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First published online February 15, 2008
Journal of Experimental Biology 211, 749-756 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.013946
Thermoregulation in pronghorn antelope (Antilocapra americana, Ord) in winter
1 Department of Zoology and Physiology, University of Wyoming, Laramie, WY
82071, USA
2 Department of Physiology, University of the Witwatersrand, Johannesburg, South
Africa
3 Physiology, School of Biomedical and Chemical Sciences, University of Western
Australia, Perth, Australia
* Author for correspondence (e-mail: mitchg{at}uwyo.edu)
Accepted 24 December 2007
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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186 W m–2. Brain
temperature (Tbrain, 39.3±0.3°C) was higher
than carotid blood temperature (Tcarotid,
38.5±0.4°C), and higher than jugular temperature
(Tjugular, 37.9±0.7°C). Minimum
Tbrain (38.5±0.4°C) and
Tcarotid (37.8±0.2°C) in winter were higher
than the minimum Tbrain (37.7±0.5°C) and
Tcarotid (36.4±0.8°C) in summer that we have
reported previously. Compared with summer, winter body temperature patterns
were characterized by an absence of selective brain cooling (SBC), a higher
range of Tbrain, a range of Tcarotid
that was significantly narrower (1.8°C) than in summer (3.1°C), and
changes in Tcarotid and Tbrain that
were more highly correlated (r=0.99 in winter vs r=0.83 in
summer). These findings suggest that in winter the effects of the carotid rete
are reduced, which eliminates SBC and prevents independent regulation of
Tbrain, thus coupling Tbrain to
Tcarotid. The net effect is that
Tcarotid varies little. A possible consequence is
depression of metabolism, with the survival advantage of conservation of
energy. These findings also suggest that the carotid rete has wider
thermoregulatory effects than its traditional SBC function.
Key words: pronghorn, winter thermoregulation, carotid rete
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). This
combination arises from the regulation of Tbrain by
selective brain cooling (SBC) at Tcarotid greater than
39.5°C, and brain warming when Tcarotid is less than
37.8°C. We concluded that the relatively constant
Tbrain was the origin of the variation in
Tcarotid. Thermoregulatory effector responses are maximal
when Tcarotid and Tbrain are changed
in parallel (Jessen and Feistkorn,
1984). When they are dissociated, for example by independent
regulation of Tbrain, responses are reduced. A predictable
result is that Tbrain stays relatively constant,
Tcarotid is not as tightly controlled and variation in
Tcarotid will increase. The advantage of variation in
Tcarotid in a hot and arid environment is conservation of
water (Jessen, 1998;
Mitchell et al., 2002).
The independent regulation of Tbrain that occurs in
summer in pronghorn (Lust et al.,
2007) is a function of the carotid rete mirabile (the `rete'). The
rete consists of a plexus of small arteries arising from the external carotid
artery. In pronghorn almost all arterial blood that reaches the brain, except
for a small supply from the basilar artery, passes through the rete
(Carlton and McKean, 1977). The
rete is surrounded by a venous cavernous sinus containing blood that is cooler
than arterial blood by virtue of its previous passage past the nasal mucosa.
The nasal mucosa is cooled by respiratory evaporative heat loss. Heat exchange
between the rete carrying warm blood to the brain and the cool venous blood
reduces arterial blood temperature and produces SBC. In the years following
the discovery of SBC (Baker and Hayward,
1968) it was assumed that its biological purpose was to protect
the brain from thermal damage when body temperatures increased, for example
during exercise (Taylor and Lyman,
1972). This function for the rete was, however, dispelled by
studies done mostly in southern hemisphere animals exposed to hot and arid
conditions (Mitchell et al.,
2002), but also in reindeer in the northern hemisphere
(Aas-Hansen et al., 2000).
These studies showed that brain temperature was not cooled below arterial
temperature during exercise. The alternative proposal developed was that the
rete modulated thermal responses (Maloney
and Mitchell, 1997; Jessen,
2001) especially to achieve water conservation
(Jessen, 1998;
Mitchell et al., 2002).
