abstract temperature computed as the weighed mean of the
daily light-dark cycle with 12 hours of light and 12 hours of temperatures of various parts of the body (12). Yet, most
darkness, 2) constant, neutral ambient temperature, and 3) food studies of the CRT rely on measurements at a single part of
and water freely available at all times. Attention will be given the body, usually the intra-abdominal cavity. This
to similarities and differences between species and between measurement of body "core" temperature is most
individuals of the same species. commonly obtained by means of probes inserted into the
intestines through the anus or by means of temperature-
The influence of non-cyclic environmental factors sensitive radio-transmitters or digital data loggers
on the CRT will be discussed next. The discussion will include surgically implanted in the peritoneal space. In small
variations in ambient temperature and in food availability. The animals, the stress of handling involved in manual
influence of cyclic environmental factors, which can measurement of core temperature can significantly affect
synchronize circadian rhythms including the CRT, will not be the animal's temperature, so that the use of radio
discussed here because most studies in this area use outputs of transmitters or data loggers is a necessity (13-15).
the circadian system other than the CRT.
3.1. Pattern of oscillation
Afterwards, the influence of biological factors will Figure 1 shows a typical, averaged body
be discussed. Biological factors include variations in the temperature rhythm. The data were obtained with a digital
organism's locomotor activity, natural maturation and aging, data logger surgically implanted in the intra-abdominal
variations in body size, and changes in reproductive state. cavity of an Anatolian ground squirrel (Spermophilus
These particular biological factors were selected for discussion xanthoprymnus) prior to the annual hibernation season. In
primarily because much research has been conducted on them, this diurnal animal, temperature is clearly low at night,
but also because age, body size, and reproductive state are rises during the day, and falls again at night. The curve is
fundamental properties of organisms. quite smooth because it depicts the average of 10
consecutive days, so that small irregular fluctuations are
Next, the relationship between the circadian and averaged out.
homeostatic components of body temperature regulation will
be discussed with emphasis on both regulatory and heat- To the extent that the CRT is a reproducible
exchange processes. The CRT is the result of an interplay of pattern of oscillation, it can be characterized by parameters
mechanisms of heat production and heat loss controlled by the that describe "pure" oscillatory phenomena such as sine or
circadian system. cosine functions. As shown in Figure 2, a regular
oscillatory process can be characterized by its mesor (mean
A final section will summarize the issues level), its amplitude (which is approximately half the full
previously discussed and will put them all in perspective. range of oscillation), its period (i.e., the duration of the
cycle), and its phase (often reported as the position of the
3. RHYTHMICITY UNDER STANDARD peak of the wave, called the acrophase, in relation to an
CONDITIONS external reference point) (16). Because the CRT is not a
pure mathematical function, two other parameters are
The expression "circadian rhythm of body needed to fully characterize it. One of them is the wave
temperature" (CRT) will be used throughout this article, but form, which often differs considerably from a sine or

Circadian rhythm of body temperature

cosine wave and sometimes approximates a square wave.
Variations in wave form, which are often affected by but
are not solely the result of random variability ("biological
noise"), invariably affect the strength and reproducibility of
the CRT. The magnitude of this reproducibility (or the
degree of "stationarity" of the time series) is the sixth
parameter of the CRT, often called the robustness of the
rhythm (17).

Although a clear oscillatory pattern is often
evident by visual inspection of data plots, sometimes
computational tools are necessary for the identification of
rhythmicity, particularly when the signal-to-noise ratio is
low. Numerical analysis is also needed as a means of
Figure 2. Diagram of an oscillatory process identifying securing an objective index of rhythmicity and of
four parameters of the oscillation: mesor, period, characterizing the parameters of the oscillation. Various
amplitude, and acrophase. Wave form and robustness are numerical procedures suitable for the analysis of circadian
not explicitly depicted. rhythms have been recently reviewed and compared (16).
Analysis of the data in Figure 1 reveals that the oscillation
has a mean level of 36.8 OC, amplitude of 1.2 OC (range of
oscillation of 2.5 OC), acrophase at 13:05 h, a relatively
sinusoidal wave form, and robustness of 60% (18).

3.2. Intra- and interspecies differences
Daily rhythmicity of body temperature has been
extensively documented in a variety of species. The
laboratory rat (Rattus norvegicus) is the species on which
the greatest number of studies has been conducted (19-68),
but many studies were also conducted on domestic mice
(69-86), golden hamsters (87-96), and many other rodent
species (97-129). A large number of studies has also been
conducted on primates (130-145), including humans (146-
184), as well as in dogs (185-188), cats (189-191), goats
(192-196), sheep (197-203), horses (203-208), cattle (209-
213), other mammals (214-234), and many species of birds
(235-252). Although only mammals and birds are true
endotherms and have the ability to generate body
temperature rhythms in homogeneous thermal
environments, other animals are capable of generating body
temperature rhythms by selecting different ambient
temperatures at different times of the day. Consistent daily
variation in the selection of ambient temperature along a
temperature gradient has been documented in crustaceans
(253-256), fishes (257-261), and reptiles (262-275). At
least one reptile -- the green iguana (Iguana iguana) -- is
capable of generating a small-amplitude rhythm of body
temperature even when housed in a homogeneous thermal
environment (276, 277). Honey bee colonies, which
function as endothermic pseudo-organisms, also exhibit
daily rhythmicity of "body" temperature (278).

