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Integrative and Comparative Biology, volume 51, number 5, pp. 676–690
doi:10.1093/icb/icr053
SYMPOSIUM
Adaptive Thermoregulation in Endotherms May Alter Responses
to Climate Change
Justin G. Boyles,1,* Frank Seebacher,† Ben Smit* and Andrew E. McKechnie*
*DST/NRF Centre of Excellence at the Percy FitzPatrick Institute, Department of Zoology and Entomology, University of
Pretoria 0002, South Africa; †School of Biological Sciences, University of Sydney, New South Wales 2006, Australia
From the symposium ‘‘A Synthetic Approach to the Response of Organisms to Climate Change: The Role of Thermal
Adaptation’’ presented at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2011,
at Salt Lake City, Utah.
1
E-mail: [email protected]
Synopsis Climate change is one of the major issues facing natural populations and thus a focus of recent research has
been to predict the responses of organisms to these changes. Models are becoming more complex and now commonly
include physiological traits of the organisms of interest. However, endothermic species have received less attention than
have ectotherms in these mechanistic models. Further, it is not clear whether responses of endotherms to climate change
are modified by variation in thermoregulatory characteristics associated with phenotypic plasticity and/or adaptation to
past selective pressures. Here, we review the empirical data on thermal adaptation and acclimatization in endotherms and
discuss how those factors may be important in models of responses to climate change. We begin with a discussion of why
thermoregulation and thermal sensitivity at high body temperatures should be co-adapted. Importantly, we show that
there is, in fact, considerable variation in the ability of endotherms to tolerate high body temperatures and/or high
environmental temperatures, but a better understanding of this variation will likely be critical for predicting responses to
future climatic scenarios. Next, we discuss why variation in thermoregulatory characteristics should be considered when
modeling the effects of climate change on heterothermic endotherms. Finally, we review some biophysical and biochemical factors that will limit adaptation and acclimation in endotherms. We consider both long-term, directional climate
change and short-term (but increasingly common) anomalies in climate such as extreme heat waves and we suggest areas
of important future research relating to both our basic understanding of endothermic thermoregulation and the responses
of endotherms to climate change.
Introduction
Anthropogenic climate change is one of the greatest
conservation issues facing biologists, land stewards,
and governments and has become a central topic
in biological research. Considerable effort is being
invested in determining the best methods to measure
the current impacts of climate change and model the
future effects (Chown et al. 2010). One of the most
obvious results of climate change is that environmental temperatures are changing at a rate much
faster than seen during natural climatic fluctuations
(IPCC 2007). Rapidly changing environmental temperatures will alter the selective pressures acting on
all animals because temperature is one of the most
important factors affecting energy and water balance;
thus, climate change has the potential for severely
affecting the fitness of many species. Despite the crucial role of energy balance in determining fitness and
the feasible impacts of climate change on energy balance, ecological physiology (the field of study most
directly concerned with environmental effects on
energy expenditure) has been underutilized until recently (Helmuth et al. 2005; Chown et al. 2010).
Endothermic species (at least classically defined
homeotherms) are often thought to maintain relatively high body temperatures (Tb) within a narrow
range by means of heat produced from metabolic
processes. Endothermic metabolic rates are several
times higher than those of ectotherms, and metabolic
heat production is regulated in response to
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677
Adaptive thermoregulation in endotherms
environmental temperature fluctuations (adaptive
thermogenesis; Lowell and Spiegelman 2000). This
specialized form of thermoregulation means that
controlling Tb constitutes a large portion of the
energy expended by endotherms when environmental
temperatures (Ta) deviate from the thermoneutral
zone (TNZ) (McNab 2002). Thus, climate change
and the associated warming trend found in many
areas may strongly affect endotherms (especially terrestrial mammals and birds) and it may have a fundamentally different impact on endotherms than on
ectotherms. Thermoregulatory flexibility may afford
multiple pathways for ectotherms to cope with a
changing climate. Some endotherms, on the other
hand, may be so thermally specialized that their
only option is to increase energy expenditure to
maintain a constant Tb as Tas increasingly deviate
from the animal’s TNZ, thereby lessening energy
available for other fundamental functions such as
growth and reproduction. This oversimplified view
of endothermic thermoregulation echos an historically prominent view (Scholander et al. 1950), but
it is gradually being replaced as additional research
suggests adaptive variation in Tb is common among
endotherms.
In a recent paper, Angilletta et al. (2010) defined
adaptive thermoregulation as any thermoregulatory
pattern that is launched to counteract an environmental stressor, whether that pattern arises from genetic changes across generations (i.e., adaptation) or
phenotypically plastic responses within a lifetime
(i.e., acclimatization). Predictions about adaptive
thermoregulation in endotherms can be made by expanding the framework commonly used in the literature on ectotherms (Huey and Slatkin 1976;
Angilletta et al. 2006). They argued that performance
in endotherms is related to Tb in a manner similar to
performance in ectotherms and can therefore be described using thermal performance curves. A performance curve describes the nonlinear relationship
between some physiological trait, in this case Tb,
and a measure of performance. A performance
curve can be described by the maximal level of performance, the optimal Tb for performance, the performance breadth, and the minimum and maximum
critical Tbs (Fig. 1). The relative characteristics of a
species’ performance curve will describe how a species reacts to changes in Tb and thus provides a convenient framework in which to make predictions
about when and why an endotherm should allow
its Tb to vary. Their stated goal was to provide a
general conceptual framework of thermoregulatory
patterns in endotherms. Here, we attempt to apply
Fig. 1 Performance curves are commonly used in the literature
on ectotherms to describe the relationship between body
temperature and performance, but they should also apply to
endotherms. This hypothetical curve shows the commonly
used descriptors of a performance curve: the thermal optimum
(Topt), performance breadth (Pbreadth), critical thermal limits
(CTmin and CTmax), and maximal performance (Pmax).
these ideas to the problem of predicting the effects of
climate change on endotherms.