The characteristics and mechanisms of thermoregulation in temperate zone
winters in large animals and their contribution to survival are less well
known. The essential conflict in winter is between increased energy
expenditure to maintain body temperature in extreme cold and the need to
conserve energy because of food shortages. It is obvious that this conflict is
resolved. For example, in two previous studies of thermoregulation in winter
in northern hemisphere artiodactyls a relatively constant body temperature has
been found. In one study on free-living mule deer, Sargeant et al.
(Sargeant et al., 1994)
recorded abdominal temperatures (Tabdominal) from seven
mule deer (Odocoileus hemionus) by radiotelemetry and found that in
winter the range of Tabdominal was on average slightly
narrower (range 37.8±0.2 to 38.4±0.3°C) than it was in
summer (range 38.0±0.2 to 38.8±0.2°C). In the second study,
Parker and Robbins (Parker and Robbins,
1984) measured rectal temperature in five mule deer and eight elk
(Cervas elephas) in captivity. They found that in both species
Trectal was constant at 38.6°C
(Parker and Robbins, 1984). It
was concluded that this constancy of temperature was achieved partly by growth
of a very thick fur undercoat and partly by behaviour, but in neither of these
studies were physiological mechanisms analysed.
A physiological mechanism that could underlie the relatively constant body
temperature that has been observed in wintering artiodactyls is reduced
cooling of the brain by the rete. The amount of cooling by the rete can be
controlled at three sites: at the nasal mucosa, at the veins directing the
pathway of returning blood, or at the rete itself. The rete is not innervated
so regulation at the last of these sites is unlikely and has not been shown.
Regulation of blood flow in the veins supplying the cavernous sinus is an
established mechanism (Johnsen et al.,
1987; Johnsen and Folkow,
1988) with the input controlled by Tbrain
(Kuhnen and Jessen, 1991). A
nasal input has been shown in sheep
(Maloney and Mitchell, 1997)
and in reindeer (Johnsen et al.,
1985). In reindeer, venous blood flow to the rete decreases when
low ambient temperatures cause nasal mucosa temperature
(Tnm) to fall. If so, then in winter conditions rete
activity should be minimal, and because changes in Tbrain
and Tcarotid will then occur together, thermoregulatory
responses will be maximal (Jessen and
Feistkorn, 1984), and variation in Tcarotid
will be reduced.
We report here the results of a study done specifically to investigate whether the functioning of the rete is reduced in winter, and more generally to provide comprehensive data on winter body temperature in artiodactyls on which to base ideas of how winter thermoregulatory mechanisms might contribute to survival. Our data suggest that rete activity is suppressed in pronghorns in winter, that this suppression is a crucial component of their winter thermoregulatory mechanisms and is a likely prerequisite for their survival. Our data also suggest that the rete has much wider thermoregulatory functions than those outlined above.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). This study, like our summer study, was done at the Tom Thorne/Beth Williams Wildlife Research Center at Sybille, southeastern Wyoming (41°47'N, 105°20'W). The study lasted for 71 days during winter from 9th November 2004 to 18th January 2005.
Animals
Five adult pronghorn antelope (two castrated males and three non-pregnant
females), body mass 40–50 kg, were captured by darting at Warren Air
Force Base, Cheyenne, WY, USA using thiafentanil at 0.1 mg
kg–1 body mass (Thiafentanil 10 mg ml–1;
Wildlife Pharmaceuticals, Inc., Fort Collins, CO, USA) and transported to the
Research Center at Sybille. Prior to the start of the study the animals were
kept in a small holding enclosure for 3–4 weeks so they could recover
from transport and acclimate to the local environment. For the duration of the
experiment they were kept in a 200 ha enclosure with five other pronghorns
where they were free-living for the recording period. Throughout the winter
they had access to alfalfa hay ad libitum supplemented by 2 kg
commercial deer pellets daily (Z+W Mills, Torrington, WY, USA).