Figure 3. Five-day segments (with 6-minute resolution) Figure 3 facilitates the comparison of the CRTs
of the records of body core temperature of of three rodent species. This figure shows raw data
representative individuals of three mammalian species: collected every 6 minutes, so that so-called ultradian
laboratory rat (Rattus norvegicus), fat-tailed gerbil oscillations can be seen as high-frequency oscillations
(Pachyuromys duprasi), and tree shrew (Tupaia superimposed on the 24-hour oscillatory pattern. Inspection
belangeri). The data were collected by telemetry in the of Figure 3 clearly indicates that the rhythms of the
laboratory. The white and dark horizontal bars at the top nocturnal animals (laboratory rat and fat-tailed gerbil) are
indicate the duration of the light and dark phases of the characterized by higher temperatures during the night,
prevailing light-dark cycle. Figure adapted from whereas the rhythm of the diurnal animal (tree shrew) is
Refinetti, 1999 (363). characterized by higher temperatures during the day. Also

variability is consistently smaller than interindividual mousebirds (313). rhythm of melatonin secretion (279). Greater CRT amplitude in the cold was observed individual's rhythm does not exceed the variability between in studies on squirrel monkeys (140).2. 310) have also been shown to entrain related to body size. 59. 283. As for the acrophase. as circadian period is "temperature compensated" namely.although.. The light-dark cycle is a potent considerable inter-species variability.. Cycles of ambient temperature (307. may be (236. seasonal hibernation (316. 238-242. 4. 68. 244.the latter is always smaller increase in amplitude is often accompanied by a reduction than the former.whenever exposure to lower temperatures down to 10 or 15 OC has there is a difference between interindividual variability and been found to increase the amplitude of the CRT. Also. 41 OC and 37. In addition. entraining agent that has been thoroughly investigated (304. no effect of ambient temperature on the amplitude of the CRT was Free-running circadian rhythms of body found in rats (39. frogmouth birds (315). the body non-cyclic variations in the environment can also mask a temperature of birds tends to be more than 3 OC higher than circadian rhythm by disturbing its wave form and thus that of mammals (on average. could be generated by another rhythmic process in the as discussed in section 4.5 OC.e. 54. 198. the circadian clock. 88. Torpor may be induced by they do not necessarily demonstrate that the CRT is directly cold (or the short photoperiod that naturally accompanies generated by the circadian clock. golden hamsters (312).e. 96. If the increase in the amplitude of the CRT in a cold 143-145.and these negative findings are studies conducted on various individuals of various species. expected. therefore. To the best of the author's knowledge. Specific masking effects of ambient nocturnal. rather external temporal cues have been documented in birds than differences in experimental methods. 305). that the variabilities differ in different parameters even in ectothermic organisms (308. the mean level is the synchronization of the endogenous clock by an of the CRT tends to be higher by more than 1 OC in large. 50-52. 41. primates (130. 128. The influence of biological factors on rectangular for the gerbil. sunbirds (314). and one for the rhythm of body Ambient temperatures constantly below or above temperature (206). of the rhythm and in different species but that -. one for the rhythm of cortisol secretion (280). one for the ambient temperatures on the CRT. Very few studies have addressed directly the question of whether intraindividual differences (i. tends to be about 3 OC lower than that of placental mammals. 105. 116. Entrainment As will be discussed in detail in section 5. but several laboratory average rhythmic patterns of different individuals of the studies have used controlled changes in ambient same species). 250. there is entrainment mechanisms. pigeons (238). Cyclic and considerable inter-species variability. The results of these studies are thermoneutrality have not been found to affect the period or consistent with the impression that one acquires by reading phase of the CRT -. 134. 159. range of The environment in which an organism lives can oscillation. temperature and food availability on the CRT will be discussed here -. That is. this other rhythmic process itself being generated by circadian system (317) and can. 311). and this intraindividual variability -. 117. and other mammals (189-191. environmental cycle. 124. 83. Ambient temperature day differences in the rhythmic pattern exhibited by an Most studies of the CRT are conducted under individual of a given species) are comparable to constant temperature conditions in the laboratory or under interindividual differences (i. but it does not seem to be availability (309. rodents (21. INFLUENCE OF ENVIRONMENTAL FACTORS rhythm is less than 2 OC for the rat but more than 4 OC for the tree shrew.in sections 4. and Australian variability. 233. 63. The range of oscillation also varies with body Several decades of research on circadian rhythms size across species: the range is almost 2 OC narrower in have generated a large body of knowledge about large species than in small ones -. day-to. 283-291). the CRT is discussed in section 5 below. 161. respectively. and the temperature of marsupial mammals in period and phase. 230. except that few large mammals are circadian rhythms. including humans (146. it usually occurs at night in nocturnal animals and during 306). 32. entrainment and through masking (304. only temperature to address the issue of the effects of different three studies have addressed the question. 282). 139. Daily torpor is controlled by the body. In principle.3. 308) and food the day in diurnal animals. tree shrews (312). although there is of the period and phase of the circadian clock. the amplitudes of the rhythms differ among the species: the daily range of oscillation of the temperature 4. again. be thought of as . 317). On the other hand. altering the mesor and amplitude and mimicking alterations respectively)." a well- 217. which is achieved through modulation sized species than in small-sized ones. higher zeniths). the rhythms of different individuals.1 and 4. or temperature recorded in controlled environments without mouse lemurs (137). 294-300). responsible for the conflicting results. environment results mostly from lower nadirs (without 171. 162. Table 1 lists the mean level. Intraindividual thirteen-lined ground squirrels (128).Circadian rhythm of body temperature evident are differences in wave form: square for the rat. differences between the uncontrolled conditions in the field. 301-303). 71. the CRT the cold of winter) or simply by restricted food availability. 66. Genuine species differences. 293). However.2. While these studies provide known mechanism of energy conservation analogous to sufficient evidence of the endogenous nature of the CRT. 138. 246-248. 292.1. 312). it is often referred to as "torpor. and acrophase (peak time) of the body affect its circadian rhythms in two major ways: through temperature rhythms of 67 species of mammals and birds. the day-to-day variability of an in mesor. and bimodal for the tree shrew. 205. 131. 281.

