Content uploaded by Justin Boyles
Author content
All content in this area was uploaded by Justin Boyles on Jan 02, 2018
Content may be subject to copyright.
Torpor Patterns in Desert Hedgehogs (Paraechinus aethiopicus) Represent
Another New Point along a Thermoregulatory Continuum
Justin G. Boyles
1,
*
Nigel C. Bennett
2,3
Osama B. Mohammed
2
Abdulaziz N. Alagaili
2
1
Cooperative Wildlife Research Laboratory, Department of
Zoology, Southern Illinois University, Carbondale, Illinois;
2
King Saud University Mammals Research Chair, Department
of Zoology, College of Science, King Saud University, P.O. Box
2455, Riyadh 11451, Saudi Arabia;
3
Mammal Research Institute,
Department of Zoology and Entomology, University of Pretoria,
Pretoria 0002, South Africa
Accepted 2/13/2017; Electronically Published 4/12/2017
ABSTRACT
Documenting variation in thermoregulatory patterns across
phylogenetically and geographically diverse taxa is key to un-
derstanding the evolution of endothermy and heterothermy in
birds and mammals. We recorded body temperature (T
b
)in
free-ranging desert hedgehogs (Paraechinus aethiopicus)across
three seasons in the deserts of Saudi Arabia. Modal T
b
’s(357–
36.57C) were slightly below normal for mammals but still warmer
than those of other hedgehogs. The single maximum T
b
recorded
was 39.27C,whichiscoolerthanmaximumT
b
’s recorded in
most desert mammals. Desert hedgehogs commonly used tor-
por during winter and spring but never during summer. Torpor
bouts occurred frequently but irregularly, and most lasted less
than 24 h. Unlike daily heterotherms, desert hedgehogs did
occasionally remain torpid for more than 24 h, including one
bout of 101 h. Body temperatures during torpor were often
within 27–37C of ambient temperature; however, we never re-
corded repeated bouts of long, predictable torpor punctuated by
brief arousal periods similar to those common among seasonal
hibernators. Thus, desert hedgehogs can be included on the
ever-growing list of species that display torpor patterns inter-
mediate to traditionally defined hibernators and daily hetero-
therms. Extant hedgehogs are a recent radiation within an an-
cient family, and the intermediate thermoregulatory pattern
displayed by desert hedgehogs is unlike the deeper and more
regular torpor seen in other hedgehogs, suggesting that this may
be a derived—as opposed to ancestral—trait in this subfamily.
We suggest that this family (Erinaceidae) and order (Eulipo-
typhla) may be important for understanding the evolution of
thermoregulatory patterns among Laurasiatheria and mammals
in general.
Keywords: body temperature, Ethiopian hedgehog, Eulipo-
typhla, heterothermy, hibernation.
Introduction
Describing variation in thermoregulatory and body tempera-
ture (T
b
) patterns and determining the distribution—both phylo-
genetically and geographically—of those patterns in mammals
and birds is vital to understanding the evolutionary history of
endothermy. Of special interest is how various derivations of
heterothermy relate to the evolutionary history of endothermy.
Patterns of heterothermy have often been considered distinct
(Geiser 1998), with daily heterothermy and hibernation (seasonal
heterothermy) differentiated by parameters including length of
torpor bouts and metabolic rate during torpor (Geiser and Ruf
1995). Increased interest in the topic and advances in technology
have led to an increase in research on species from tropical, sub-
tropical, and desert regions, and exceptions that fall in-between
the normal classifications of heterothermy are common enough
(Lovegrove et al. 2001; Lovegrove and Genin 2008; Geiser and
Mzilikazi 2011; Geiser and Martin 2013) that many researchers
now view the metabolic plasticity between normothermy and
hibernation as a continuum(Canale et al. 2012; Boyleset al. 2013;
van Breukelen and Martin 2015) arising from ancestral hetero-
thermy (Lovegrove 2012a).
Differentiating between the two competing views of hetero-
thermy (distinct categories vs. a continuum) will become easier
as more data on T
b
of phylogenetically and geographically di-
verse species become available. One such phylogenetically im-
portant order is the Eulipotyphla (solenodons, shrews, moles,
hedgehogs, and moonrats), which occupy an interesting (albeit
contentious) position in the mammalian phylogeny (Mouchaty
et al. 2000; Douady et al. 2002). They are most commonly placed
sister to the rest of Laurasiatheria (Douady et al. 2002; Bininda-
Emonds et al. 2007), diverging 75–85 million years ago (Douady
and Douzery 2003; Hallström and Janke 2010). The Eulipo-
typhla have been singled out as important in understanding the
evolution of heterothermy in mammals because of their early
divergence from the other laurasiatherians (Lovegrove 2012b).
Among the Eulipotyphla, the thermal physiology of hedge-
hogs (subfamily Erinaceinae) has long interested researchers
*Corresponding author; e-mail: jgboyles@siu.edu.
Physiological and Biochemical Zoology 90(4):445–452. 2017. q2017 by The
University of Chicago. All rights reserved. 1522-2152/2017/9004-6169$15.00.