Measurement of body temperature
Temperature was measured and recorded from four body sites (brain, carotid
artery, jugular vein and abdominal cavity) using small bead thermistors
(ABOE3-BR11KA 103K-L10, GE Thermometrics, Edison, NJ, USA). Data were stored
on data loggers (XTIC 32+34+36, Onset, Pocasset, MA, USA) connected to the
thermistors by a flexible coax cable (no. 83265, Belden, Richmond, IN, USA),
and able to record temperature between 34°C and 46°C, every 5 min, to
an accuracy of 0.04°C. The loggers were waxed (paraffin wax/Elvax,
Mini-Mitter, Sunriver, OR, USA) to make them waterproof and biologically
inert. After waxing, the loggers weighed approximately 55 g and had dimensions
of 50 mmx 45 mmx20 mm. Each of the thermistor/logger assemblies
was calibrated against a thermometer (Quat 100, Heraeus, Hanau, Germany) that
measures temperatures to an accuracy of ±1x10–2
K (Arce et al., 2006), and is a
recognized reference thermometer (Bock et
al., 2005).
Surgical procedures
At the time of surgery the animals were re-darted using thiafentanil and
anaesthetized with isoflurane (Abbott Animal Health, Abbot Park, IL, USA)
administered via a face mask at a concentration of 8% for induction and
1–2% for maintenance in oxygen. The effects of thiafentanil were
reversed with 2 mg kg–1 naltrexone (Nalterzel, 50 mg
ml–1; Wildlife Pharmaceuticals, Inc.).
Using aseptic surgical techniques, thermistors were implanted into the four body sites. The loggers for the brain and blood vessel thermistors were buried subcutaneously on the side of the neck about half-way between the head and thoracic inlet. The abdominal logger and its thermistor were implanted in the abdominal cavity.
Brain temperature: a thermistor was encased in a rigid guide tube (cellulose acetate butyrate tubing: World Precision Instruments, Sarasota, FL, USA; o.d. 3.2 mm, i.d. 1.98 mm, 34 mm in length) and pushed through a 3.2 mm hole drilled through the skull in the midline, 12.5 mm anterior to the suture between the frontal and parietal bones, so that the thermistor in the tip of the guide tube was near the hypothalamus. These coordinates were determined by prior dissection and analysis of pronghorn heads, and placement was confirmed at autopsy. The guide tube was attached to a head plate (LxWxH 22 mmx15 mmx9 mm) which was fixed to the skull by two 6 gauge, 15 mm long, self-tapping, stainless steel screws. No clinical signs of neurological lesions arose from this procedure.
Blood vessel temperature: thermistors in a blind-ended, thin-walled, polytetrafluorethylene (PTFE) tube approximately 100 mm long, made from a catheter (o.d. 0.9 mm; Straight Flush 4F Catheter, Cordis, The Netherlands), were inserted into the carotid artery and jugular vein about midway along the length of the neck in a direction opposite to that of blood flow so that the thermistor was detecting the temperature of free-flowing blood. The site of insertion in the vessels was closed by a purse string suture using 4/0 nylon.
Abdominal temperature: thermistors used to measure abdominal temperature were encased in the wax surrounding the logger. The abdominal thermistor was inserted into the abdominal cavity through an incision made at the left paralumbar fossa. The loggers were free floating in the abdomen.
All animals were given 5 ml dexamethasone (2 mg ml–1; Vedco, St Joseph, MO, USA) and 2 ml of a combination of penicillin G benzathine plus penicillin G procaine (300 000 units ml–1; Hanford Manufacturing Co., Syracuse, NY, USA) intramuscularly at the start of surgery. Enrofloxacin tablets (Baytril 22.7 mg: Bayer HealthCare LLC, Shawnee Mission, KS, USA) were placed in all surgical sites prior to wound closure.
Climatic conditions
Weather conditions during the study were measured using a 15 channel HOBO
weather station (Onset, Pocasset, MA, USA). Six variables were measured: black
globe temperature, ambient air temperature, solar radiation, relative
humidity, and wind speed and wind direction. Black globe temperature
(Tglobe) integrates air temperature, solar radiation and
wind speed. Snow precipitation was measured separately at the research station
and data from three other sites in Wyoming were also obtained, to estimate
snowfall in southeastern Wyoming over the study period.