5 2.8 6 246 Glaucomys volans 37.5 2.2 8 242 Gallus domesticus 40.2 10 147 Homo sapiens 36.2 10 159 Homo sapiens 37.6 3.5 6 236 Coturnix coturnix 41.0 10 495 Homo sapiens 37.8 0.1 10 154 Homo sapiens 36.7 0.0 19 213 Canis familiaris 38.2 1.4 1.3 16 189 Felis catus 38.0 15 190 Felis catus 38.4 14 209 Bos taurus 38.5 13 252 .8 0.2 10 162 Homo sapiens 36.1 1.Circadian rhythm of body temperature Table 1 Parameters of the CRT of 67 species of mammals and birds.5 1.0 1.9 1.4 2.4 16 202 Capra hircus 39.8 1.9 18 102 Antechinus stuartii 36.5 0.0 0.2 9 507 Homo sapiens 37.1 0.0 1.0 9 171 Homo sapiens 37.8 10 196 Cebus albifrons 37.7 14 194 Capra hircus 39.9 0. as determined in 160 published studies Mean Range Acrophase Species Source (OC) (OC) (HALO a) Acomys russatus 37.0 9 151 Homo sapiens 36.5 11 187 Canis familiaris 39.5 6 248 Gallus domesticus 40.8 1.5 3.0 1.0 0.7 0.2 16 219 Eulemur fulvus 38.5 18 98 Aethomys namaquensis 36.0 1.7 6 338 Columba livia 41.7 6 132 Columba livia 40.8 10 160 Homo sapiens 36.4 12 387 Capra hircus 38.4 1.0 8 181 Homo sapiens 37.8 10 169 Homo sapiens 37.1 12 249 Gallus domesticus 40.0 14 205 Erinaceus europaeus 35.9 1.0 1.9 14 207 Equus caballus 38.0 1.2 0.1 6 235 Columba livia 40.5 2.8 10 212 Bos taurus 39.3 15 240 Cynomys ludovicianus 37.5 14 191 Gallus domesticus 40.0 1.8 8 164 Homo sapiens 36.6 1.7 17 103 Apodemus mystacinus 38.2 0.7 5 106 Bettongia gaimardi 37.1 2.9 18 211 Bos taurus 38.0 2.9 1.5 3.3 2.4 18 131 Apodemus flavicollis 37.9 18 130 Felis catus 37.4 4.1 10 153 Homo sapiens 37.0 11 170 Homo sapiens 37.0 0.2 6 105 Arvicanthis niloticus 37.9 12 210 Bos taurus 39.2 10 177 Homo sapiens 37.3 1.6 1.3 1.5 2.8 3.0 12 208 Equus caballus 38.8 3.2 1.1 2.7 10 172 Homo sapiens 36.5 16 218 Isoodon obesulus 36.2 17 98 Arvicanthis ansorgei 38.0 10 192 Capra hircus 38.0 1.1 19 214 Aotus trivirgatus 37.6 18 227 Didelphis marsupialis 35.0 6 68 Arvicanthis niloticus 37.7 1.8 0.0 0.5 7 216 Dasypus novemcinctus 35.5 1.0 20 218 Equus caballus 37.8 1.4 1.5 19 218 Didelphis virginiana 35.2 0.3 1.7 13 195 Capra hircus 38.4 1.7 22 215 Bos taurus 38.7 11 188 Canis familiaris 39.1 17 108 Heterocephalus glaber 33.0 0.8 1.7 2.2 2.3 10 155 Homo sapiens 37.2 2.8 15 220 Homo sapiens 36.8 0.6 18 217 Dasyurus viverrinus 36.4 2.6 10 163 Isoodon macrouros 36.4 0.