DOI: 10.1086/691542
445
This content downloaded from 131.230.059.106 on April 17, 2017 05:37:48 AM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
(Dmi’el and Schwarz 1984; Soivio et al. 1968). Hedgehogs typi-
cally maintain normothermic T
b
between 337and 357C (Shkolnik
and Schmidt-Nielsen 1976; Fowler and Racey 1990; Król 1994;
Hallam and Mzilikazi 2011), which is intermediate between
monotremes, metatherians, and more basal placental mammals
(T
b
of 307–337C; Grant 1983; Grigg et al. 2003; Nicol and An-
derson 2006; Lovegrove and Genin 2008) and the more typical
mammalian T
b
of 377–387C. Even among the Eulipotyphla, hedge-
hogs display unusually low T
b
(Whittowetal.1977;Campbell
et al. 1999). While a large body of literature exists on thermo-
regulation of hedgehogs, relatively little work has been pub-
lished on T
b
patterns of this taxon in the wild, especially in arid
environments. Laboratory and semicaptive studies suggest that
the European hedgehog (Erinaceus europaeus) probably under-
goes the longest and deepest torpor bouts among hedgehogs
(Dmi’el and Schwarz 1984; Soivio et al. 1968; Fowler and Racey
1990; Webb and Ellison 1998), but other hedgehog species also
display relatively long torpor bouts characterized by low T
b
(Hal-
lam and Mzilikazi 2011; Mouhoub-Sayah et al. 2012). The four
species for which T
b
data are available come from a variety of
climates (temperature and subtropical) and habitats (woodlands
and grasslands), and all use torpor.
We recorded T
b
of free-ranging desert hedgehogs (Paraechi-
nus aethiopicus) across three seasons in a harsh desert environ-
ment. Desert hedgehogs are unusual among the hedgehogs be-
cause of their adaptations to extremely arid environments; thus,
their thermoregulation is likely to be unusual as well. Given that
heterothermy seems ubiquitous among the hedgehogs, we ex-
pected heterothermy in desert hedgehogs as well. However, given
the unusual ecology of this species relative to other hedgehogs, we
had no a priori expectations about the form of heterothermy.
Methods
Study Species
The desert hedgehog (150–600 g) is an arid-adapted insectivore
found throughout the nonmountainous regions of the Arabian
Peninsula and in extreme northern Africa. Relatively little is
known about the natural history, behavior, and ecology of this
species compared with European hedgehogs and several species
and hybrids commonly kept as pets. Courtship behavior most
commonly occurs during late winter and into early spring (Ya-
maguchi et al. 2013). They are mostly nocturnal, and seasonal
activity levels of captive animals decrease considerably during
midwinter (Al-Musfir and Yamaguchi 2008), and T
b
appears to
drop when exposed to low ambient temperatures (as cited by
Corbet 1988), so it has been assumed they hibernate. It is also
known that desert hedgehogs bask during cool winter days, pre-
sumably to help control T
b
(Abu Baker et al. 2016)
Experimental Design
We hand captured desert hedgehogs over two sessions in sandy
habitats on or near date farms of the Unizah province, Saudi
Arabia (26.1367N, 43.9757E). We started each capture period
just after sunset in winter and around midnight in summer. The
first collection period was in summer 2013 (June 2013). The
second collection period was in winter 2013–2014 (November
2013). We captured 20 animals in each season.
We temporarily housed the hedgehogs in an animal facility
at the Department of Zoology of King Saud University in Ri-
yadh. We used temperature-sensitive data loggers set to re-
cord at 1-h intervals (0.06257C resolution, iButtons, DS1922L,
4.2 g withwax, Maxim Semiconductors,Dallas) to measurecore T
b
.
We did not have proper equipment available to fully calibrate
data loggers. Previous experience with this model of data logger
indicates that most are accurate within values claimed by the
manufacturer (0.57C) and that precision within a batch is high
(J. G. Boyles, personal observation). However, a weakness of this
model is that a small proportion of them deviate outside these
values. Therefore, before implanting the data loggers, we com-
pared their recorded temperatures to measured air temperatures
to remove any data loggers with a clear offset. Thus, we are
confident that our measurements are within 50.57C of actual T
b
values. We then coated the data loggers with biologically inert wax
and had them implanted intraperitoneally by a licensed veteri-
narian following standard procedures. The veterinarian im-
planted data loggers after anesthetizing animals with isoflurane
and sutured the incision with absorbable catgut. Animals were
given a long-acting, broad-spectrum antibiotic (Oxytetracy-
cline, Pfizer) to minimize chances of postsurgery infection and
were held for at least 7 d to ensure recovery from surgeries. Fi-
nally, to facilitate recapture, we clipped a few spines and glued
(Torbot Liquid Bonding Cement, Torbot) radio transmitters (RI-
2B, 10 g, Holohil Systems) to the dorsal skin. Combined, the data
logger and transmitter were well below 5% body mass of all in-
dividuals. We released the animals in the same area where we
had captured them and attempted to recapture them approx-
imately 2 mo after the first capture period and 5 mo after the
second capture period. The first period was completed wholly
during summer. The second period began in early winter and
ended in late spring/early summer. Recapture was lower during
summer because hedgehogs more commonly left the area or
were killed on roads. We euthanized animals using ether to re-
trieve data loggers. These capture procedures were conducted
under permits issued by the Saudi Wildlife Authority. Experi-
mental protocols were approved by the Animal Use and Care
Committee of the University of Pretoria (ethics clearance EC029-
16).