Data analysis
At the end of the study the animals were killed, and the loggers and
thermistors removed. Temperatures recorded were calibrated against
pre-insertion calibration data. Data were obtained from all five brain
assemblies, all five carotid assemblies, four abdominal loggers (one logger
failed to launch) and three jugular vein assemblies (one jugular assembly
failed to launch and at autopsy it was found that the other had come out of
the vein). We obtained over 300 000 temperature measurements in total, over 40
days from pronghorn M476, 52 days from pronghorn F471, 53 days from pronghorn
M475, 68 days from pronghorn F473 and 68 days from pronghorn F474.
The data were consolidated first by pooling the 12, 5 min interval data points obtained from each logger for each hour of measurement to produce 24 average hourly temperatures for each animal for each day. These hourly averages for the five animals were, in turn, averaged to produce a weighted mean hourly temperature for them as a group. These averages could be further pooled for all study days or component days of the study period to provide a comprehensive overview of body temperature throughout the recording period.
Specifically, body temperature data were consolidated into three categories consisting of the six warmest days (Tglobe 5.8±1.9°C), six coldest days (Tglobe –10.2±2.2°C) and six intermediate days (Tglobe 0.1±0.2°C) in the study period, to assess whether thermoregulatory mechanisms differed depending on environmental conditions. A second consolidation was to average daily means into a week, to produce nine separate weekly temperature profiles for each body site over the study period. These nine weekly periods were used to establish correlations between the weather variables and body temperatures in each week of the study period. Similar consolidations were made for weather data using the two data points recorded each hour for each of the variables.
Calculation of cerebral blood flow
We calculated cerebral blood flow (CBF) in each animal using a modified
convective heat loss equation (Lust et
al., 2007):
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T is the difference between Tbrain
and Tcarotid. The units of CBF are g 100
g–1 min–1, which was converted to ml 100
g–1 min–1 by dividing by the density of
blood (1.055 g ml–1). This equation was used to assess the
extent to which observed differences between the carotid and brain
temperatures that we found in this study could be attributed to increased or
decreased removal of heat by CBF.
Statistics
The data were entered into an Excel data analysis spreadsheet. Three
statistical tests were used. For comparison of summer and winter temperatures,
Student's two-sample t-test assuming unequal variance was used with
P<0.05 being regarded as significant. For assessing whether body
site had an influence on recorded temperatures we used repeated measures ANOVA
and an ANOVA single-factor test to compare temperatures between body sites,
with P<0.05 being significant. Relationships between temperatures
and environmental cues were assessed by linear regression analysis.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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20°C colder, mean
Tglobe was 25°C colder, mean daytime solar
radiation was halved (186±20 vs 380±107 W
m–2), and mean day length was 5 h 45 min shorter. Wind speed
was 2.2±0.5 m s–1 in winter (vs
1.1±0.3 m s–1 in summer). Mean snowfall at four
weather stations in SE Wyoming was 668 mm over the study period with 1085 mm
being recorded at the Research Center at Sybille.
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Body temperature
Mean temperature for the four body sites in each of the animals and the
weighted means for all animals are shown in
Table 2. For comparison the
mean summer temperatures for the same body sites also are shown. Body site had
a significant influence on temperature (d.f.=2, F=17.5097,
P=0.0003). As in summer, in winter Tbrain was
higher than Tcarotid (d.f.=1, F=7.3266,
P=0.0268) and Tjugular (d.f.=1,
F=28.1442, P=0.0007). Tabdominal was
higher than Tjugular (d.f.=1, F=15.7443,
P=0.0041) but not different from Tbrain (d.f.=1,
F=3.24, P=0.1096) or Tcarotid (d.f.=1,
F=0.8757, P=0.3768). Tcarotid was
significantly higher than Tjugular (d.f.=1,
F=10.5263, P=0.0118). Mean temperatures for
Tbrain, Tcarotid,
Tabdominal and Tjugular were not
significantly different between summer and winter, but minimum
Tbrain (38.5±0.4°C) and minimum
Tcarotid (37.8±02°C) were significantly higher
in winter than in summer (t7=2.718, P=0.017).