8 1.1 19 69 Mus musculus 36.6 2.0 2.1 18 509 Rattus norvegicus 37.0 1.0 2.6 2.2 287 Rattus norvegicus 37.3 2.4 1.6 10 134 Macropus giganteus 34.5 2.2 16 27 Rattus norvegicus 37.8 21 84 Mus musculus 36.3 1.8 1.0 17 20 Myrmecobius fasciatus 35.7 19 361 Rattus norvegicus 37.8 2.5 137 Microcebus murinus 36.8 12 87 Ovis aries 38.3 18 42 Rattus norvegicus 37.4 18 24 Rattus norvegicus 37.8 8 115 Octodon degus 37.9 16 221 Macaca fuscata 37.3 1.0 3.8 18 60 Rattus norvegicus 37.7 1.8 18 50 Rattus norvegicus 37.3 12 87 Meriones unguiculatus 36.4 1.5 17 30 Rattus norvegicus 37.3 17 89 Microcebus murinus 36.9 14 19 Mesocricetus auratus 36.4 1.1 1.0 1.0 2.4 18 53 Rattus norvegicus 37.3 2.5 17 25 Rattus norvegicus 37.7 1.2 12 250 Mephitis mephitis 36.0 1.0 16 136 Mus musculus 36.5 2.8 19 222 Macropus rufus 36.5 18 139 Microcebus murinus 36.4 18 290 Rattus norvegicus 37.6 19 70 Mus musculus 36.3 10 109 Meleagris gallopavo 40.3 1.5 11 19 Octodon degus 37.4 17 508 Mus musculus 36.9 20 225 Oryctolagus cuniculus 39.8 18 41 Rattus norvegicus 37.7 14 19 Mesocricetus auratus 36.0 2.7 1.0 1.6 2.3 0.7 17 222 Marmota monax 37.5 1.0 15 86 Mus musculus 36.2 1.7 8 111 Meriones unguiculatus 37.2 16 15 Mus musculus 36.2 16 73 Mus musculus 37.1 1.2 1.3 2.6 1.9 1.0 1.7 18 32 Rattus norvegicus 37.5 17 93 Mesocricetus auratus 38.0 2.8 10 223 Nasua nasua 37.1 18 21 Rattus norvegicus 37.7 18 74 Mus musculus 36.3 9 198 Pachyuromys duprasi 36.5 2.0 9 199 Ovis aries 39.6 1.0 5.0 5 117 Octodon degus 36.Circadian rhythm of body temperature Lasiorhinus latifrons 35.8 2.0 292 Macaca mulatta 38.4 2.5 1.2 2.5 2.9 2.5 16 37 Rattus norvegicus 36.9 7 224 Octodon degus 36.5 1.9 2.9 19 31 Rattus norvegicus 37.5 18 118 Petaurus breviceps 37.1 1.4 1.9 2.7 5 113 Octodon degus 37.0 18 45 Rattus norvegicus 37.8 0.4 1.0 6 114 Oryctolagus cuniculus 38.2 18 226 Procyon lotor 38.4 18 43 Rattus norvegicus 37.1 16 19 Rattus norvegicus 37.0 18 14 Rattus norvegicus 37.6 1.4 1 87 Rattus norvegicus 36.3 14 202 Ovis aries 40.8 1.7 18 94 Mesocricetus auratus 36.5 1.2 1.5 1.3 2.3 18 20 Rattus norvegicus 37.4 1.6 2.5 18 65 Rattus norvegicus 37.9 0.4 18 69 Rattus norvegicus 37.8 18 138 Microcebus murinus 36.4 9 133 Macaca mulatta 36.3 2.7 1.4 10 135 Macaca mulatta 37.2 1.2 1.8 2.2 18 77 Mus musculus 36.3 17 26 .5 1.

Furthermore.2. 156. 327.5 18 318 Spalax ehrenbergi 36. 286. 285. and because animals and humans tend to eat induced hypothermia. no food was provided.0 293 Sarcophilus harrisii 35.2 8 19 Spermophilus xanthoprymnus 37.5 2. 330-333).4 14 230 Sus scrofa 39. by its body size. 205.9 2. quail (328). the animal received a single a side effect of the circadian rhythm of locomotor activity meal each day (indicated by the arrows). Locomotor activity The fact that the CRT persists in the absence of The daily/circadian rhythms of locomotor activity daily oscillation in food consumption does not imply that and body temperature have been simultaneously monitored disturbance of the usual pattern of feeding cannot affect the in many studies on various species (30. in animals deer mice (355). 361. 130.1 1. true homeotherms exhibit circadian-modulated starvation- 320-322). In reality. 362).7 4.0 7 18 Struthio camelus 39.4. INFLUENCE OF BIOLOGICAL FACTORS that characterizes the CRT.2 3. For the next three and will discuss how the CRT is affected by the days.0 6 126 Spermophilus richardsonii 36. CRT. the concentration of feeding during the light 357. 51. finches (353).0 5. fed ad libitum. 237.4 1. 88.7 6 141 Saimiri sciureus 37.4 18 234 a HALO = hours after lights on a large-amplitude CRT. the CRT persists in the absence of daily oscillation in food Over a century of research on circadian rhythms consumption. the rodents have shown that food restriction can cause both temporal courses of the two rhythms are very similar. What is heterothermic species. pigeons (235. does not occur indiscriminately. The rectal temperature physiological process. subjected to temporarily modulated by environmental factors (359. conceivable that the CRT could be a mere side-effect of the mousebirds (313.0 7 128 Spermophilus tridecemlineatus 36. The fact that the CRT is endogenously generated does temperature (24.8 18 68 Saimiri sciureus 37. 31. 324).2 6 108 Tupaia belangeri 38. However. even if it can be partially and animals and humans fed no meal at all (that is.1 18 129 Thallomys paedulcus 36. 230. and goats (194).5 2. it is not currently known In a number of species. This has been documented in doves mostly at certain times of the day (323. 245.1. 237. it is restricted to the inactive phase of the circadian cycle. 334-338). moderate food whether daily torpor involves a distinct physiological deprivation induces a reduction in metabolic rate and a fall process or is simply an extension of the CRT in in body temperature (42.0 14 228 Sus scrofa 39. Food deprivation caused a developmental state of an organism. clearly preserved. 358). 237.9 18 102 Trichosurus vulpecula 37. rats (42.4 5. consider (and reject) the possibility that the CRT is merely During the first three days. pygmy mice (354). 329. various acute rise in body temperature in various species (197. but rhythmicity was by its reproductive state. lemurs (136. 159. 74.4 4.0 5 233 Vombatus ursinus 34. that it is generated as an autonomous An example is provided in Figure 4.6 2. 352). 95.5 5 124 Spermophilus beecheyi 36.3 10 19 Spermophilus tridecemlineatus 36. In sections 5. Generally. sheep (202). 350.4 2. I will of a goat was recorded at 3-hour intervals for several days.7 4. 180.8 1. The hypothermia suggest that torpor is a natural extension of the CRT (318.5 9 229 Thallomys nigricauda 36. Numerous studies of "food anticipatory activity" in 110.5 4. 318.4 5 125 Spermophilus lateralis 36. 326). 339-349). 135. domestic mice (356). 223. phase or the dark phase of the light-dark cycle could possibly result in the chronic elevation of body temperature 5. 219. genetically inherited. 338.8 2.2 18 227 Sminthopsis macroura 36. 351). and small decline in body temperature.6 0.0 6. 327-329). 248. 202. 329.4 2.0 8 140 Saimiri sciureus 37. Although some 4.8 9 251 Suncus murinus 35.0 1. it is (282).0 4. That is. 5.2 5. total food deprivation) still show daily rhythmicity in body 360).7 1. however.1 through 5.9 16 218 Tupaia belangeri 37. Instead. however. circadian rhythm of food consumption. not mean. the activity and body temperature rhythms . 43. Food availability animals have a natural disposition to exhibit daily torpor Because food ingestion is associated with an even when fed regularly (128. induced by food deprivation (or chronic food restriction) 319). humans and animals fed small meals at has produced extensive evidence that circadian rhythms are regular intervals throughout the day nonetheless exhibit endogenously generated and that the period of a rhythm is clear CRTs (172. 138). 188.Circadian rhythm of body temperature Rattus norvegicus 37. 325. diurnal animals. A few studies investigating the especially interesting about this phenomenon is its ambient temperature selected by torpid animals seem to modulation by the circadian system. Thus. In entrainment and masking of the CRT (55.