We calculated basic descriptive statistics for each individual
(modal, minimum, and maximum T
b
) as well as the hetero-
thermy index (HI), which is a biologically meaningful modifi-
cation of a simple standard deviation that quantifies the amount
of variation around the modal T
b
instead of the mean T
b
(Boyles
et al. 2011b) and allows for comparison of thermoregulatory
patterns of species with diverse physiologies (Boyles et al. 2013).
During summer, we recorded hourly air temperature (T
a
) in the
shade using an iButton. We recorded T
a
in the same way during
the second study period but lost the data, so we downloaded air
temperature from a weather station approximately 27 km north-
west of the study site (Prince Nayef bin Abdulaziz Regional Air-
port). Air temperatures on thestudy site may therefore be slightly
446 J.G.Boyles,N.C.Bennett,O.B.Mohammed,andA.N.Alagaili
This content downloaded from 131.230.059.106 on April 17, 2017 05:37:48 AM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
different than reported, and we make only qualitative compari-
sons between T
a
and T
b
during winter. We compared modal,
minimum, and maximum T
b
and HI values between seasons and
sexes using PROC GLM in SAS University Edition (SAS Insti-
tute, Cary, NC), after verifying that the data met all assump-
tions of that test. We used PROC MIXED to evaluate the effect
of maximum T
a
on maximum T
b
. For all analyses with seasonal
comparisons, we considered data for the first study period as
summer (June 16–August 16, 2013), and we split the second
study period into winter (January 7–March 15, 2014) and spring
(March 16–May 30, 2014). We chose to split the winter and
spring data on these dates somewhat arbitrarily on the basis of
a noticeable shift in thermoregulatory patterns of every indi-
vidual around mid-March. This also coincides with the period of
increased activity reported for this species in captivity (Al-Musfir
and Yamaguchi 2008). Because the data are from the same in-
dividuals, winter and spring data are not completely indepen-
dent, but we could not account for individuals in the analyses
because of the inclusion of summer data, which are from different
individuals. We avoid quantification of torpor patterns based on
the torpor cut-off method (Boyles et al. 2011a) and use only
approximate descriptions of torpor patterns for the duration of
torpor bouts. The data are available from the authors for analyses
associated with future meta-analyses.
Results
We successfully recovered data for five individuals (three males,
two females) during the first (summer) capture session and 13
individuals (nine males, four females) during the second(winter/
spring) capture session. There was more variation in descriptors
of thermoregulatory patterns among seasons than between sexes
(table 1; fig. 1). Body temperatures were normally distributed
when pooled by season but were clearly skewed when pooled by
hour within season (fig. 2). Generally speaking, T
b
’s were highest
in late afternoon during summer (fig. 2). Mean modal T
b
’s were
significantly higher during summer (P!0.0001) than spring or
winter, during which time modal T
b
’s were nearly identical (35.87
vs. 35.97C; Pp0.8890; table 1). Mean maximum T
b
’s varied
significantly among seasons (F
2, 25
p112.2, P!0.0001) but were
again similar in winter and spring (37.07vs. 36.97C; Pp0.5713).
During summer, maximum T
b
was significantly affected by max-
imum T
a
(F
1, 212
p15.64, Pp0.0001), but there was no significant
effect of individual (F
4, 212
p2.22, Pp0.0684). Ignoring indi-
vidual then, the equation for a simple regression of the effects of
maximum T
a
on maximum T
b
is T
b
p33.06 10.0998T
a
(R
2
p
0.047, Pp0.0012). The single warmest T
b
recorded was 39.27C.
Minimum T
b
’s were significantly different in all seasonal com-
parisons (P!0.0001 in all comparisons) in the expected order
(summer minimum T
b
1spring minimum T
b
1winter mini-
mum T
b
; table 1). The single minimum T
b
recorded during winter
was 10.97C, and the tenth percentile was 14.97C at 0900 hours
during winter (fig. 2). During winter and spring, the lowest T
b
’s
were recorded early morning and were slightly out of phase with
T
a
(fig. 3). During summer, the lowest T
b
’s were recorded just
after sunrise.