Maximum Tbrain and Tcarotid were not
different in summer and winter (t7=1.1746,
P=0.139).
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Between individual animals maximum and minimum Tcarotid
and Tbrain varied
(Table 3). The mean values for
minimum Tcarotid in winter were significantly lower than
those for Tbrain (d.f.=1, F=11.0860,
P=0.010) but maximum Tcarotid and
Tbrain were not different (d.f.=1, F=3.751,
P=0.0888). Comparing summer with winter, the difference between
maximum and minimum Tcarotid of 1.8±0.7°C was
significantly narrower than it was in the summer (3.1±0.4°C;
t7=3.52, P=0.0098). The frequency distribution of
0.1°C temperature intervals for Tbrain,
Tjugular and Tcarotid is shown in
Fig. 1. In summer
Tcarotid varied between 35.8 and 40.3°C
(T=4.5°C) and Tbrain varied between
37.4 and 40.7°C (T=3.3°C). In winter
Tcarotid varied between 37.8 and 40.6°C
(T=2.8°C) and Tbrain varied between
38.0 and 40.5°C (T=2.5°C). In addition, in summer the
frequency distributions had long tails to the left while in winter the tails
were shifted to the right.
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Factors affecting body temperature
Unlike in summer, where we established that changes in
Tcarotid over the 14 week study period correlated
significantly with Tglobe mean (r=0.78,
P<0.001) and range (r=0.916, P<0.001), no
similar relationship was found for winter (r=0.272,
P>0.05 and r=–0.188, P>0.05,
respectively) probably because Tcarotid varied very little
each day (0.9±0.1°C vs 1.6±0.7°C in summer).
However, each animal did have an identifiable maximum and minimum daily
Tcarotid, and consecutive maximum and minimum
Tcarotid occurred on average 23 h 55 min ±88 min
and 23 h 18 min ±102 min apart over the entire study period.
When the times of maximum and minimum Tcarotid in each
of the 9 weeks of the study period were correlated with the external
environmental cues of the time of Tglobe maximum and
Tglobe minimum, day length, and the time of sunrise and
sunset, the only significant correlations were between the time of maximum
solar radiation and the time of maximum Tcarotid
(r=0.569, P<0.01), and between the time of minimum
Tcarotid and the time of sunset (r=0.601,
P<0.01). The mean time of maximum Tcarotid
during winter (15 h 11 min ±62 min; range 13 h 45 min to 16 h 43 min)
occurred significantly earlier in winter than in summer
(t18=8.24, P=1.59e–07) and
closer to the time of maximum solar radiation (11 h 52 min ±25 min). In
summer, maximum Tcarotid occurred at 18 h 47 min
±65 min and the time of solar maximum was 12 h 24 min ±24 min,
so body temperature was highest 6.5 h after solar `noon'. In winter the
delay was 3.5 h. The time of minimum Tcarotid in
winter was earlier (07 h 36 min ±78 min) than in summer (09 h 18 min
±72 min) but not significantly so.
Respiratory evaporative heat loss
The difference between Tcarotid and
Tjugular is an indicator of whether heat loss is occurring
from the nasal mucosa. By this measure, during winter nasal cooling occurred
continuously (Fig. 2). Mean
Tjugular in winter was the same as it was in the summer
(Table 2), but the pattern of
Tjugular was different. In summer, maximum
Tjugular was always higher than the simultaneously
measured Tcarotid and at low Tcarotid
the mean, maximum and minimum Tjugular were higher than
the simultaneously measured Tcarotid. In winter, maximum,
minimum and mean Tjugular were always lower than the
simultaneously measured Tcarotid
(Fig. 2).
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39.5°C threshold for
SBC observed in summer (Figs 1,
2). Brain warming was minimal
(Fig. 2). Minimum
Tbrain consistently was above simultaneously measured
Tcarotid, a pattern quite different from the pattern found
in summer. Moreover, as Fig. 2
shows, the range of temperatures recorded narrowed as the days became colder.