Some argue that masking can be mathematically filtered out (374). exhibit high values during the day and low values during 5. Figure adapted susceptibility to masking caused by environmental light from Piccione. Weak rhythmicity appears again at 25 days of age hours before awakening and then rises abruptly (more so in and attains the adult range (1. including the need for 24-hour light-dark cycle with and without daily meals frequent collection of blood (or saliva) samples and a high (which are indicated by the vertical arrows). and Refinetti. 134. although adult rhythms seem to be attained activity and temperature.it is natural to wonder body temperature but a form of cold-induced torpor (378. As a matter of fact. during the night. 373). but it seems to vanish by 15-20 days of age (376- rodents. 368-370). Although nocturnal animals are earlier than in calves. The melatonin rhythm has the Figure 4. Maturation and aging the night. may confidently say that the body temperature rhythm in rhythmicity matured over several weeks and attained a animals. 2003 (194). it does not cause it. measurements taken at dawn 326). but not in pups kept in isolation can elevate body temperature in humans (2. In rabbits. so that the daily elevation in body temperature associated with Newborn calves lack daily rhythmicity of body circadian rhythmicity might be a direct result of increased temperature. One research group reported the presence of rhythmicity two In order to investigate the potential causal link weeks after birth (385). some researchers argue that the CRT is so strongly masked by changes in activity in free-living subjects that it should not be relied upon as a marker of the state of the circadian clock. the different rates. the activity and body temperature In rats. Because the early temperature rhythm vanishes in a few days and is observed only when the pups are kept at an Because the rhythms of body temperature and ambient temperature below thermoneutrality. large daily fluctuations in ambient temperature (about 20 several researchers recorded the body temperature rhythm O C). 384). but the autonomy of Lambs (young sheep) and foals (young horses) the CRT has been demonstrated by analysis of the day- also develop daily rhythms of body temperature during night difference in the correlation between the rhythms of early life. Bed rest cannot be used with animals. In both humans and birth. stable level by 6 weeks after birth (387). Thus. is not caused by the activity rhythm. and other vertebrates (91.2. which probably caused the fluctuation in body of human subjects maintained in continuous bed rest (156. a rhythm of body temperature with a rhythms of nocturnal animals exhibit high values during the range of oscillation of 2-4 OC is observed on the day after night and low values during the day. body temperature is higher at night regardless of the actual different species develop the body temperature rhythm at activity level (51. temperature. about 1 OC was achieved between 50 and 60 days after while the activity rhythm may alter the amplitude and birth (209).Circadian rhythm of body temperature enhanced or disrupted (masked) by changes in activity. as a stable dusk-dawn difference is generally more active at night than during the day. rodents than in humans) at wake time (363). Although the amplitude of the rhythm is reduced decreased gradually until a stable dusk-dawn difference of under this condition. In calves maintained under constant ambient 158. 220. 180. robust rhythmicity persists. Thus. 371). 130. 92. we for several days after birth. it is well as early as 4 or 5 days after birth in pups allowed to remain known that acute episodes of physical activity and exercise with the doe (303. Conversely. whereas others recommend that the CRT be replaced by the rhythm of melatonin secretion as a reliable marker of the state of the clock (375). Indeed. Evidently. ease of measurement. Conversely.both under a light-dark thought not to be a true precursor of the adult rhythm of cycle and in constant conditions -. but their calves were exposed to between the activity rhythm and the temperature rhythm. 204. 176. whether the temperature rhythm is not simply a 383). equal-size meals (172. are not observed until two months after birth (209). their achieved about one month after birth (386). first 10 days of life. Different species of domestic animals activity rhythm does not imply that the CRT cannot be . Daily rhythms comparable to those of adults activity. dogs. body temperature starts to ascend slowly several 381). temperature rhythmicity can be observed consequence of the activity rhythm. lambs. and The fact that the CRT is not caused by the foals are not evident. 95. 364-367) with continuous intra-esophageal feeding (379). shape of the body temperature rhythm. The reasons for the differences in timing among calves. Regardless of breed or sex. and demonstrated autonomy from the activity rhythm. In dogs.6 OC) at 45 days of age (382). whereas the susceptibility to masking is a major disadvantage. Seven-day segment of the records of rectal advantage of being resistant to masking caused by activity temperature of a goat (Capra hircus) maintained under a but has several disadvantages. The advantages of the CRT include tradition. this rhythm is activity proceed closely together -. Caola. temperature. Later on. 372. puppies of three different breeds body temperature of diurnal animals is higher during the failed to exhibit statistically significant daily rhythmicity day regardless of the actual activity level (363). as in humans. or undergoing a "constant routine" protocol. 325. no difference between measurements taken at which involves bed rest as well as sleep deprivation and the dawn and measurements taken at dusk was found for the ingestion of frequent.