Our goals in this article are 3-fold. First, we briefly
review the themes found in current literature predicting the responses of endotherms to climate
change, focusing on studies that have a physiological
component. Second, we review the available literature on the responses of endotherms to high Tbs.
Finally, we discuss how the effects of climate
change on endotherms will vary with varying thermal
physiologies, using the concepts of thermoregulation
and thermal sensitivity, as well as co-adaptation between them.
Previous research on responses of
endotherms to climate change
As interest in the effects of climate change has increased over the past two decades, the number of
studies on responses of mammals and birds to a
generally warming climate has grown steadily. As
with other organisms, most studies have employed
a correlative approach, which focuses on changes in
the environment and not on specific characteristics
of the organisms of interest (Kearney and Porter
2009; Buckley et al. 2010). These models assume
that a species’ multidimensional niche space is
fixed and that the subset of climatic conditions an
organism currently occupies is an accurate predictor
of its range under future climates, i.e., an organism
will shift its range to find suitable habitat as climate
changes. For example, many studies have used
678
climate-envelope models to predict shifts of range in
endotherms (e.g., Thomas and Lennon 1999; Both
and Visser 2001; Parmesan 2006; Coetzee et al.
2009). Generally speaking, these studies have reported latitudinal shifts (generally poleward shifts),
altitudinal shifts, or range contractions, in response
to climate change. Other papers have reported phenological shifts (especially migrants arriving earlier)
in endothermic species (e.g., Inouye et al. 2000).
Of more interest herein are papers that have focused on physiological processes underlying responses to climate change by endotherms, which
are rare compared to papers taking this approach
with ectotherms (Helmuth et al. 2005). Such mechanistic approaches can be directly contrasted to the
simple correlative models described above because
they include biophysical, physiological, behavioral,
or ecological characteristics of the organism of interest in addition to information about the environment. Mechanistic models have many advantages
over simple correlative methods, but are more complex and thus more difficult to parameterize
(Helmuth et al. 2005; Buckley 2008; Helmuth 2009;
Buckley et al. 2010; Fuller et al. 2010; Kearney et al.
2010). While they are still relatively rare compared to
correlative approaches, there has been a recent increase in the number of papers using mechanistic
approaches to predict the effects of climate change
on endotherms by examining physiological characteristics of the organism and some interaction between these characteristics and environmental
characteristics (e.g., Humphries et al. 2002;
Humphries et al. 2004; Monahan 2009; Kearney
et al. 2010; McKechnie and Wolf 2010; Molnár
et al. 2010; Porter et al. 2010).
To date, authors of such mechanistic models have
viewed physiological traits as fixed within an individual and species, and the possibility of adaptive physiological responses as climates change have rarely
been considered (Atkins and Travis 2010; Chevin
et al. 2010; Chown et al. 2010). While these static
models may offer more information than do correlative approaches, the next progression in these
models will be to include genetic adaptation within
populations, intraspecific and interspecific variation
in physiological traits, and the possibility of
within-individual acclimatization to a changing climate. A number of studies have shown some level of
genetic adaptation in response to recent climate
change (Bradshaw and Holzapfel 2006; Bradshaw
and Holzapfel 2008; Husby et al. 2011), but data
are still relatively limited, especially with respect to
how fast physiological traits can respond to changing
environments. Endotherms show considerable
J. G. Boyles et al.
variation in traits related to physiological maintenance, such as energetic requirements (metabolic
rate), thermoregulation, and thermal tolerance, and
we argue that the potential for traits being flexible in
response to changing environments (including both
genetic changes in populations as well as
within-individual plasticity of traits), needs to form
an intricate part of predicting species’ responses.
The co-adaptation of thermoregulation
and thermal sensitivity in endotherms
The idea that performance of all systems from biochemical to organismal should be affected by temperature is not new. One possible advantage of
endothermy, and more specifically homeothermy, is
that maintaining a narrow range of Tbs allows biochemical systems to perform maximally at normal Tb
(Heinrich 1977; Hochachka and Somero 2002).
However, maintaining a high and constant Tb is energetically expensive and thus we should expect some
variation in Tb, either temporally or regionally within
the body, for all endotherms (Arnold et al. 2004;
Angilletta et al. 2010). If variation occurs in all endotherms, we should further expect thermoregulation and thermal sensitivity (i.e., the magnitude of
change in a measured performance across a range of
Tbs) of an organism to be co-adapted in a way that
maximizes fitness. In other words, the optimal temperature for performance should coincide with the
most commonly displayed active Tb, and thermal
specialists (i.e., species strongly affected by changes
in Tb) should maintain a relatively narrow range of
Tbs while thermal generalists (i.e., species weakly affected by changes in Tb) should display larger fluctuations in Tb (Levins 1968; Huey and Hertz 1984;
Angilletta et al. 2006; Angilletta et al. 2010). Thus, a
specialist–generalist trade-off may exist with specialists performing at a high level at a specific Tb, while
generalists perform at some lower level, but across a
wider range of Tbs. Differing environmental pressures will change the relative benefit of being a specialist as opposed to being a generalist
thermoregulator. As a point of clarification, we do
not view thermal specialists and thermal generalists
as a true dichotomy of thermoregulatory patterns.
Instead, we view the thermoregulatory landscape as
a continuum and use the terms ‘‘specialist’’ and
‘‘generalist’’ only in relative terms. While it may be
argued that these terms are interchangeable with
‘‘homeotherm’’ and ‘‘heterotherm’’, we only use
those terms when specifically discussing past research
based on those definitions because of the inherent
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Adaptive thermoregulation in endotherms
baggage they have accumulated over many years of
research.
