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Temperature effects on the metabolism of amphibians and reptiles: Caveats and recommendations

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129
chapter six
Temperature effects
on the metabolism of
amphibians and reptiles
Caveats and recommendations
Denis Vieira de Andrade
Introduction
All animals need energy. Indeed, each and every activity, or behavior,
an animal will engage in throughout its lifetime will require the use of
energy. As in the majority of other animals, Squamate reptiles derive
their energy from the breakdown of organic substrates, often referred to
as catabolism, acquired through feeding. Adenosine triphosphate (ATP)
will eventually be hydrolyzed to adenosine diphosphate (ADP) and Pi,
releasing the energy stored in its chemical bonds to power subcellular
structures, cells, tissues, organs, and systems, which, acting under neural
and/or humoral control, will be manifested as identiable activities and
behaviors (see Chapter 1). Thus, by focusing on metabolism, one is in a
privileged position to appreciate the interactions of a given organism in
terms of energy exchange with the biotic and abiotic components of its
particular environment. This is of indisputable value as it can reveal cur-
rent and future tradeoffs in terms of functional and energetic constraints
Contents
Introduction .................................................................................................... 129
Body temperature variation ......................................................................... 132
Value of incorporating thermal biology into metabolic determinations ..... 134
Temperature variation and metabolism...................................................... 136
Methodological caveats and recommendations ........................................ 139
Concluding remarks ...................................................................................... 146
Acknowledgments ......................................................................................... 147
References ....................................................................................................... 147
© 2016 by Taylor & Francis Group, LLC
130 Amphibian and reptile adaptations to the environment
with important ecological and evolutionary consequences (see Bennett
1982; Congdon etal. 1982; Nagy 1983; Pough etal. 1992; Nagy etal. 1999;
McNab 2002; Suarez 2012). Putting it simply, every living organism
requires energy to exist and the patterns of its acquisition and utilization
are fundamental for the success of any given species.
It follows that the relevance of metabolic measurements has always
been acknowledged by animal physiologists, including those interested
in amphibians and reptiles. As a consequence, metabolic rate determina-
tion is, quite probably, one of the most intense and widespread physiologi-
cal parameters quantied for any animal group (Benedict 1932; Kleiber
1947, 1961; Bennett and Dawson 1976; Schmidt-Nielsen 1984; MacNab
2002; Suarez 2012). Furthermore, aerobic metabolism can be determined
based on the rate of oxygen consumption, which is relatively uncompli-
cated, accurate, and not an overly expensive methodology (Lighton 2008).
Accordingly, in this chapter, I will focus entirely on aerobic metabolism
and will use rates of oxygen uptake and metabolism interchangeably,
as this will sufce to tackle the main goals of this review. This does not
imply, to any extent, the denial of the relevance of anaerobic metabolism
for the behavioral ecology and physiology of amphibians and reptiles,
and readers are advised to consider some early, but now classic, studies
focusing on this particular aspect (Bennett 1972; Bennett and Licht 1974;
Ruben 1976; Feder and Arnold 1982; Gleeson 1991).
Metabolic rate is inuenced by a number of intrinsic features depen-
dent on the animal being measured (e.g., body mass, sex, and fed state), as
well as by external parameters, usually biotic or abiotic variables from the
particular habitat where the animal is found (see McNab 2002). Among
the physical abiotic variables known to exert an inuence on the metabolic
rate of animals, temperature can easily be identied as the one whose
effects have been largely investigated. This is justiable, as temperature
is widely recognized as the single physical parameter with the most pro-
found impacts on animal function (Huey 1982; Angilletta 2009; Tattersall
etal. 2012). In the case of ectothermic animals, including amphibians and
reptiles, the inuence of temperature on metabolism might be especially
important in an ecological and evolutionary context when compared
to endothermic animals (Angilletta et al. 2002). The metabolic rate of
amphibians and reptiles is orders of magnitude lower than similar sized
endothermic vertebrates (Bennett 1978, 1980; Else and Hulbert 1981; Pough
1983; di Prampero 1985; Else and Hulbert 1985; Bennett and Harvey 1987;
Bennett 1994; Hedrick etal. 2015) meaning that, along with the lack of
effective insulation, their capacity to use metabolically derived heat for
body temperature regulation is usually (but not always, as discussed
later in this chapter) negligible (see Seebacher et al. 2005). As a conse-
quence, body temperature regulation in amphibians and reptiles is highly
dependent on external heat sources and the behavioral exploration of the
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131Chapter six: Temperature effects on the metabolism
different thermal niches available in a particular habitat (Bartholomew
1982; Huey 1982; Hutchison and Dupré 1992; Seebacher et al. 2005). This
thermoregulatory strategy is often conducive to a daily or seasonal ther-
mal cycle in which animals naturally are exposed to very large uctua-
tions in body temperature and changes in activity level (Huey and Pianka
1977; Avery 1982; Gregory 1982; Pinder etal. 1992; Abe 1995; Carvalho etal.