and the mean the fact that other bodily rhythms also undergo maturation. The amplitude of the body to both. more between the mesor (mean level) of the CRT and body size studies are needed to clarify these apparently conflicting (B). on average. the abscissa is scaled logarithmically. 404. development of mechanisms downstream from the 431). a daily pattern is noticeable at 3 CRT (Figure 5. 163. as reported in 135 published studies on 55 mammalian results. species. in large animals than in small animals. because. body temperatures of animals in the 10-g range. delay in the expression of rhythms is most likely due to the 430) or identified a weak positive correlation (427. and shortening of circadian period was also observed in deer mice (415). body temperature. Furthermore. Relationship between the daily range of periods of young and old subjects (426). and only three body temperature and body size based on literature surveys months after birth in humans (393. 78. 119. However. For instance. Studies on golden hamsters have generally found that circadian period is shortened in old age (415-421). the CRT is affected by aging. By far the best characterized alteration in the circadian system related to aging is a reduction in the amplitude of circadian rhythms (401-403). 390). 411-414) and rodents (61. at least in rats and sheep. Again. 60. and laboratory rats (422). the fact that the CRT is not present at birth interpretation of this weak albeit statistically significant seems to be a common finding. this is presumably due to the greater thermal inertia of large Despite interspecies differences in the rate of animals. although the effect is modest (as indicated by the Newborn human babies do not have a rhythm of relatively small correlation coefficient of -0. one study found no difference between the free-running Figure 5. Aging seems to also be associated with a change in the phase and period of circadian rhythms. Curiously. lengthening of circadian period was observed in aging domestic mice (423. and a mature daily rhythm is not reached have. Immaturity of the circadian system is suggested by temperature rhythm was found to be smaller. large bodies buffer the effects of the of rhythmicity. and it is to be expected that in small animals in the body mass range from 10 g to 1. intraspecies studies in dogs (387) and circadian pacemaker. The absence of the CRT in relationship. 61. The data were obtained from the animals than in small animals in the body weight range subset of mammalian studies listed in Table 1 from 10 g to 1 kg (427). or Aschoff's prediction (428). independent studies in mammals has also confirmed to immaturity of mechanisms of heat gain and heat loss.26). Reduction in the amplitude of the body temperature rhythm in old age has been documented in humans (162. 428. 77. body temperatures 0. level to be higher. principally through the development of heat conservation mechanisms (400). 394). The straight lines were fitted to the data by 5. between body temperature and body mass. Clearly. In humans.3. At the other end of the age spectrum. A small advance in the phase angle of entrainment in old age has been documented in humans (163. Body size the method of the least squares (and the correlation Many years ago. the have either failed to identify a significant correlation (429. Presumably.6 OC higher than the until a year or more after birth (389. A recent literature survey based on 125 early life may be due to immaturity of the circadian system. Aschoff pointed out that the coefficient and its associated probability under the null amplitude of the CRT is 3 to 6 times smaller in large hypothesis are indicated).000 differences will also exist in the ontogenetic development kg. oscillations in heat production and heat loss responsible for the CRT. but only two weeks Interspecies studies of the relationship between after birth in hamsters and rats (392). although few of these studies monitored the CRT. the thermoregulatory system is known to undergo maturation in young mammals and birds. Animals in the 1. whereas another oscillation of the CRT and body size (A) and relationship found shorter periods in older subjects (162). the rhythm of melatonin secretion is present immediately after birth in seals (391). In both graphs. 424) and canaries (425). The data from 135 independent studies shown in Figure 5 (panel A) confirm that the exhibit different parameters of body temperature amplitude is about 3 times smaller in large mammals than rhythmicity in adulthood (388). The data for . panel B). 407). 405) as well as in various rodent species (53. the humans (432) identified a significant inverse correlation pacemaker itself is already oscillating before birth (395. and again caution should be exercised in the maturation. The body temperature of a newborn body size has the opposite effect on the mean level of the oscillates randomly. 406-410). Curiously.000-kg range months of age. However.Circadian rhythm of body temperature 399).