Every individual commonly entered torpor during winter and
spring, but none did so during summer (fig. 1). HI values were
significantly different in all seasonal comparisons (P!0.0001 in
all comparisons) in the expected order (summer HI !spring
HI !winter HI; table 1). Among all the included descriptors of
thermoregulatory patterns, only HI values were significantly
different between sexes (F
1, 25
p11.33, Pp0.0025) and in the
season #sex interaction (F
2, 25
p5.28, Pp0.0122). The HI values
for males and females were similar in summer and spring but
were significantly higher for females (9.457C) than males (5.857C)
in winter (Pp0.0003). All but 10 recorded torpor bouts were
less thana day long, but thelongest bout was morethan 101 h (fig.1;
estimated conservatively excluding cooling and warming phases
of the bout). Although the number of torpor bouts longer than
24 h was small, they appear more common among females (six
bouts by four individuals) than males (four bouts by nine indi-
viduals). There were several individuals that used multiday
torpor bouts well into spring, including one individual that was
torpid for ∼50 h during May 18–20, 2014. Similar to shorter
bouts in spring and in contrast to longer bouts in winter, T
b
Table 1: Summary statistics of thermoregulatory patterns in desert hedgehogs (Paraechinus aethiopicus) in Saudi Arabia
Season nModal T
b
Heterothermy index Minimum T
b
Maximum T
b
Summer:
Male 3 36.4 5.25 .76 5.19 34.0 5.40 38.6 5.57
Female 2 36.5 5.00 .82 5.07 34.0 5.84 39.2 5.01
Combined 5 36.5 5.18 .78 5.14 34.0 5.50 38.9 5.52
Winter:
Male 9 35.8 5.23 5.85 51.76 13.7 52.47 37.0 5.16
Female 4 35.9 5.00 9.45 5.69 11.8 5.69 37.0 5.14
Combined 13 35.8 5.20 6.96 52.28 13.1 52.23 37.0 5.15
Spring:
Male 9 35.9 5.26 3.63 5.86 22.3 5.32 36.9 5.27
Female 4 35.9 5.10 4.75 5.25 22.3 5.29 36.9 5.28
Combined 13 35.9 5.22 3.98 5.90 22.3 5.30 36.9 5.26
Note. All euthermic and torpid data are included, and values are presented as means 5SD. T
b
, body temperature.
Body Temperature of Desert Hedgehogs 447
This content downloaded from 131.230.059.106 on April 17, 2017 05:37:48 AM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
remained above 227C during these long spring torpor bouts.
The lowest T
a
recorded at the airport during any of these spring
bouts was 227C.
At some point during midwinter, nearly every individual
went through a period of several days to several weeks with low
nighttime T
b
’s but short torpor bouts (fig. 3). While we did not
have T
a
data from the site and specifically from within the bur-
rows used by these animals, minimum T
b
’s often approached
(and were occasionally below) T
a
recorded at a nearby weather
station. Unfortunately, without T
a
data from the site, it is diffi-
cult to quantitatively analyze the T
b
-T
a
differential.
Discussion
The data on T
b
patterns reported here are some of the first for a
small desert mammal across multiple seasons. Desert hedgehogs
maintain relatively low normothermic T
b
’s during all seasons,
with summer modal T
b
’s of only 36.57C (table 1). There was no
indication of torpor during summer, but short torpor bouts with
low T
b
’s(!157C) were common in winter, and short torpor
bouts with moderate T
b
’s(1227C) were common in spring, when
reproductive activity increases (Alagaili et al., forthcoming).
Mammals often display larger variation in T
b
in winter than
summer (Chappell and Bartholomew 1981; Mustonen et al. 2007;
Boyles et al. 2013), but the combination of strict homeothermy
during summer and short torpor bouts during winter is rarely
reported for mammals (Ruf et al. 1989; Mzilikazi and Lovegrove
2004). More commonly discussed in the literature are species
that (1) maintain homeothermy (or rarely use heterothermy)
during summer and hibernate during winter (e.g., Zervanos
and Salsbury 2003; Levesque and Tattersall 2010; Whiteman
et al. 2015) or (2) use some form of heterothermy in all seasons
(e.g., Geiser and Baudinette 1987; Bartels et al. 1998; Dzal and
Brigham 2013). It is unclear whether these patterns are more
common or are simply overrepresented in the literature be-
cause of geographic biases of researchers (McKechnie and
Mzilikazi 2011). It seems logical that use of daily torpor during
winter and homeothermy during summer should be common,
especially among subtropical and desert species inhabiting en-
vironments that are hot during summer and either cold or offer
variable food sources during winter. Among many likely can-
didates are those known to use short torpor bouts during winter
but for which summer data are not available (e.g., Boyles et al.
2012; Cory Toussaint et al. 2010).
The daily cycle of T
b
’s was slightly out of phase with T
a
during
winter and spring, with T
b
’s still decreasing as T
a
’s were in-
creasing in the morning (figs. 2, 3). The smallest T
b
-T
a
differ-
entials were often several hours after the minimum T
a
was re-
corded on a given day. This pattern was most pronounced on days
when hedgehogs used torpor during winter, because it appeared
that they allowed T
b
to drop until the increasing heat of morn-
Figure 1. Representative body temperatures (T
b
) of desert hedgehogs (Paraechinus aethiopicus) in Saudi Arabia during winter (January 7–
March 15, 2014; a), spring (March 16–May 30, 2014; b), and summer (June 16–August 16, 2013). The temperature tracing depicted for winter
was from a female and chosen to demonstrate both the normal pattern of T
b
(as seen during most of February) and the longest torpor bout
recorded in any individual (during mid-January). Data are T
b
’s, and insets are ambient temperatures for the same periods (X-axes are not
labeled for clarity). Note the different scales on the Y-axes of the insets.