2010; Gunderson and Leal 2015; Sanders etal. 2015). For example, differ-
ences of more than 10°C in the body temperature during a diurnal cycle
are quite commonly experienced by many species of amphibians and
reptiles (Brattstrom 1963, 1965; Hutchison and Dupré 1992; Andrade etal.
2004). All these factors taken into consideration underscore the relevance
of quantifying the effects of temperature on the metabolic rate of these
particular animals.
Indeed, temperature effects on the metabolic rate have been thor-
oughly quantied in diverse representatives of amphibians and reptiles
from the early days of comparative animal physiology up to the pres-
ent (Benedict 1932; Bennett and Dawson 1976; Andrews and Pough 1985;
Gatten etal. 1992; Rome etal. 1992; Hillman etal. 2009). As is true for
other ectothermic organisms, the metabolism of amphibians and rep-
tiles usually increases with body temperature for the temperature range
within their thermal tolerance limits (Bennett and Dawson 1976; Gatten
et al. 1992; Halsey et al. 2015). Beyond these limits, functional erosion
will happen and disrupt the relationship between physiological function
and temperature (Huey and Stevenson 1979). Within the limits of ther-
mal tolerance, the metabolism of amphibians and reptiles will increase
with temperature, often linearly, approximately doubling for each 10°C
increase in body temperature; that is, the Q10 value usually hovers around
2 (Bennett and Dawson 1976; Gatten etal. 1992; White etal. 2006; Halsey
etal. 2015). As body temperature regulation in amphibians and reptiles
is dissociated from metabolic heat production, the temperature effect on
their metabolism is assumed to be a mostly passive thermodynamic con-
sequence of the temperature on the biochemical reactions sustaining the
different physiological systems (see Gillooly etal. 2001), including those
sustaining changes in activity levels (see Halsey etal. 2015). The sum of
the energetic expenditures of all these reactions is nothing more than the
metabolic rate itself. Although the same can be said for any living organ-
ism, there is a fundamental difference between ectothermic and endother-
mic organisms on how metabolism varies as a function of temperature
(Bennett 1980; Bartholomew 1982; Pough 1983). This is related primarily to
the fact that endotherms usually (but not always) will defend a constant
body temperature with the expense of metabolic expenditure, a case usu-
ally referred to as homeothermic endothermy (Lowell and Spiegelman
2000; McNab 2002). In such cases, there will be a lower and upper critical
temperature below and above which, respectively, animals will spend a
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132 Amphibian and reptile adaptations to the environment
surplus energy to keep their body temperature constant. In the middle
temperature interval set by the lower and upper critical temperatures,
animals can modulate the heat being produced with the amount of heat
being exchanged with the environment, keeping their body temperature
constant with little, or negligible, change in metabolism. This is referred
to as the thermoneutral zone (Nichelmann and Tzschentke 1995).
While the concept of thermoneutral zone has long been incorporated
in the measurements of the temperature effects on the metabolism of
endothermic organisms, the peculiarities of body temperature regulation
of amphibians and reptiles has often been neglected by those measur-
ing their metabolic rate. The current paradigm for the assessment of the
effects of temperature variation on the metabolism of amphibians and
reptiles is the measurement of animals submitted to constant temperature
regimes for a pre- or postestablished experimental period that can extend
for hours or even days. In some cases, the duration of the experiment and
even the choice of the experimental temperatures are often determined
without a proper consideration of the thermal biology of the animals
being measured. As a consequence, animals that normally experience
considerable variation in body temperature during the diurnal cycle for
their entire life are submitted, by default, to a constant temperature regime
while having their metabolic rate determined. As experiments may last
for periods up to many days, animals are then subjected to experimen-
tal conditions that they most likely never experience in nature. Although
previous data on the metabolism of amphibians and reptiles obtained
under constant temperature regimes remain relevant (see Benedict 1932;
Bennett and Dawson 1976; Andrews and Pough 1985; Gatten etal. 1992;
Rome etal. 1992; Hillman etal. 2009; and references therein), more solid
and reliable insights about energy use may be attained by narrowing the
gap between methodological protocols and the thermal biology of the
experimental organisms (see Newman etal. 2015 for a similar approach
on another subject). Thus, goals of this chapter can be dened as (1) a plea
for the incorporation of thermal biology information in the assessment of
the temperature effects on the metabolism of amphibians and reptiles; (2)
an alert that temperature effects on metabolism can be associated with
subtle attributes of temperature variation rather than to plain differences
in mean averages; and (3) a discussion on the methodological caveats, and
potential ways to get around them, involved in the examination of the
temperature effects on the metabolism of amphibians and reptiles.