the many species of mammals and birds exhibit estrous studies that allegedly supported the set-point explanation of rhythmicity in body temperature (66. Somehow. and being secondarily modulated by the (387). For instance. production of the body temperature rhythm but that. It is 6. pigeons (475. 2009 point. 6. On the other hand. 449. Regulatory process Thermal physiologists have generally assumed that the CRT is primarily under homeostatic control and is secondarily modulated by the circadian system through an oscillation in the thermoregulatory set point (293. of preventing out above that the body temperature rhythm of endotherms deviations from an ideal set point. 209.1. The finding implies an elevation of the set point (because. In order to 242. 446. 471- 473). 240. in rats in mammals overall but uncovered significant relationships (474). the use of circadian control of body temperature imposes a persistent behavioral responses can provide a reliable measure of the oscillation in body temperature. at the same time. most studies of daily and circadian rhythms of body set point. and it was pointed the goal of ensuring stability -. For this thermoregulatory set point. presumably. RHYTHMICITY AND HOMEOSTASIS known that autonomic and behavioral thermoregulatory responses can complement each other in the homeostatic The homeostatic control of body temperature has control of body temperature (480-486). In addition. The negative correlation between body temperature and body size has a coefficient The idea that the CRT might result from a daily of -0. 114. . a recent literature review identified no body temperature. 234. bypassing the thermoregulatory set adapted from Piccione. 442. 459-463). the does not require behavioral responses. the circadian pacemaker acts on the thermoregulatory thermostat so that the set point is Figure 6. the CRT failed to evaluate set point changes. ambient temperature is kept constant). 476). The straight line nocturnal animals). Rectal temperature as a function of body size for elevated during subjective day and lowered during 115 dogs of 19 different breeds ranging from 2-kg subjective night in diurnal animals (or vice versa in Yorkshire Terriers to 85-kg Great Danes. and heat conservation responses are significant relationship between temperature and body mass activated during the phase of high body temperature. All of these judge whether there is circadian modulation of the processes can mask the CRT in multiple ways.57. 435-451). 461-470). The for particular subgroups (433). 452.2. The finding that injection of causes of the scaling must be found in ecological factors antipyretics could reduce the amplitude of the CRT of that affected the evolution of different phylogenetic groups otherwise undisturbed rats (58) provided further support for differently. one temperature (or of locomotor activity. enhanced thermogenesis scaling relationship was found in bats. dogs are shown in Figure 6. that the scaling of body temperature is positive in some the elevation in the set point was responsible for the phylogenetic groups but negative in others implies that the enhanced heat production). The reproductive cycle us anything about the state of the set point. more logical was fitted to the data by the method of the least squares from the viewpoint of circadian biologists. Why interspecies coefficients should be positive oscillation of the thermoregulatory set point seemed to be and intraspecies coefficients be negative is not evident. Figure under circadian control. vaginal activated -. As a responses are activated during the circadian phase of low matter of fact. behavioral sexual mechanisms of heat production or heat loss must be receptivity (445. and humans (148. How this is accomplished in terms of physiological control will be discussed in section 6. Giudice. would be to (and the correlation coefficient and its associated have the circadian oscillation in body temperature primarily probability under the null hypothesis are indicated). was that the measurement of autonomic thermoregulatory so that reproduction is possible only during the appropriate responses at different times of the day does not really tell phase of an ovulatory cycle (434). and Refinetti. Research conducted in the past 10 years or so strongly supports the alternate explanation. 451. 243. for that matter) are needs a variable that is not normally required for the conducted on males. 448. the notion of circadian modulation of the set point. and locomotor activated in order for body temperature to change (if activity (66. 453. 114. 452. 435. 5.4. An alternate arrangement. 234. Therefore. whereas a negative during the circadian phase when body temperature is high scaling relationship was found in artiodactyls. How it is accomplished in terms of effector mechanisms will be discussed in section 6.that is. 444. 250. 438. these two state of the set point. thermoregulatory system. but supported by laboratory evidence that autonomic heat loss there must clearly be differences between species. for instance. In order to measure the state of the set point. a positive reasoning was that.and it is a thermodynamic necessity that discharges (234. 452-454). Reproductive state What was wrong with the preceding reasoning Most female animals do not ovulate on demand. According to this view. one must be able to monitor the reason. It tells us only involves not only timed ovulation but also estrous that heat production and heat loss mechanisms are being rhythmicity in hormonal secretions (250.Circadian rhythm of body temperature antithetic processes must be integrated. 455-458).1. 437. does reflect the operation of the set point. 477-479). In other words. Fazio.

body temperature was high during the is. Research in many other laboratories over the years. Notice that heat production leads body the rhythms of body temperature and of preferred ambient temperature by 1. 504). 1998 thermoregulatory center in the preoptic area of unlesioned (118). the animals behaviorally studies on a large number of species. there is no reason Daily oscillation in the body core temperature of to assume that the set point oscillates at all (499. The following year. and heat loss of a rat (top three graphs). whereas heat loss trails body temperature in fat-tailed gerbils (Pachyuromys duprasi) temperature by 0. production. This phase difference is presumably due to temperature selection was. An example is shown in Figure 8.Circadian rhythm of body temperature The thermoregulatory system's opposition to the circadian oscillation of body temperature is evidently not fully successful. The other way was by impairing the thermoregulatory system through surgical ablation of the Figure 7. Cosine dunnarts (318). Heat-exchange process body temperature than during the phase of high temperature In order to produce a CRT. has a margin of stimuli were perceived as more pleasant during the hysteresis error. and humans (319). and vice versa. In other words. squirrel monkeys (141.3 hours. As a matter of fact. Carlisle noticed that rats exposed to the cold would press a lever for heat more vigorously during the phase of low 6. This has indeed been observed in (492). the amplitude of the temperature rhythm is effectively reduced by the action of the thermoregulatory system. it can be inferred that the with 6-minute resolution. the circadian system The first investigator to directly address the issue generates an oscillatory signal that is communicated to the was probably Hensel. The rhythm of behavioral by 6 hours. who studied the thermal organs responsible for heat production and heat loss. has produced and/or in the amount of heat lost to the documented that higher ambient temperatures are preferred environment. species. each studied over 10 consecutive days from inhibitory control. The average rhythms are area releases the circadian oscillation of body temperature derived from 5 gerbils.2. 489-491). PERSPECTIVE the set point cannot possibly be responsible for the temperature rhythm. waves were fitted to the raw data of body temperature. degus (115). the thermoregulatory system generates a set subjects at different times of the day and noticed that warm point that. The vertical dashed lines indicate the acrophases of the Figure 7 illustrates the phase opposition between rhythms. environmental temperatures are selected when body temperature is low. higher animals of different body sizes (427). the body must (488). At the sensation evoked by warming of the hand of human same time. The amplitude of the body temperature rhythm was reduced in tree shrews and flying squirrels allowed to select their environmental temperature (108). in rats (22. a phase difference of 6 hours is found. The integrated output of the two systems is circadian phase of low body temperature than during the an oscillation whose amplitude is restricted to the phase of high temperature (487). like most control systems. tree shrews (108). 180O out of phase with thermal inertia of the body and should be different in the rhythm of body temperature. and the daily range of oscillation is between 1 and . Relationship between the average rhythm of body main thermoregulatory center in the preoptic area of the temperature and the average rhythm of selected ambient brain. Aschoff reasoned early on that both heat during the phase of low body temperature.9 hour. mice of heat production (7). and that the ambient temperatures are preferred during the phase of high oscillation of heat loss needed to lag behind the oscillation body temperature. implying that ablation of the preoptic cycle (as indicated by the shading). however. the oscillation of 7. Clearly. 45. If heat balance is calculated tested in a temperature gradient. stripe-faced (172. That nocturnal animal. This has been shown in two ways. in 1978. As mammals and birds has been documented in numerous body temperature oscillates. 493). One way was by comparing the amplitude of the rhythm in animals maintained in a constant-temperature environment with the amplitude in animals allowed to continually select their environmental temperature in a gradient. produce an oscillation in the amount of metabolic heat using a variety of behavioral research techniques. flying squirrels (108). 329. 293). Body temperature is counteract the oscillation to defend the unaltered set point. 490. and humans (495-498). golden hamsters (93. As expected for a (bottom panel). Siberian hamsters rats (64. heat lemurs (494). The amplitude of the body temperature rhythm was temperature of fat-tailed gerbils (Pachyuromys duprasi) greatly enhanced in rats and golden hamsters with preoptic maintained in a temperature gradient under a 24-h light-dark lesions (501-503). The mean oscillation of body temperature imposed by the circadian level of the oscillation is between 36 and 41 OC in most system. boundaries of hysteresis error. as witnessed by the very existence of the rhythm. 287). the heat-balance rhythm leads the temperature rhythm night and low during the day. generally higher during the day in diurnal species and The thermoregulatory system actually opposes the higher during the night in nocturnal species. Figure adapted from Refinetti. and lower production and heat loss needed to oscillate. However. fat-tailed gerbils (118). animals restricts the oscillation of body temperature to an acceptable range. Thus. Thus. 500). 48.