The range of Tcarotid and Tbrain was
3.3°C on the warmest days, 2.5°C on intermediate days and 2.3°C on
the coldest days.
The absence of SBC implies that in winter the cooling effect of the rete
was much reduced, a conclusion supported by comparing the relationship between
Tcarotid and Tbrain in pronghorn in
summer (Fig. 3A)
(Lust et al., 2007) and in
winter (Fig. 3B), and the
relationship we have found in summer in the horse, an animal that has no rete
(Fig. 3C)
(Mitchell et al., 2006).
Fig. 3 also shows the
calculated CBF in each case. In winter the relationship between
Tbrain and Tcarotid was more similar
to that of the horse than it was to pronghorn in the summer: there was no SBC,
Tbrain minima rarely were less than contemporaneous
Tcarotid, the range of Tbrain and
Tcarotid was right shifted compared with summer and was
higher than it was in the horse by 0.5°C, and changes in
Tbrain and Tcarotid were highly
correlated. The product-moment correlation (r) between
Tbrain and changes in Tcarotid in
summer was 0.83, in winter it was 0.99, and in horses it was 1.0, over the
range of temperatures recorded.
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It can also be seen that in summer many of the calculated values for CBF
lie above or below the theoretical maxima and minima for CBF
(Fig. 3A)
(Lust et al., 2007). In winter
virtually all of the CBF values lie within these limits
(Fig. 3B), while in the horse
the range of calculated CBF is very narrow
(Fig. 3C). Thus, in winter in
pronghorns (and in horses) the changes in Tbrain could be
accounted for by increases or reductions in CBF alone. In contrast, in
pronghorn in summer the differences between Tbrain and
Tcarotid cannot be accounted for by changes in CBF alone,
and other mechanisms such as cooling of blood in the rete combined with
changes in CBF must be occurring (Lust et
al., 2007).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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9 h vs 15 h in summer).
Snowfalls are frequent and snow is persistent. In a climate like this
pronghorn grow a very thick fur undercoat that is a highly effective insulator
(O'Gara and Yoakum, 2004)
and/or migrate. If migration is blocked, many thousands die because their body
fat content is low [at 3 g 100 g–1 vs 27–32 g
100 g–1 for cattle (Eaton
and Konner, 1985; O'Gara and
Yoakum, 2004)], and energy depletion leads to hypothermia. If food
is available then, as our study shows, despite exposure to very cold
environmental conditions they, like mule deer and elk
(Parker and Robbins, 1984;
Sargeant et al., 1994), can
maintain a relatively constant body temperature of around 38.5°C. This
constancy, like that of mule deer and elk, is achieved partly by growth of a
very thick fur undercoat and partly by behaviour. We did not quantify the
contributions of these factors to the regulation of body temperature in
pronghorns but it was clear from inspection that they have two hair layers.
One layer consists of fine, short and closely packed hairs, which grows in
winter and is shed in summer. The other persists throughout the year and
consists of thick, long and separated hairs. We do not know whether reduced
movement formed part of their winter behaviour pattern as it does in red deer
(Arnold et al., 2004) but it
was clear that the pronghorns made use of the landscape to minimize the
effects of ambient conditions as they do in summer. They thus were able to
maintain their body temperature without being able to migrate.
They also seem to shift their daily temperature cycles seasonally to make
use of solar radiation in winter and to avoid it in the summer. Maximum
Tcarotid occurred significantly earlier in winter than in
summer and the time of maximum Tcarotid was weakly but
significantly correlated with the time of maximum solar radiation. We also
noted that the time of minimum Tcarotid was linked to
sunset but occurred at 07:30 h. An explanation for this finding is that
the longer the length of night (the earlier the sunset) the larger the fall in
Tcarotid. Metabolic rate is depressed at night by up to
60% in red deer (Arnold et al.,
2004) and in pronghorn early morning Tcarotid
could be up to 2.7°C colder than maximum Tcarotid
suggesting that a similar effect occurred.