Biochemical rates have a thermal optimum at
which the activities of enzymes are maximized
(Daniel et al. 2010), and it may be that thermal
optima of enzymes and, hence, performance are
matched to the modal Tb in homeothermic species
(Morrison et al. 2008). Humans are a good example
of a species in which Tb is tightly regulated, and in
which performance in muscle, neurobehavioural, and
cognitive functions co-vary with Tb to be maximal at
the active Tb (Kleitman et al. 1938; Kleitman and
Jackson 1950; Wright et al. 2002; Dodd et al. 2006;
Racinais and Oksa 2010). Data from humans have
likely contributed to the rise of the paradigm that
performance is optimized at the Tb most commonly
experienced by organisms. Surprisingly, however, this
paradigm remains largely untested in other endotherms, and data on the relationship between thermal performance breadth and thermoregulatory
patterns are sparse. Tissue-level examinations have
revealed that interspecific variation occurs in the
thermal breadth of muscle performance (e.g.,
Bennett 1984; Choi et al. 1998), and while it appears
qualitatively that the thermal breadth of muscle performance increases as the level of heterothermy expressed by a species increases, explicit tests are still
needed to verify this conclusion (Angilletta et al.
2010). Other functions, such as immune responses,
are also likely to vary with thermoregulatory patterns
and we would expect species with large variation in
Tb (e.g., hibernators) to be able to mount at least
some immune response across a wider range of Tbs
than could a species exhibiting small variations in
Tbs (e.g., daily heterotherms). There is evidence
that hibernators greatly reduce, but probably do
not completely abandon, immune function during
hibernation (Bouma et al. 2010); however, comparative data across species displaying a range of thermoregulatory patterns are lacking.
The effect of Tb on whole-organism performance
has received relatively little attention in endotherms,
although it might be possible to draw some conclusions by examining muscle-level performance. For
example, in humans, a decrease in Tb strongly affects
performance; for example, a 18C decrease in muscle
temperature corresponds to a 2–5% decrease in performance (Racinais and Oksa 2010). In contrast,
Wooden and Walsberg (2004) showed that Tb did
not affect running speed or force production in
highly heterothermic round-tailed ground squirrels
(Spermophilus tereticaudus) across a wide range of
tested Tbs (30–428C). Future work in this area is
obviously important, but will likely require
pharmacological manipulations, especially in homeotherms, to test performance across a wider range of
Tbs.
With the exception of these few studies, which
support the idea of co-adaptation of thermoregulation and thermal sensitivity in endotherms, no explicit work has been carried out on the subject,
despite the important role this relationship might
play in modeling the effects of climate change on
endotherms. While we can provide no new evidence
that thermoregulation and thermal sensitivity are
co-adapted in endotherms, we do attempt to provide
some of the groundwork for such experiments.
Specifically, we hope to fill a gap left by Angilletta
et al. (2010) on the possibility of an individual or
species adaptively altering thermal sensitivity in response to thermal stress. If physiological responses to
high temperatures and heat stress are adaptive in
endotherms, there should be some variation in physiological responses among individuals, populations,
and species to Ta above the TNZ (although variation
may also occur for nonadaptive reasons). In other
words, variation in thermoregulatory responses is
necessary (but not sufficient) evidence of adaptive
alterations in thermal sensitivity in endotherms
under thermal stress. Here, we focus on the limited
evidence for variation in response to high temperatures because they will be more applicable to climate
change, although a similar exercise would also be
useful in reference to low temperatures.
Evidence of variation in thermal
sensitivity at high temperatures
Tolerance of high body temperatures
Endotherms must respond to temperatures above the
TNZ by either increasing Tb or thermoregulatory
effort to maintain a constant Tb within the preferred
range. It is unclear whether endotherms will be able
to shift their ranges fast enough to avoid such Tas,
especially given that relatively small changes may be
highly detrimental to some species (Tewksbury et al.
2008). Thus, it is important to consider responses to
high Tas. Facultative increases in Tb in response to
high Ta are relatively widespread among birds
(Tieleman and Williams 1999), with reported
values for Tb during facultative hyperthermia varying
between 41.18C and 45.88C among species (Tieleman
and Williams 1999). However, far less is known
about upper lethal limits or how physiological performance decreases with increasing Tb. Dawson
(1954) found that towhees (Piplio spp.) lost the capacity for coordinated movement at Tb4458C and
died at Tb478C. Lethal Tb values for four breeds of
680
chicken were in the range of 45.9–46.28C (Arad and
Marder 1982), although higher values ranging from
46.0 to 47.88C have also been reported (Randall
1943). California Quail (Lophortyx californicus) tolerated Tb ¼ 468C for short periods (Brush 1965), and
Common Starlings (Sturnus vulgaris) exhibited
Tb ¼ 45.88C at Ta ¼ 458C (Dmi’el and Tel-Tzur
1985). Lethal Tbs for mammals appear generally
lower than those for birds: 43.48C, 42.58C, and
41.78C for rabbits, rats, and dogs, respectively
(Adolph 1947), 41.98C in a single long-nosed bat
(Leptonycteris yerbabuenae) (Carpenter and Graham
1967), and 43.58C in Antrozous pallidus, Tadarida
brasiliensis, and Myotis yumanensis (Licht and
Leitner 1967).