448 J.G.Boyles,N.C.Bennett,O.B.Mohammed,andA.N.Alagaili
This content downloaded from 131.230.059.106 on April 17, 2017 05:37:48 AM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
ing pushed it higher. The cyclical pattern was also seen during
multiday torpor bouts but to a muted degree (e.g., figs. 1, 3); it is
unclear whether T
b
cycles during multiday torpor are driven by
intrinsic or extrinsic factors. Occasionally, T
b
dropped below re-
corded T
a
during torpor bouts. We do not have behavioral ob-
servations of these animals during the periods when we were
recording T
b
, so we cannot distinguish between two possible ex-
planations for this pattern: either the weather station tempera-
tures were slightly different than those at the study site, or hedge-
hogs were using burrows or other structures that buffered T
a
(e.g., dead woody material, which we know they do use). Pre-
vious work on captive desert hedgehogs confirms that they are
nocturnal and inactive during the day (Al-Musfir and Yama-
guchi 2008), so the recorded T
b
pattern is not surprising. From
an energetic standpoint, it would be most efficient to cool into
torpor as quickly as possibleand remain in torpor as long as pos-
sible. Behavioral observations will be useful to determine whether
the quick increases in T
b
in the morning are related to adaptive
behavior (e.g., basking) or reflect minimum available environ-
mental temperatures, even in burrows.
Despite extensive laboratory work on thermoregulation of
desert mammals, data on summer T
b
patterns of small desert
mammals are surprisingly rare. During summer, most variation
in T
b
occurs above normothermy. The diurnal species studied in
the field occasionally reach T
b
’sgreaterthan417C(Chappelland
Bartholomew 1981; Elvert et al. 1999; Alagaili et al. 2017). The
few nocturnal species studied in the field do show regular in-
creases in T
b
above normothermy but reach maximum T
b
’s
several degrees lower than diurnal species (Elvert et al. 1999;
this study). It remains unclear whether these increases in T
b
represent an adaptive water conservation technique or are sim-
ply a biophysical reality for a small animal in a hot environment
(Walsberg 2000).
The torpor patterns we recorded for desert hedgehogs dur-
ing winter are intermediate to those classically described for
hibernators and daily heterotherms (Geiser and Ruf 1995). The
duration of most torpor bouts we recorded for hedgehogs was
similar to daily torpor bouts used by daily heterotherms, but
torpid T
b
’s were regularly lower than those of daily heterotherms,
especially for an animal that weighs 150–600 g (Geiser and Ruf
1995). Furthermore, while most torpor bouts were less than 24 h
long, several individuals underwent bouts of 2, 3, or 4 d, which is
unusual among daily heterotherms. Body temperatures often ap-
proached T
a
, suggesting that metabolic rates must have been low
(Geiser and Mzilikazi 2011). Conversely, while minimum torpid
T
b
’s were similar to those of some hibernators, torpor bouts were
unpredictable, and no individual ever maintained a pattern of
long torpor bouts interrupted by occasional euthermic periods,
as is characteristic of hibernators. The pattern we recorded in
desert hedgehogs is unusual among the hedgehogs studied to
date, which show longer and more predictable torpor bouts
during winter (Fowler and Racey 1990; Hallam and Mzilikazi
2011; Mouhoub-Sayah et al. 2012). This may relate to the more
arid habitat of desert hedgehogs compared with the other species
and the unpredictability of food resources in this habitat.
In the strictest sense, one could argue that the desert hedgehog
is an unusual species that mixes physiological characteristics of
hibernators and daily heterotherms, bringing to three the number
of genera known to use such a pattern of torpor. Alongwith desert
hedgehogs, Patagonian opossums (Lestodelphys halli;Geiserand
Figure 2. Body temperatures of desert hedgehogs (Paraechinus aethiopicus) across the day in winter, spring, and summer. Lines represent
median T
b
’s, and shaded areas are bounded by the tenth and ninetieth percentiles.
Body Temperature of Desert Hedgehogs 449
This content downloaded from 131.230.059.106 on April 17, 2017 05:37:48 AM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
Martin 2013) and several sengis in the genus Myurus (also known
as elephant shrews and locally as klaasneus) meet this strict
criterion (Mzilikazi and Lovegrove 2004; Geiser and Mzilikazi
2011; Boyles et al. 2012). While ancestral hedgehogs appear in
the fossil record shortly after the Cretaceous-Paleogene ex-
tinction event (O’Leary et al. 2013), the radiation of modern
hedgehog genera was sudden and much more recent (Banni-
kova et al. 2014). The ecology of desert hedgehogs suggests they
are derived from more temperate and semiarid species, so the
unusual thermoregulatory pattern might also be derived. If so,
this would be interesting because it has been suggested that this
unusual pattern may be representative of an ancestral state in
sengis and opossums (Geiser and Martin 2013).
A more liberal interpretation of the pattern of torpor we
recorded in desert hedgehogs is that this pattern is not truly
unique and represents another point along a gradient of ther-
moregulatory patterns (Boyles et al. 2013; van Breukelen and
Martin 2015). If so, it strengthens the argument that greater
variation in thermoregulatory patterns exists than traditionally
realized and that desert hedgehogs are simply another exception
to a strict classification scheme that separates daily heterotherms
and hibernators (Canale et al. 2012). It is true that most arguments
for a thermoregulatory continuum are based on measurements of
T
b
, and other characteristics of thermoregulation (e.g., metabolic
rates) need to be detailed more thoroughly in species with T
b
patterns intermediate to daily heterotherms and hibernators.