We found no SBC in winter even though Tbrain and
Tcarotid exceeded temperatures at which SBC occurred in
summer. There was also a higher and right-shifted range of
Tbrain and Tcarotid with a frequency
distribution (Fig. 1) showing
that in winter lower body temperatures occurred less frequently than they did
in the summer, while in summer it was high body temperatures that occurred
less frequently. Tbrain and Tcarotid
were also more closely correlated than in summer, and
Tjugular was consistently lower than
Tcarotid. The tight coupling of Tbrain
and Tcarotid produced a smaller variation in the range of
body temperature in the pronghorns in winter than we found in summer. This
result supports the observations made by Parker and Robbins
(Parker and Robbins, 1984) in
mule deer and elk, and those of Sargeant et al.
(Sargeant et al., 1994) in
mule deer.
The differences in temperature profiles between summer and winter can be
explained by a much reduced functioning of the rete cooling mechanism. In
short, in winter, pronghorns appear to thermoregulate in a way very similar to
that of a non-rete animal (Fig.
3). This conclusion raises the question of why such a response
would be advantageous. The most parsimonious explanation is that the response
conserves energy, although this conclusion is counterintuitive. More precise
regulation of body temperature should increase energy consumption
(Lindstedt and Boyce, 1985).
However, energy would be conserved if the result of a higher
Tbrain was depression of appetite and metabolism. These
two responses are well established mechanisms for reducing energy use in
herbivores in winter (Moen,
1978; Arnold et al.,
2004). Both appetite and metabolism are depressed by high body
temperature in pigs through suppression of the release of leptin and thyroid
hormones (Collin et al., 2002),
but a similar link has not yet been evaluated in herbivore artiodactyls. These
effects, if they exist, combined with the growth of fur and its consequential
lowering of the thermoneutral zone
(Nilssen et al., 1984) could
significantly reduce energy use.
Rete function is controlled by the regulation of blood flow from the nasal
mucosa to the cavernous sinus that surrounds the rete. Johnsen et al.
(Johnsen et al., 1985)
identified three channels for blood returning from the nasal mucosa. One
channel could divert cold nasal blood to the cavernous sinus via
vasodilatation of the angularis oculi vein (AOV) and constriction of the
facial vein to effect SBC, with the opposite occurring to inhibit carotid rete
cooling (Johnsen and Folkow,
1988). A second channel directed cold blood to the jugular vein
via the dorsal nasal vein (DNV) to effect whole-body cooling, and a third
channel was a countercurrent heat exchanger. Johnsen and colleagues
(Johnsen et al., 1985)
theorized and later showed (Johnsen et
al., 1987) that when heat conservation was needed, the DNV and
vessels of the nasal mucosa were constricted and warm blood entering the nasal
mucosa passed cold venous blood returning from it, warming the venous blood
and cooling the arterial blood to the periphery so that heat loss was
minimized. The venous effluent entered the sphenopalatine and jugular veins at
temperatures similar to arterial temperature. These studies showed that
constriction of nasal mucosa vessels was caused by decreases in
Tair and nasal mucosa temperature
(Tnm) until at Tair and
Tnm, and below 0°C there was no blood flow in the DNV
(Johnsen et al., 1985;
Johnsen et al., 1987). When
heat dissipation and/or whole-body cooling were required from the brain or
body, nasal cooling increased and blood flow in the nasal mucosa vessels was
unidirectional with cold effluent blood entering either the AOV en route to
the cavernous sinus/rete to effect SBC, or the jugular vein to effect
whole-body cooling. In sheep, similar pathways exist
(Nijland et al., 1989;
Maloney and Mitchell, 1997).
In pronghorns the AOV seems to be a minor pathway, if a pathway at all, and
they have two main pathways for the return of venous blood from the cooling
surfaces of the nose – the DNV and the palatine system
(Carlton and McKean, 1977).