Tolerance of high environmental temperature
There also appears to be considerable interspecific
variation in the extent to which endotherms can tolerate high environmental temperatures. In birds, for
instance, fatal hyperthermia in towhees exposed to Ta
of 39–438C (Dawson 1954), and Zebra Finches exposed to Ta of 45–468C (Cade et al. 1965) contrasts
with the maintenance of Tb542.58C in Houbara
Bustards exposed to Tas of 50–558C (Tieleman
et al. 2002), and Tbs of 41–428C at Ta ¼ 608C in
heat-acclimated Rock Doves (Marder and Arieli
1988). Henderson (1971) noted that Gambel’s
Quail (Lophortyx gambelli) survived short-term exposure to Ta ¼ 458C better (two of three birds) than
did Scaled Quail (Callipepla squamata) (one of five
birds). Likewise, behavioral responses to hot weather
can show striking variation among species. Birds
breeding in the Salton Sea during summer experience
extremely high Ta and a lack of shaded microsites
(Grant 1982). At this site, charadriiform adults
shared incubation duties, relieving each other more
frequently during the hottest part of the day, thereby
allowing for more frequent visits to water for drinking and belly-soaking (Grant 1982). In Black-necked
Stilts, for instance, the average length of an incubation bout decreased from 57 min at Tas of 15–208C
to just 13 min at Tas of 40–448C (Grant 1982). In
stark contrast, female Lesser Nighthawks incubated
throughout the day without leaving the nest to
drink or belly-soak, even during extremely hot
weather (Grant 1982), suggesting a high tolerance
for dehydration and/or a pronounced capacity for
facultative hyperthermia.
The capacity of caprimulgids to tolerate extremely
high environmental temperatures has been noted by
several authors (Bartholomew et al. 1962; Dawson
and Fisher 1969; Grant 1982). Since this group of
J. G. Boyles et al.
birds is also one of the most heterothermic avian
taxa (Brigham et al. 2000; McKechnie et al. 2007),
we asked whether the caprimulgids’ capacity for heat
tolerance reflects a generalist Tb phenotype, with
caprimulgids exhibiting labile Tb both above and
below the normothermic range. Somewhat surprisingly, the limited data available suggest the opposite,
with caprimulgids tending to defend Tb within a
narrower range of values in very hot environments
than do many other species. Spotted Nightjars
(Eurostopodus argus), for instance, defended
Tb5438C even at Ta4508C (Dawson and Fisher
1969). This leads to several important questions
about the characteristics of thermal performance
curves that should be addressed for endotherms.
First, is the entire performance curve of a generalist
species shifted toward colder Tbs compared with
thermal specialists, such that the lower critical
limit, upper critical limit, and thermal optimum
are all lower than those of specialists (Fig. 2A)?
Conversely, are thermal generalists able to maintain
a wider overall range of Tbs, such that the lower
critical limit is lower, and the upper critical limit
higher, than in specialists (Fig. 2B)? No explicit
tests have been conducted on this topic, but published literature may give some clues. In a comparison of responses to heat stress by four
similarly-sized species of bird, Lasiewski and
Seymour (1972) found that the Common Poorwill
(Phalaenoptilus nuttalli), a highly heterothermic species, exhibited much smaller increases in Tb at
Ta4408C than did three other more homeothermic
species, namely Village Weavers (Ploceus cucullatus),
Chinese painted quails (Excalfactoria chinensis), and
Inca doves, (Scardafella inca), apparently as a result
of a higher ratio of evaporative heat loss to metabolic
heat production. The observations that a highly heterothermic group of birds (i.e., caprimulgids) appears to maintain lower Tb during heat stress than
do many less heterothermic groups suggests that
upper critical limits of thermal generalists might be
lower than those of specialists (Fig. 2A).
Among mammals that inhabit hot sub-tropical deserts, large species that cannot avoid high Tas by
seeking shelter in microsites such as burrows may
regularly endure Ta values well above their Tb. In
these species, thermoregulatory responses to very
hot weather primarily involve increases in the amplitudes of circadian Tb cycles, rather than increases in
mean Tb (Taylor 1969; Ostrowski et al. 2003;
Ostrowski and Williams 2006; Hetem et al. 2010).
Air temperatures 408C were associated with circadian Tb cycles of 68C in captive Beisa oryx (Oryx
gazelle beisa) (Taylor 1969), 7.78C in free-ranging
Adaptive thermoregulation in endotherms
681
Fig. 2 A trade-off may exist such that a thermal specialist can perform at a high level, but across a narrow range of body temperatures
while a thermal generalist can perform across a wide range of body temperatures, but at a low level at all temperatures. Research is
needed to determine the relative characteristics of the performance curves describing generalist and specialist endotherms. This figure
represents two examples of how the relative characteristics may vary.
Arabian oryx (Oryx leucoryx) (Hetem et al. 2010),
and 2.38C in Arabian sand gazelles (Gazella subgutturosa marica) (Ostrowski and Williams 2006).
However, we are not aware of data showing interspecific or intraspecific variation in tolerance of high
environmental temperature in large mammals.
It appears that considerable variation exists in the
thermal responses of endotherms above the TNZ.
Again, this is necessary, but not sufficient, to argue
that the responses are adaptive. Unfortunately, evidence is still too scarce to determine whether this
variation occurs in predictable ways, as would be
expected given the past selective pressures on a population or species, or if the variation is driven by
phylogenetically-related differences in the cellular
functioning among species, for example, in the composition of membranes and the expression of heat
shock proteins (Hazel 1995; Feder and Hofmann
1999). When considering the possibility that responses are adaptive, it is important to consider
both large-scale climatic effects and local ecological
effects. For example, large mammals such as ungulates
in desert environments might a priori be expected to
exhibit more pronounced thermoregulatory responses
to high temperatures simply because they have little
choice but tolerate them, whereas small mammals can
avoid them by using cool microclimates.
What patterns of thermoregulation
and thermal sensitivity should we
expect among endotherms?