The thermoregulatory pattern we measured herein adds in-
teresting variation to thermoregulatory patterns seen among
the Erinaceidae (hedgehogs and gymnures) and Eulipotypha
and further solidifies suggestions that these taxa are interesting
for thermoregulatory studies (e.g., Lovegrove 2012b). Even with
the Erinaceidae, the opportunities to test predictions of evolu-
tionary and ecological drivers of thermoregulation abound. For
example, the divergence of gymnures (subfamily Galericinae) ap-
pears quite old, happening in the middle to late Eocene, while the
extant hedgehogs radiated recently (Bannikova et al. 2014). Thus,
within this single family, there is a diverse and contrasting evolu-
tionary history (Bannikova et al. 2014). While conflated with
phylogeny, there is also variation in habitat (forest, grassland,
and desert) and latitude (tropical to high temperate) within this
family. Finally, there is wide variation in thermoregulatory pat-
terns, ranging from apparent homeothermy in lesser gymnures
(Hylomys suillus; Genoud and Ruedi 1996) to deep hibernation in
temperate hedgehogs. Despite the logistical difficulties associated
with studying many species in this taxon, we encourage further
study of thermoregulatory patterns of the Eulipotyphla to inform
Figure 3. Representative winter body temperature (T
b
) of a male desert hedgehog (Paraechinus aethiopicus)overa10-dperiodduringFebru-
ary 4–13, 2014. Ambient temperature (T
a
) comes from a weather station approximately 27 km northwest of the study site (Prince Nayef bin
Abdulaziz Regional Airport). Body temperatures were similar for females, but the T
b
-T
a
differentials were generally smaller during deep torpor
than seen in males.
450 J.G.Boyles,N.C.Bennett,O.B.Mohammed,andA.N.Alagaili
This content downloaded from 131.230.059.106 on April 17, 2017 05:37:48 AM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
our understanding of evolution of thermoregulation in laura-
siatherians, eutherians, and mammals as a whole.
Acknowledgments
This project was financially supported by the Deanship of
Scientific Research at the King Saud University through the
research group (project RGP_VPP_020), the South African
National Research Foundation (grant 64756), and the Uni-
versity of Pretoria.
Literature Cited
Abu Baker M.A., N. Reeve, I. Mohedano, A.A.T. Conkey,
D.W. MacDonald, and N. Yamaguchi. 2016. Caught basking
in the winter sun: preliminary data on winter thermoregu-
lation in the Ethiopian hedgehog, Paraechinus aethiopicus,
in Qatar. J Arid Environ 125:52–55.
Alagaili A.N., N.C. Bennett, O.B. Mohammed, and D.W. Hart.
Forthcoming. The reproductive biology of the Ethiopian hedge-
hog, Paraechinus aethiopicus, from central Saudi Arabia: the
role of rainfall and temperature. J Arid Environ.
AlagailiA.N.,N.C.Bennett,O.B.Mohammed,I.S.Zalmout,
and J.G. Boyles. 2017. Body temperature patterns of a small
endotherm in an extreme desert environment. J Arid En-
viron 137:16–20.
Al-Musfir H.M. and N. Yamaguchi. 2008. Timings of hiber-
nation and breeding of Ethiopian hedgehogs, Paraechnius
aethiopicus, in Qatar. Zool Middle East 45:3–10.
BannikovaA.A.,V.S.Lebedev,A.V.Abromov,andV.V.
Rozhnov. 2014. Contrasting evolutionary history of hedge-
hogs and gymnures (Mammalia: Erinaceomorpha) as in-
ferred from a multigene study. Biol J Linn Soc Lond 112:499–
519.
Bartels W., B.S. Law, and F. Geiser. 1998. Daily torpor and
energetics in a tropical mammal, the northern blossum-bat
Macroglossus minimus (Megachiroptera). J Comp Physiol B
168:233–239.
Bininda-EmondsO.R.P.,M.Cardillo,K.E.Jones,R.D.E.
MacPhee, R.M.D. Beck, R. Grenyer, S.A. Prices, R.A. Vos,
J.L. Gittleman, and A. Purvis. 2007. The delayed rise of
present-day mammals. Nature 446:507–512.
Boyles J.G., B. Smit, and A.E. McKechnie. 2011a. Does use of the
torpor cut-off method to analyze variation in body tem-
perature cause more problems than it solves? J Therm Biol
36:373–375.
———. 2011b. A new comparative metric for estimating
heterothermy in endotherms. Physiol Biochem Zool 84:115–
123.
Boyles J.G., B. Smit, C.L. Sole, and A.E. McKechnie. 2012.
Body temperature patterns in two syntopic elephant shrew
species during winter. Comp Biochem Physiol A 161:89–94.
Boyles J.G., A.B. Thompson, A.E. McKechnie, E. Malan, M.M.
Humphries, and V. Careau. 2013. A global heterothermic
continuum in mammals. Glob Ecol Biogeogr 22:1029–1039.