Body temperature variation
As true for any ectothermic organism, the body temperature of amphib-
ians and reptiles is highly dependent on the prevalent ambient thermal
conditions, which are explored predominantly via behavioraladjustments
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133Chapter six: Temperature effects on the metabolism
(Huey and Pianka 1977; Seebacher et al. 2005; Pough et al. 2015).
Thermoregulatory costs and benets are integrated for a given set of condi-
tions and tradeoffs resulting in different thermoregulatory patterns (Huey
and Slatkin 1976) and activity (Gunderson and Leal 2015). Obviously, this
response also varies considerably according to thermal characteristics of
the environment and with the thermoregulatory capabilities of the animal
being considered. For example, the high specic heat capacity of water
makes it almost impossible for the majority of the aquatic amphibians or
reptiles to regulate their body temperature at a temperature different from
that of the water body where they happen to be immersed (Hillman etal.
2009). For the body size range typical of most amphibians and reptiles,
any thermal difference will rapidly equilibrate with the water as they lack
any effective insulation. We can also attribute diel and seasonal changes
in body temperature that are minimized for those organisms thriving in
the aquatic environments, compared to those found in terrestrial habitats,
to the physical properties of the water (Tracy 1976, 1982; Spotila etal. 1992).
There are, however, few remarkable exceptions, even in aquatic habitats.
Leatherback sea turtles and large crocodiles, for example, are able to use
their large body size, coupled with metabolic and cardiovascular adjust-
ments, to keep their body temperature relatively constant despite consid-
erable changes in the thermal environment (Fray etal. 1972; Seebacher
etal. 1999; Bostrom etal. 2010). Leatherbacks are, indeed, able to keep their
body temperature well elevated above sea water temperature (Paladino
etal. 1990; Casey etal. 2014). Finally, incorporating historical and adaptive
factors, different species will be more dedicated to buffering body tem-
perature from change in the thermal environment (commonly referred to
as active thermoregulators), while others will be more relaxed in terms of
allowing greater body temperature variations (referred to as thermocon-
formers) (Huey and Slatkin 1976).
In general, amphibians, with their predominantly nocturnal activity,
their close association with water, and their moist skin, which constrain
some thermoregulatory possibilities, are biased to the thermoconfor-
mity end of the scale (Tracy 1975; Hillman etal. 2009). Exceptions exist
(Shoemaker et al. 1987, 1989; Tattersall etal. 2006), however, including
some strategies for regulating the temperature of the environment of
developing eggs (Méndez-Narváez et al. 2015). Reptiles, on the other
hand, present a more even distribution on the thermoregulatory spec-
trum, with diurnal heliothermic lizards representing the epitome of active
thermoregulation (Huey 1982). Abandoning our mammalian paradigm,
an important point to be made is that an accurate thermoregulation for
an ectotherm organism does not necessarily mean a higher and constant
body temperature. While a higher constant body temperature does indeed
favor the performance of many activities that depend on muscle contrac-
tion, it is equally true that lower body temperatures favor important
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134 Amphibian and reptile adaptations to the environment
aspects of life history. Most importantly for the sake of this chapter, lower
body temperatures correspond with lower metabolic rate and an associ-
ated savings in energy expenditure.
In conclusion, a fundamental step in the assessment of the effects of
temperature on the metabolism of amphibians and reptiles is the assess-
ment of variation in body temperature experienced by these animals
under natural settings. Ideally, one should accomplish this by incorporat-
ing data on activity within a daily and seasonal time scale. Sadly, such
studies are exceedingly scarce, especially for amphibians.