The concept of co-adaption between thermoregulation and thermal sensitivity has been well studied in
ectotherms (Angilletta 2009; Kingsolver 2009) and
to a lesser extent in homeothermic endotherms
(especially humans) (Benzinger 1961; Wright 2002).
However, few attempts have been made to generalize
the concept to encompass all endothermic species
across the entire gradient of thermoregulatory patterns (Angilletta et al. 2010). In very general terms,
homeothermic individuals, populations, or species
should have narrower thermal performance curves
than do heterothermic individuals, populations, or
species. Thus, a hibernator should be able to maintain some level of performance (even if it is very
low) over a wider range of Tbs than should a
highly homeothermic species. Likewise, if expression
of the trait is highly plastic, the performance breadth
should widen during the season in which the animal
displays the widest range of Tbs, which can vary even
within a species (Hetem et al. 2009).
An interesting comparison of the relationships between thermal sensitivity and thermoregulation may
also come from examining species with varying
migratory patterns. Highly migratory or nomadic
species should largely avoid harsh environmental
conditions and periods of low availability of
energy; thus, we expect these species to display performance curves with narrow breadths. Conversely,
nonmigrants must cope with a wider range of Tas
and availabilities of energy, and should therefore be
less sensitive to changes in Tb. If thermoregulation
and thermal sensitivity are co-adapted, we would
therefore expect migrants to be relatively less heterothermic compared to closely related nonmigratory
species. Note that the presence of heterothermic migrants (e.g., hummingbirds and some bats) does not
negate this prediction. If fact, it will be of interest to
determine whether the most migratory species in
these groups are also the most thermally specialized.
682
Can characteristics of thermal
performance be used to predict
relative responses to climate
change?
Thermoregulation, thermal sensitivity, and the
co-adaptation of the two will play an important
role in how populations or species of endotherms
will respond to a changing climate. For example,
others have speculated that plasticity of physiological
responses used by heterothermic endotherms might
put them at a competitive advantage over homeothermic endotherms in a changing environment
(Canale and Henry 2010). Bioenergetic models suggest that seasonally heterothermic mammals may increase in abundance relative to homeothermic species
as rising temperatures allow hibernators to shift into
some high latitude areas (Humphries et al. 2004) and
phylogenetically-independent analyses suggest that
heterothermic thermoregulation might lead to decreased risk of extinction (Liow et al. 2009). Such
discussions about how variation in thermoregulatory
characteristics will affect a species’ response to climate change are important and lead us to ask several
deceptively simple questions: Will sympatric endotherms with different thermal characteristics display
different responses to a warming climate? What roles
will future adaptation and phenotypic plasticity play
in responses by endotherms and what are the limits
of these factors in mediating responses to climate
change? What effects can we expect short-term, but
increasingly common, anomalies in weather to have
on endotherms?
Here, we ask what effect differences in thermal
characteristics of species will have on the species’
responses to climate change. For simplicity, let us
first assume that thermal performance curves do
not vary intraspecifically and that endotherms have
no capacity to adapt or acclimatize to climate
changes in the future (i.e., thermal performance
curves are fixed, at least relative to the speed of environmental change) and that two species in the
same environment experience climate change in the
same way. These are likely unrealistic assumptions
(Jiguet et al. 2010; Sears and Angilletta 2011), but
these simplifications provide a convenient starting
point for the discussion. Several factors may affect
these responses, including the relative characteristics
of the thermal performance curves of the species in
question. For example, assume that a single value of
Tb represents the thermal optimum of both a thermal specialist and a thermal generalist, but they
differ in thermal breadth. The principles of Jensen’s
Inequality (Ruel and Ayres 1999; Martin and Huey
J. G. Boyles et al.
2008; Boyles and McKechnie 2010) predict that the
skewed relationship between Tb and thermal performance may lead to a larger relative decrease in performance in a thermal specialist than in a thermal
generalist as Tb exceeds the optimum. In this scenario, the specialist may have to increase the time and/
or energy spent on thermoregulation substantially,
whereas the generalist may have to spend less time
and/or energy on thermoregulation, thereby gaining
a relative advantage over the specialist. Thus, either
long-term directional increases in Ta or short-term
weather events that drive Ta above the TNZ should
favor generalist thermoregulators over their more
specialized competitors.
The response will also vary according to the seasonal timing of increases in temperature associated
with climate change. If it is during summer in a
warm area where Tas are likely to be within or
above the TNZ, warmer environmental temperatures
will necessarily cause either an increase in Tb or an
increase in the energy or time (or both) devoted to
thermoregulation to maintain Tb near optimal levels.
Therefore, the relative responses should be similar to
those described above. Conversely, if the increases in
temperature occur during winter or in temperate
regions (IPCC 2007) when Tas are below the TNZ,
a thermal specialist could gain an advantage relative
to a thermal generalist because the time and energy required to maintain Tb within a narrow
range will decrease, which is likely to be more beneficial to homeothermic species than to heterothermic species.
These predictions can be extended to shifts in
range as well. For example, in a hot desert environment, an increasing maximum Ta may exert
stronger selective pressure on a thermal specialist
than on a generalist, making a shift in range
more likely for the specialist. In environments in
which endotherms experience both Ta4Tb and
scarce, unpredictable water resources, the physiological conflict between evaporative cooling and
conservation of water will exacerbate selective pressure on thermal specialists that maintain Tb within
a very narrow range. Conversely, a warming winter
in a cold temperate climate may impose a cost on
a generalist (e.g., if it warms enough to make
torpor less efficient energetically but not warm
enough to allow heterotherms to completely
avoid it) while lessening the pressure on specialists
(e.g., by lessening the cost of maintaining a high
Tb). In this scenario, the generalist species is likely
to gain more benefit from a poleward shift in
range range than is the specialist.