CampbellK.L.,I.W.McIntyre,andR.A.MacArthur.1999.
Fasting metabolism and thermoregulatory competence of the
star-nosed mole, Condylura cristata (Talpidae: Condyluri-
nae). Comp Biochem Physiol A 123:293–298.
Canale C.I., D.L. Levesque, and B.G.Lovegrove.2012.Tropical
heterothermy: does the exception prove the rule or force a
re-definition? Pp. 29–40inT.Ruf,C.Bieber,W.Arnold,and
E. Millesi, eds. Living in a seasonal world: thermoregula-
tory and metabolic adaptations. Springer, Berlin.
Chappell M.A. and G.A. Bartholomew. 1981. Activity and
thermoregulation of the antelope ground squirrel (Ammos-
permophilus leucurus) in winter and summer. Physiol Zool 54:
215–223.
Corbet G.B. 1988. The family Erinaceidae: a synthesis of its
taxonomy, phylogeny, ecology and zoogeography. Mamm
Rev 18:117–172.
Cory Toussaint D., A.E. McKechnie, and M. van der Merwe.
2010. Heterothermy in free-ranging male Egyptian free-
tailed bats (Tadarida aegyptiaca)inasubtropicalclimate.
Mamm Biol 75:466–470.
Dmi’el R. and M. Schwarz. 1984. Hibernation patterns and
energy expenditure in hedgehogs from semi-arid and tem-
perate habitats. J Comp Physiol B 155:117–123.
Douady C.J., P.I. Chatelier, O. Madsen, W.W. de jong, F.
Catzeflis, M.S. Springer, and M.J. Stanhope. 2002. Molec-
ular phylogenetic evidence confirming the Eulipotyphla con-
cept and in support of hedgehogs as the sister group to shrews.
Mol Phylogenet Evol 25:200–209.
Douady C.J. and E.J.P. Douzery. 2003. Molecular estimation of
eulipotyhlan divergence times and the evolution of “Insec-
tivora.”Mol Phylogenet Evol 28:285–296.
Dzal Y.A. and R.M. Brigham. 2013. The tradeoff between torpor
use and reproduction in little brown bats (Myotis lucifugus).
J Comp Physiol B 183:279–288.
Elvert R., N. Kronfeld, T. Dayan, A. Haim, N. Zisapel, and G.
Heldmaier. 1999. Telemetric field studies of body tempera-
ture and activity rhythms of Acomys russatus and A. cahi-
rinus in the Judean Desert of Isreal. Oecologia 119:484–492.
Fowler P.A. and P.A. Racey. 1990. Daily and seasonal cycles of
body temperature and aspects of heterothermy in the hedgehog
Erinaceus europaeus. J Comp Physiol B 160:299–307.
Geiser F. 1998. Evolution of daily torpor and hibernation in
birds and mammals: importance of body size. Clin Exp Phar-
macol Physiol 25:736–740.
Geiser F. and R.V. Baudinette. 1987. Seasonality of torpor and
thermoregulation in three dasyurid marsupials. J Comp Physiol
B157:335–344.
Geiser F. and G.M. Martin. 2013. Torpor in the Patagonian opos-
sum (Lestodelphys halli): implications for the evolution of daily
torpor and hibernation. Naturwissenschaften 100:975–981.
Geiser F. and N. Mzilikazi. 2011. Does torpor of elephant shrews
differ from that of other heterothermic mammals? J Mammal
92:452–459.
Geiser F. and T. Ruf. 1995. Hibernation versus daily torpor in
mammals and birds: physiological variables and classifi-
cation of torpor patterns. Physiol Zool 68:935–966.
Body Temperature of Desert Hedgehogs 451
This content downloaded from 131.230.059.106 on April 17, 2017 05:37:48 AM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
Genoud M. and M. Ruedi. 1996. Rate of metabolism, tem-
perature regulations, and evaporative water loss in the lesser
gymnure Hylomys suillus (Insectivora, Mammalia). J Zool
(Lond) 240:309–316.
Grant T.R. 1983. Body temperatures of free-ranging platy-
puses, Ornithorhyncus anatinus (Monotremata), with ob-
servations of their use of burrows. Aust J Zool 31:117–122.
Grigg G.C., L.A. Beard, J.A. Barnes, L.I. Perry, G.J. Fry, and M.
Hawkins. 2003. Body temperature in captive long-beaked echid-
nas (Zaglossus bartoni). Comp BiochemPhysiol A 136:911–916.
Hallam S.L. and N. Mzilikazi. 2011. Heterothermy in the southern
African hedgehog, Atelerix frontalis. J Comp Physiol B 181:437–
445.
Hallström B.M. and A. Janke. 2010. Mammalian evolution
may not be strictly bifurcating. Mol Biol Evol 27:2804–2816.
Król E. 1994. Metabolism and thermoregulation in the eastern
hedgehog Erinaceus concolor. J Comp Physiol B 164:503–507.
Levesque D.L. and G.J. Tattersall. 2010. Seasonal torpor and
normothermic energy metabolism in the eastern chipmunk
(Tamias striatus). J Comp Physiol B 180:279–292.