Despite these anatomical differences, our data can be explained by the
Johnsen et al. (Johnsen et al.,
1985) model. For example, if cold environmental temperatures cause
Tnm to fall and cause increasing constriction of the DNV
then it could be predicted that Tjugular would not
decrease because it too would be deprived of cold blood. Our data show that in
pronghorn in winter, Tjugular decreased less, and varied
far less, than it did in summer. Constriction of the DNV in pronghorns also
would direct blood to the palatine veins and countercurrent warming of blood
would occur. If this warm blood entered the CS surrounding the rete, rete
cooling would be reduced and the absence of SBC that we found in winter, and
the higher average Tbrain, would be explained. In these
circumstances, however, removal of heat from the brain and control of brain
temperature must depend on changes in CBF. As
Fig. 3B shows, virtually all
the temperature gradients we found in pronghorn in winter could be accounted
for by changes in CBF alone.
In pronghorn, regulation of the nasal countercurrent system and the rete
countercurrent system must be independent because typically in pronghorn
Tjugular was colder than Tcarotid
while at the same time rete functioning was suppressed. Thus flow of cold
blood from the nasal mucosa to the jugular vein was occurring at the same time
that flow of cold blood to the veins supplying the cavernous sinus was being
reduced. The first and traditional regulator of the direction of nasal venous
blood flow is a rising Tbrain, which increases nasal
cooling and, when it reaches 39.5°C, triggers SBC
(Kuhnen and Jessen, 1991). We
could only detect this response in the summer. The second regulation is
initiated by a low environmental temperature and predominates over the
mechanism that regulates SBC. The location of the thermoreceptor that detects
low ambient temperature is likely to be the nose and nasal mucosa, which are
the only parts of the body that are unprotected from environmental
temperature. A thermoreceptor sensitive to cold is present in the nasal cavity
of sheep (Bligh, 1963;
Maloney and Mitchell, 1997)
and in reindeer (Johnsen et al.,
1985). In sheep a cold Tnm and constriction of
the AOV occur only when Tcarotid is at the low end of its
temperature range (Maloney and Mitchell,
1997). At high Tcarotid, a low
Tnm increases AOV flow and SBC in sheep, whereas in
pronghorn and reindeer this latter response appears to be absent. In the sheep
study, however, Tnm was never less than 15°C, while in
reindeer and presumably in pronghorn, Tnm approached the
low temperatures that inhibit rete cooling at all
Tcarotid. Thus our data are consistent with the idea that
provided Tnm is sufficiently low, nasal thermoreceptors
may independently regulate the supply of blood to the cavernous sinus,
reducing rete cooling while allowing some whole-body cooling via the jugular
vein.
If this interpretation of our data is correct, then our results, apart from
providing a mechanism for the conservation of energy in winter, extend our
understanding of the functioning of the rete. The rete's traditional role and
biological purpose is SBC, and the protection of an allegedly more vulnerable
brain from thermal damage. This role has been dispelled by a number of studies
that have shown consistently that during exercise, because of increased
sympathetic nerve activity, and/or a change from nasal to open mouth breathing
that bypasses the nasal mucosa, rete function and SBC are reduced and brain
temperature increases. Whole-body cooling results
(Jessen, 1998). Jessen
proposed therefore that the role of the rete was to modify thermoregulatory
responses and conserve water (Jessen,
1998; Jessen,
2001). Our previous study on pronghorns in the summer supports
this conclusion. Dissociation of Tbrain and
Tcarotid in pronghorns resulted in a low variation in
Tbrain and a wide variation in
Tcarotid. Our winter data extend this role of the rete. In
winter, suppression of rete activity results in a narrow and higher range of
Tbrain and Tcarotid, and we speculate
that corollaries are depression of appetite and metabolism and conservation of
energy, especially if their pelage provides excellent insulation.
The rete, therefore, seems to be able to cool the brain when Tbody is high but also to regulate Tbrain throughout the year to achieve optimum thermoregulatory responses according to environmental or seasonal needs, even to the extent of differentiating between `warm' and `cold' days in winter. It functions over a wide range of body temperatures, and its effects can be adjusted to accommodate high and low environmental temperatures.
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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