683
Adaptive thermoregulation in endotherms
The role of phenotypic plasticity
Acclimation and acclimatization
Mammals and birds exhibit considerable phenotypic
plasticity in physiological parameters related to thermoregulation. Most of the available data focus on
phenotypic flexibility (i.e., short-term, reversible phenotypic adjustments), rather than on developmental
plasticity (i.e., nonreversible developmental adjustments) (Piersma and Drent 2003). Phenotypic flexibility has been most commonly investigated in the
context of acclimation or acclimatization to cold;
many mammals and birds respond to cold environments by increasing the capacity for heat production
(Klingenspor et al. 1996; McKechnie 2008; Glanville
and Seebacher 2010b), although in mammals the direction of seasonal body mass and metabolic adjustments is strongly related to body mass (Lovegrove
2005). However, phenotypic flexibility manifested
through acclimatization can also potentially influence
endotherms’ capacity to tolerate high environmental
temperatures in several ways. First, endotherms may
be able to increase mean normothermic Tb in response to hot environments. Such a response
would be particularly advantageous if the thermoregulatory system were ineffective in maintaining Tb
within a normothermic range. There is some evidence that Tbs change in response to acclimation
temperatures (Shido et al. 1989; Shido et al. 1991;
Buono et al. 1998; Glanville and Seebacher 2010a),
but the overall picture that emerges is that acclimation to heat does not lead to increases in mean Tb,
and in fact often leads to the opposite. Human subjects acclimated to exercising in a hot, humid environment (Ta ¼ 358C, 75% relative humidity)
exhibited a small but significant decrease in Tb
during rest, which was correlated with lower Tb at
the end of exercise sessions (Buono et al. 1998).
Lower Tb may be advantageous by improving at
least aerobic exercise performance (Ranalli et al.
2010). In birds, the available evidence also suggests
that phenotypic adjustments to heat do not involve
increases in Tb. Heat-acclimated chickens maintained
lower Tb than did control birds (Hillerman and
Wilson 1955), and heat-acclimated White-winged
Doves maintained lower Tb at Ta ¼ 458C than did
individuals acclimated to room temperature
(McKechnie and Wolf 2004). These data suggest an
endothermic thermoregulatory system is generally
effective in maintaining normothermia at high
temperatures.
An endotherm’s hydration state should also be
important in the expression of facultative hyperthermia (Angilletta et al. 2010), although data on the role
of water in thermoregulation are rare (especially in
free-living endotherms). Hydrated endotherms
should be able to maintain Tb within a narrow
range, but if water is scare it may become more
beneficial to allow Tb to increase at higher temperature, thereby reducing the risk of dehydration. Thus,
a second way in which heat acclimation or acclimatization may affect endotherms are alterations to
heat-loss avenues which, in at least some birds, concerns the partitioning of evaporative heat loss into
respiratory and cutaneous components. Columbiform birds (doves and pigeons), in particular,
appear to be able to significantly vary the relative
contributions of respiratory and cutaneous avenues
of evaporative heat loss (Hoffman and Walsberg
1999; McKechnie and Wolf 2004). In desert
White-winged Doves (Zenaida asiatica mearnsii),
heat-acclimated individuals exhibited significantly
higher rates of cutaneous evaporative water loss
(CEWL) than did individuals acclimated to room
temperature, with these responses reflecting reduced
cutaneous resistance to diffusion of water vapor in
heat-acclimated birds (McKechnie and Wolf 2004).
The benefit of higher CEWL in these doves appeared
to relate to the energetic cost of increasing respiratory evaporative water loss (REWL) through mechanisms such as panting and gular flutter; at Ta ¼ 458C
the metabolic rate of heat-acclimated doves was 35%
lower than that of cool-acclimated birds (McKechnie
and Wolf 2004). Avian adjustments in CEWL are
driven by changes in the skin’s structure and lipid
composition (Menon et al. 1988, 1989,1996; Peltonen
et al. 1998; Haugen et al. 2003) and by adjustments
in blood flow that result in elevated hydrostatic
pressures in the skin’s microvasculature (Ophir
et al. 2002).
Facultative hyperthermia
As noted above, some birds and mammals respond
to very high Tas by means of facultative, reversible
periods of hyperthermia during which Tb increases
above normothermic values, and which serve to reduce evaporative water loss by reducing the Ta—Tb
gradients that need to be maintained by evaporative
heat loss. In mammals, these responses may involve
increased amplitudes of circadian Tb, with increases
in diurnal Tb as well as decreases in nocturnal Tb
(Taylor 1969; Ostrowski and Williams 2006; Hetem
et al. 2010).
In the most thorough recent review of this avian
facultative hyperthermia, Tieleman and Williams
(1999) critically evaluated laboratory studies in
which avian EWL was measured at Ta 458C, and
684
concluded that in many cases, Tb was increasing, and
values of EWL were not representative of steady-state
Tb conditions. By modeling heat storage and changes
in dry heat transfer at high Ta, these authors estimated that during a 5-h hyperthermic bout (Tb ¼ 448C)
at Ta ¼ 458C, savings of water associated with facultative hyperthermia were strongly dependent on
body mass, with 10 g birds saving 50% of TEWL,
but 1000 g birds incurring a net loss of water
(Tieleman and Williams 1999). The Ta of 458C
used by these authors closely approximates the current Ta maxima typical of sites in several subtropical
deserts [for instance, Yuma AZ, USA and Birdsville,
Australia (44.6 and 44.08C, respectively)—see
McKechnie and Wolf (2010)]. However, the relative
water savings bird can achieve via facultative hyperthermia are likely to decrease rapidly as air temperature increases above 458C. The mean hyperthermic
Tb for 28 species was 43.5 1.28C, with a maximum
value of 45.88C (Tieleman and Williams 1999), and
it is likely that biochemical constraints preclude the
possibility of birds maintaining Tbs much higher.