588 (1884) The CRT is robust under constant. Philos Trans R production. Proc R Soc Lond 18. can generate CRTs if provided with the opportunity to select the temperature of their environment. Understanding the causes and properties of the CRT is important because homeothermic endothermy provides physiological and ecological benefits believed to be responsible for the adaptive success of birds and mammals in a wide range of aerial. 143-147 (1983) Maturational stage. by change of climate. Therm Biol 8. Interestingly. and heat loss of a laboratory rat maintained in Soc Lond 135. E. Davy: On the temperature of man. The last graph at the bottom compares the body 221-245 (1866) temperature rhythm with the heat-balance rhythm (where heat balance is defined as the difference between the normalized 4. 286-314 (1896) can also be observed in animals with restricted access to food. 5. with the oscillation of heat loss lagging behind the oscillation of heat production by a few hours. O. Aschoff: Circadian control of body temperature. rhythms. George's Hosp Rep 1. it has been extensively documented that extant ectothermic species.). Maurel: Experiences sur les variations depending on the species. Dashed vertical lines indicate the acrophases of the of the human body in health. Proceedings of the 11th ISB Congress. 513-528 (1870) 5 OC. heat 2. Although it is generally assumed that hibernation and torpor are relatively recent specializations arising from homeothermic ancestors. the CRT may very well be a mild recent form of an ancient process of daily torpidity. In: Driscoll. REFERENCES 1. and is secondarily modulated SPB Academic Publishing. therefore. F. Relationships between body temperature.Circadian rhythm of body temperature by the thermoregulatory system. and reproductive state can also affect the CRT. Thus. Under constant environmental conditions. Rattray: On some of the more important values of heat production and heat loss). Thus. It is possible. & Box. 319-333 (1845) constant darkness. as from temperate to tropical. L. Thin lines correspond to actual data collected at 6-minute intervals. Ann Sci Nat Serie 2 20. primarily under circadian control. body size. and the reverse. Ogle: On the diurnal variations in the temperature to the data. D. Thick lines are cosine waves fit 3. that the evolutionarily "new" drive to maintain homeostasis in homeotherms conflicts with the "old" universal drive to oscillate body temperature -. 8. St. particularly reptiles (262-275). G. Although the CRT persists in the absence of daily 7. but its amplitude is enhanced in 6. The Hague: thermoregulatory set point. E. Hobday: Notes on physiological temperatures. W.and this may explain the opposition between the thermoregulatory system and the circadian system in the control of body temperature in contemporary homeotherms. activity can greatly affect the CRT. 293-326 (1843) Figure 8. 2003 (287). it has been proposed that heterothermy may have actually preceded homeothermy in vertebrates (506). neutral environmental conditions. nycthemerales de la temperature normale. the rhythm free-runs with a period shorter or longer than 24 hours. C. J cold environments in some species. 325-337 . 8. Enhanced amplitude Comp Pathol Ther 9. Hahn: Body temperature rhythms in farm animals: a review and reassessment relative to The circadian oscillation in body temperature is environmental influences. J. the violation of homeothermy represented by the CRT must be seen as much more than just a curious deviation from an ideal pattern. C R Seances Soc Biol Paris 37. Figure adapted from physiological changes induced in the human economy Refinetti. bypassing the (Eds. and terrestrial environments (505). aquatic. Chossat: Recherches experimentales sur l'inanition. J. which further supports the notion of an ancestral origin of daily/circadian rhythmicity. J rhythmicity in activity. pp. The actual change in temperature is achieved by modulation of heat balance. A.

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