Value of incorporating thermal biology
into metabolic determinations
Most estivating or hibernating species exhibit signicant changes in mean
body temperature, and they also exhibit marked changes in their daily
pattern of body temperature variation. For example, in the black and white
South American tegu lizards, Salvator merianae, body temperature exhibits
a marked variation along the daily cycle during the hot and rainy sea-
son (roughly corresponding to the spring and summer) in Southeastern
Brazil (Andrade etal. 2004; Milsom etal. 2012; Sanders etal. 2015). Similar
changes in activity and body temperature are widespread in many other
species of reptiles and amphibians (Gregory 1982; Abe 1995). In the spe-
cic case of S. merianae, active lizards emerge from their nightly retreat
early in the morning to bask, resulting in a rapid rise in body tempera-
ture accompanied by a remarkable increase in heart rate (Andrade etal.
2004; Sanders etal. 2015). Tegus then keep their body temperature high,
around 35°C, for the period they are active. Afterwards, in late afternoon,
lizards halt activity and return to the shelter where they will spend the
night. At this time, a massive and almost instantaneous drop in heart
rate is observed, even before any change in body temperature is noticed.
As a consequence, much of the heat gained during the day is trapped
within the lizard’s body and is lost only very slowly throughout the night
(Andrade etal. 2004; Sanders etal. 2015), although some thermogenesis
may also contribute (discussed in the next section). On the other hand,
during the cold and dry winter months, tegus spend the entire season in
a dormant state hidden in shelters dug in the soil. Under this condition,
body temperature equilibrates with shelter temperature and daily uc-
tuations in body temperature are compressed to the level dictated by the
uctuations in the shelter temperature, which are minor since shelters are
usually well insulated (Milsom etal. 2012).
The detailed description of the tegu’s thermal biology just discussed
was only obtained years later, after some researchers, myself included, had
examined the seasonal variation in a number of physiological parameters,
including the seasonal changes in metabolism (Abe 1983, 1995; Andrade
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135Chapter six: Temperature effects on the metabolism
and Abe 1999; Andrade etal. 2008a,b). The problem was that at the onset
of such investigations, tested temperatures were established not on the
basis of the thermal biology of the lizards themselves but on the average
temperature of their shelters (i.e., 17°C and 25°C). As a consequence, half
of our results were obtained at a temperature (25°C) that coincides only
briey twice a day with the body temperature of active tegus as it varies
up and down along its circadian cycle, while the other half, obtained at
the lower temperature of 17°C, completely fails to reect the body tem-
peratures experienced by the active tegus, at any given time (Figure 6.1).
For the dormancy period, as the animals allow their body temperature
to equilibrate with their retreat shelters, the lower temperature of 17°C
agrees well with the temperature experienced by the animals. On the other
hand, the higher experimental temperature of 25°C is never experienced
by any dormant lizards (see Andrade etal., 2004). Adjusting experimental
temperatures across different seasons was a necessary compromise for
comparative purposes. However, I regret that some of the previous physi-
ological measurements on this lizard species were not made in tempera-
tures more realistically bounded to its thermal biology. Undoubtedly, the
validity of any discussion on aspects of animal temperature and energet-
ics is certainly compromised when metabolic determinations are taken
19.00
15
20
25
30
35
22.00 01.00 04.00 07.00 10.00
17°C
25°C
Time (h)
Body temperature (°C)
Figure 6.1 Daily variation in the body temperature of an adult tegu lizard
(S. merianae) (red circles) superimposed on arbitrarily chosen experimental tem-
peratures (blue dashed lines). The graph illustrates how the choice of experimental
temperatures without proper consideration of the thermal biology of the animal
under study may seriously compromise data interpretation (see text for details).
Body temperature data were recorded by radio-telemetry during the season of
activity for this species under seminatural conditions (see Sanders etal. 2015).
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136 Amphibian and reptile adaptations to the environment
at temperatures that the animal never experiences or experiences only
briey during the day. Clearly, solid ecophysiological inferences involving
the examination of temperature effects on metabolism demand a careful
consideration of the thermal biology of the organism being studied (see
also Dabruzzi etal. 2012) and such an approach, although seemingly obvi-
ous, should be actively encouraged.