Thus, whereas facultative hyperthermia may permit
substantial savings in water at current air temperature maxima of about 458C, such savings will rapidly
decrease as air temperatures increase.
Coping with short-term anomalous
heat waves
For endotherms, one of the most detrimental, yet
understudied, aspects of anthropogenic climate
change may be the increasing frequency of extreme
climatic events, including heat waves and droughts
(Parmesan et al. 2000; McKechnie and Wolf 2010).
Examples of mass die-offs of birds and bats have
been reported several times over the past century
(Finlayson 1932; Miller 1963), but the number of
reports seems to have increased in the past decade
(Welbergen et al. 2008; McKechnie and Wolf 2010).
These short, but extreme, heat waves and droughts
impose very different pressures on endotherms than
does a slowly warming climate (Parmesan et al.
2000). During heat waves, the most important consideration is survival, often at the expense of reproduction, growth, or other necessary functions. Thus,
thermoregulation with the goal of maintaining Tb
below the upper lethal temperature should be of primary importance.
If short-term weather anomalies severe enough to
lead to sudden die-offs are sufficiently rare, the selective pressure imposed by these events should be
relatively low. However, increasing frequency of such
extreme events will increase the selective pressure
J. G. Boyles et al.
favoring individuals with the ability to cope with
them (e.g., thermal generalists should be at an advantage). If extreme climatic events selectively kill
some individuals, changes in frequencies of genotypes within the population will occur. For example,
Welbergen et al. (2008) found that mortality during
heat waves was greater among tropical black
flying-foxes (Pteropus alecto) than among temperate
gray-headed flying-foxes (Pteropus poliocephalus). In
addition to this variation in mortality rates between
species, they also found considerable variation in
mortality rates among genders and age classes. This
variation will obviously affect the demography of the
populations. Depending on the relationship between
tolerance above and tolerance below the TNZ within
an individual, these changes in demographic structure and the associated truncating of genetic diversity
caused by very high temperatures may lead to populations less capable of dealing with low temperatures or other normal weather events.
Adaptation and phenotypic plasticity
among heterothermic endotherms
Climate change will affect heterothermic endotherms
including daily heterotherms and hibernators. Since
conservation of energy is such an important aspect of
torpor, it was long thought that most species maximized the expression of torpor and hibernation, regardless of environmental conditions (Humphries
et al. 2003b). However, evidence is mounting that
heterotherms, especially hibernators, instead vary
the expression of hibernation in an adaptive
manner, adjusting it to fluctuating environmental,
ecological, and physiological conditions (Humphries
et al. 2003a; Munro et al. 2005; Boyles et al. 2007;
Wojciechowski et al. 2007; Landry-Cuerrier et al.
2008). Therefore, it is important to consider the possibility that adaptive thermoregulation and plasticity
in the expression of heterothermy might mediate responses to climate change. Recent evidence suggests
there is variation between populations in thermoregulation and in the metabolic rates of hibernating endotherms, and that the patterns are predictable along
latitudinal gradients (Munro et al. 2005; Fenn et al.
2009; Dunbar and Brigham 2010; Zervanos et al.
2010) (Fig. 3). It appears that at least some of that
variation is conserved even under common garden
conditions, suggesting some genetic component to
the patterns (Fenn et al. 2009). Thus, different populations may respond differently to similar changes in
climate, which may be especially important in widely
ranging species. Counteracting this adaptation may be
the relationship between Ta and energy expenditure
Adaptive thermoregulation in endotherms
685
Fig. 3 Body temperature across the season of hibernation for three populations of woodchucks (Marmota monax) across a latitudinal
gradient in North America (Maine: 438420 N; Pennsylvania: 408220 N; South Carolina: 348400 N). Reproduced from Zervanos et al.
(2010) with permission from The University of Chicago Press.
during hibernation, which increases exponentially
with a Q10 of 2–3. While this relationship may be
modified by metabolic inhibition, generally speaking,
a southerly population (in the northern hemisphere)
is likely hibernating at warmer temperatures than are
northerly conspecifics, and thus an increase in the
temperature of hibernacula will lead to a larger expenditure of energy in the southern population than
in the northern one (Dunbar and Brigham 2010).
Limits to adaption in endothermic
thermoregulation
While adaptation and phenotypic plasticity will undoubtedly buffer the effects of climate change on
endotherms, there are fundamental physiological
limits to how much, and how quickly, organisms
can respond to a changing climate. Endothermic
thermoregulation produces considerable metabolic
heat. Under normal circumstances, excess heat
energy is dissipated through evaporative, radiative,
conductive, or convective cooling. However, as environmental temperature increases, dissipation of heat
becomes increasingly difficult and Tb will necessarily
increase. It has been suggested that humans (and
other endotherms) can adapt to environmental temperatures only up to the point at which dissipation
of heat is impossible (Sherwood and Huber 2010).
Evaporative cooling, for instance, is the most efficient route of dissipation of heat when environmental temperature exceeds the Tb of an endotherm, but
endotherms face fundamental limitations to the efficiency of using evaporative cooling to lose heat.
There are biophysical limits to the rates of heat
loss via evaporative cooling, and these rates depend
heavily on the differential in water vapor between the
surface of the organism and the air. Evaporative
cooling can only occur when the surface temperature
of the endotherm is higher than the environmental
wet-bulb temperature, and evaporative heat loss is
severely curtailed at high humidities. To adapt to
more humid and hotter environments, endotherms
would need to increase their Tb to maintain a negative Tb–Ta gradient. However, since most endotherms regulate Tbs near lethal or physiological
limits, there is likely a limited scope for thermal
adaption in this sense.