Lovegrove B.G. 2012a. The evolution of endothermy in Ce-
nozoic mammals: a plesiomoprhic-apomorphic continuum.
Biol Rev 87:128–162.
———. 2012b. A single origin of heterothermy in mammals.
Pp. 3–11inT.Ruf,C.Bieber,W.Arnold,andE.Millesi,eds.
Living in a seasonal world: thermoregulatory and metabolic
adaptations. Springer, Berlin.
Lovegrove B.G. and F. Genin. 2008. Torpor and hibernation in a
basal placental mammal, the lesser hedgehog tenrec Echinops
telfairi. J Comp Physiol B 178:691–698.
Lovegrove B.G., J. Raman, and M.R. Perrin. 2001. Heterothermy in
elephant shrews, Elephantulus spp. (Macroscelidea): daily tor-
por or hibernation? J Comp Physiol B 171:1–10.
McKechnie A.E. and N. Mzilikazi. 2011. Heterothermy in
Afrotropical mammals and birds: a review. Integr Comp
Biol 51:349–363.
MouchatyS.K.,A.Gullberg,A.Janke,andU.Arnason.2000.
The phylogenetic position of the Talpidae within Eutheria
based on analysis of complete mitochondrial sequences. Mol
Biol Evol 17:60–67.
Mouhoub-Sayah C., J.-P. Robin, A. Malan, P. Pévet, and M.
Saboureau. 2012. Patterns of body temperature change in the
Algerian hedgehog (Atelerix algirus) during autumn and winter.
Pp. 307–316 in B.G. Lovegrove and A.E. McKechnie, eds.
Hypometabolism in animals: hibernation, torpor and cryo-
biology. Interpak, Pietermaritzburg.
Mustonen A.-M., J. Asikainen, K. Kauhala, T. Paakkonen, and
P. Nieminen. 2007. Seasonal rhythms of body temperature in
the free-ranging raccoon dog (Nyctereutes procyonoides) with
special emphasis on winter sleep. ChronobiolInt 24:1095–1107.
Mzilikazi N. and B.G. Lovegrove. 2004. Daily torpor in free-
ranging rock elephant shrews, Elephantulus myurus:ayear-
long study. Physiol Biochem Zool 77:285–296.
Nicol S. and N.A. Anderson. 2006. Body temperature as an
indicator of egg-laying in the echidna, Tachyglossus aculeatus.
J Therm Biol 31:483–490.
O’Leary M.A., J.I. Bloch, J.J. Flynn, T.J. Gaudin, A. Giallom-
bardo, N.P. Giannini, S.L. Golberg, et al. 2013. The placental
mammal ancestor and the post–K-Pg radiation of placentals.
Science 339:662–667.
Ruf T., S. Steinlechner, and G. Heldmaier. 1989. Rhythmicity
of body temperature and torpor in the Djungarian hamster,
Phodopus sungorus. Pp. 53–62 in A. Malan and B. Canguilhem,
eds. Living in the cold: 2nd international symposium. Libbey,
London.
Shkolnik A. and K. Schmidt-Nielsen. 1976. Temperature reg-
ulation in hedgehogs from temperate and desert environ-
ments. Physiol Zool 49:56–64.
Soivio A., H. Tähti, and R. Kristoffersson. 1968. Studies on the
periodicity of hibernation in the hedgehog (Erinaceus euro-
paeus L.). III. Hibernation in a constant ambient temperature
of 257C. Ann Zool Fennici 5:224–226.
van Breukelen F. and S.L. Martin. 2015. The hibernation con-
tinuum: physiological and molecular aspects of metabolic
plasticity in mammals. Physiology 30:273–281.
Walsberg G.E. 2000. Small mammals in hot deserts: some
generalizations revisited. BioScience 50:109–120.
WebbP.I.andJ.Ellison.1998.Normothermy,torpor,and
arousal in hedgehogs (Erinaceus europaeus)fromDunedin.
N Z J Zool 25:85–90.
Whiteman J.P., H.J. Harlow, G.M. Durner, R. Anderson-
Sprecher, S.E. Albeke, E.V. Regehr, S.C. Amstrup, and M. Ben-
David. 2015. Summer declines in activity and body temper-
ature offer polar bears limited energy savings. Science 349:
295–298.
Whittow G.C., E. Gould, and D. Rand. 1977. Body temper-
ature, oxygen consumption, and evaporative water loss in a
primitive insectivore, the moon rat, Echinosorex gymnurus.
J Mammal 58:233–235.
Yamaguchi N., A. Al-Hajri, and H. Al-Jabiri. 2013. Timing of
breeding in free-ranging Ethiopian hedgehogs, Paraechinus
aethiopicus,fromQatar.JAridEnviron99:1–4.
Zervanos S.M. and C.M. Salsbury. 2003. Seasonal body tem-
perature fluctuations and energetic strategies in free-ranging
eastern woodchucks (Marmota monax). J Mammal 84:299–
310.
452 J.G.Boyles,N.C.Bennett,O.B.Mohammed,andA.N.Alagaili
This content downloaded from 131.230.059.106 on April 17, 2017 05:37:48 AM
All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).