686
Increasing Tb beyond the limits within which acclimation and adaptation are effective will slow
enzyme activities by shifting the equilibrium between
active and inactive states, and ultimately by denaturing proteins (Daniel et al. 2010). Additionally, cellular function will be disrupted by damage to the
membranes of cells and organelles (Hazel 1995).
Even if membranes were not directly affected by temperature, an increase in Tb may cause an increase in
the production of reactive oxygen species (ROS),
which will damage mitochondrial membranes and
affect organelle’s function (Brand et al. 2004).
Reactive superoxide (O2) is produced in the
high-energy environment of the inner mitochondrial
membrane, and mitochondria possess a natural, enzymatic defense system. Superoxide dismutase turns
superoxide into the less reactive hydrogen peroxide
(H2O2). Catalase and glutathione peroxidase
break-down hydrogen peroxide into water and molecular oxygen (H2O þ O2) thereby eliminating the
threat from ROS. However, the system is not perfect,
and secondary radicals, particularly hydroxyl radicals
(oOH), form from superoxide. These radicals react
with the mitochondrial membrane, disrupting its
proper function. Heat stress increases ROS production and thereby performance in mammals and birds
(Zuo et al. 2000; Azad et al. 2010), but it is likely to
be a mechanism that can facilitate negative effects of
climate change on animal function. For example,
ROS can cause a decrease in telomere length and
thereby shorten lifespan and decrease fitness
(Monaghan et al. 2009). Furthermore, increases in
Tb can affect the efficacy of ATP production if the
thermal sensitivities of mitochondrial proton leak
and oxidative phosphorylation shift so that an increasing proportion of the electronmotive force
across the inner mitochondrial membrane is released
as heat rather than being converted into ATP (Abele
et al. 2002; Seebacher et al. 2010). The consequences
would be that heat load would increase thereby exacerbating already existing heat stress, and that the
cells would be starved of ATP.
Conclusions
While much is known about endothermic thermoregulation, we know unfortunately little about how
variation in Tb characteristics of individuals, populations, and species will interact with the effects of
climate change to determine the response of endotherms. We have already addressed the quickly growing body of literature using mathematical modeling
to address the effects of climate change on endotherms. Future efforts along these lines will
J. G. Boyles et al.
undoubtedly lead to new insights in the field, but
will be vastly improved by including the types of
variation we address in this review. As a simple example, McKechnie and Wolf (2010) modeled the
survival time of birds exposed to increased frequencies of extreme heat waves. They assumed physiological parameters were fixed for birds of a given body
mass and therefore predict that all birds of a given
size will be equally stressed under the same conditions. However, species’ responses will be influenced
by interspecific variation in trade-offs between tolerance to dehydration tolerance and the risk of hyperthermia. For instance, variation in the rate at which
EWL increases with increasing environmental temperatures will mean that, for a given body mass,
some species will reach their limits of tolerance to
dehydration more rapidly than will others. Such variation may be expected to directly affect selection on
tolerance of high Tb and will be vital in future modeling efforts.
It appears increasingly clear that thermoregulatory
characteristics of endotherms are adaptive and have
been shaped by past and current selective pressures
when exposed to temperatures below the TNZ.
However, little research has explicitly addressed the
possibility that responses to high temperatures vary
among and between populations and species in a
manner consistent with the predictions of the concept of adaptive thermoregulation (Angilletta et al.
2010). Furthermore, a vital line of future enquiry in
climate research will be to determine the extent to
which endotherms can acclimate and acclimatize to
rapidly changing selective pressures associated with
anthropogenic climate change and how important
those shifts will be in terms of fitness. Recent evidence suggests that climate change has led to shifts in
phenology and morphology and subsequently increased fitness in some endotherms (Ozgul et al.
2010). However, other authors have argued that evolutionary processes have done little to stave off extinctions associated with climate change (Parmesan
2006).
Research on adaptive thermoregulation and thermal sensitivity in endotherms in a manner relevant
to climate change will be difficult for several reasons.
First, long generation times and relatively slow reproductive rates make mammals and birds less conducive to experimental evolutionary research than
are many ectotherms. Although a few well-studied
model species have been, and will continue to be,
important in elucidating the mechanisms of adaptation, some research on adaptation will likely have to
be conducted on populations exposed to natural selective
pressures.
Second,
obvious
ethical
Adaptive thermoregulation in endotherms
considerations mean that it will be difficult (although
not impossible) to gain substantial new insights into
how endotherms respond to extremely high temperatures under controlled conditions. Thus, much of
the research on extreme weather events may have
to take advantage of natural events, making planning
and experimental design difficult. Finally, the consideration of adaption and phenotypic plasticity is likely
to increase complexity and therefore difficulty in
writing, interpreting, and presenting models of responses by endotherms to climate change. Despite
these difficulties, we believe the study of adaptive
responses to a changing climate has important implications for both our understanding of the evolutionary processes governing thermoregulation in
endotherms and of the conservation of our natural
world.
Acknowledgments
Special thanks to M. Sears and M. Angilletta for
organizing this symposium and inviting our participation. B. Cooper and C. Schmidt provided useful
comments on earlier versions of the manuscript.
We thank Blair Wolf and an anonymous reviewer
for comments that greatly improved the quality of
the manuscript.
Funding
University of Pretoria Post-Doctoral Fellowship
and a Claude Leon Post-Doctoral Fellowship (to
J.G.B.); PhD. bursary from the DST/NRF Centre of
Excellence at the Percy FitzPatrick Institute (to B.S.);
Department of Zoology and Entomology and Faculty
of Natural and Agricultural Sciences at the University
of Pretoria funds (to J.G.B.).
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