Temperature variation and metabolism
If the choice of experimental temperatures may have some obvious con-
sequences for assessing the temperature effects on the metabolism of
amphibians and reptiles, differences in the thermal regime, between
those normally experienced by the animals and the one to which they are
subjected during experimental measurements, may have more subtle and
largely neglected effects. The central difference here lies in the fact that
while most amphibians and reptiles experience a circadian cycle of body
temperature variation (Huey and Pianka 1977; Bartholomew 1982; Huey
1982; Hutchison and Dupré 1992), metabolic measurements have tradition-
ally been made under a constant thermal regime (Bennett and Dawson,
1976; Andrews and Pough 1985; Gatten etal. 1992; Rome etal. 1992). While
the potential caveats associated with the neglect of thermal regimes are
uncertain, we can expect that they are likely to be more pronounced in
those species showing more marked thermal cycles (see Kearn etal. 2015)
and for experimental protocols demanding longer measurement dura-
tions, such as many days. Constant temperature measurements are cer-
tainly adequate to answer specic questions and have contributed to our
understanding of the intricate interplay between metabolism and tem-
perature in amphibians and reptiles. However, extrapolations based on
metabolic measurements taken under constant temperature into an eco-
logical/behavioral framework, in which animals normally experience a
uctuating thermal regime, might be potentially misleading, particularly
when examining processes over longer time scales (see also Kingsolver
etal. 2015; Stahlschmidt etal. 2015).
Daily thermal cycles are known to inuence a number of physiological
funct ions/rhythms, often in asso ciation with light-dark cycles (Underwood
1984). However, su rprisingly few studies have being dedicated to the effects
of thermal cycles on metabolism. Gavira and Andrade (2013a) examined
the effect of a uctuating thermal regime (12:12 h, 20–30°C) compared to
the equivalent constant temperature (i.e., 25°C) during the digestion of a
neotropical pitviper, Bothrops alternatus, a process that extends for many
days (Figure 6.2). Their results showed that both the resting metabolic rate
measured before feeding and the maximum rate measured during the
meal digestion were lower in those snakes measured under the uctuat-
ing thermal regime. However, as the duration of the digestion was longer
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137Chapter six: Temperature effects on the metabolism
in this same group, the nal energetic cost of meal digestion did not dif-
fer between the different thermal regimes. These results allowed for the
discussion of some important ecological consequences of the temperature
effects on the digestion of snakes that would not be possible by examina-
tion only under constant thermal regimes. Indeed, the initial impetus to
perform this study was the observation that captive rattlesnakes (Crotalus
durissus) kept in outdoor pens were able to nish meal digestion even when
experiencing nighttime temperatures as low as 6°C, as long as they could
freely thermoregulate in the intervening days, while, under experimental
Body temperature (ºC)
15
20
25
30
35
40
(b)
Time (days)
PostfeedingFasting
0
0
50
100
150
200
250
300
VO2 (mL O2 · kg–1 · h–1)
.
(a)
50 100 150
Time (h)
200
250
Figure 6. 2 (a) The postprandial metabolic response of the neotropical viperid
snake B. alternatus fed with a mouse meal equaling 30% of the snake’s body mass
under a constant thermal regime of 25°C (lled circles) and under a 12:12 h uctu-
ating thermal regime from 20°C to 30°C (open squares). The metabolic response
recorded under the latter regime reects more realistically the body temperature
variation normally experienced by snakes (as shown in b). Time “0” indicates the
time of feeding; samples at every 70 min; n = 8 (see Gavira and Andrade 2013a).
(b) Body temperature variation recorded from an adult rattlesnake, C. durissus,
few days prior and after feeding a rat meal equaling to 30% of its body mass
(D.V. Andrade, unpublished data).
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138 Amphibian and reptile adaptations to the environment
conditions they would usually fail to complete digestion at constant ther-
mal regimes as high as 20°C (Andrade, unpublished observation).
Focusing on the effects of thermal regime on the resting metabolic
rate of B. alternatus clearly show that animals under a uctuating regime
have a lower metabolism than those submitted to the constant regime. For
example, the metabolic rates measured at constant 20°C and 30°C were
28% and 18% greater than the rates measured at these same temperatures
when they uctuate between each other by a 12 h interval (Gavira and
Andrade 2013a). In another viperid species, the South American rattle-
snake, C. durissus, we have found that the lowering of metabolism under
uctuating thermal regimes compared to constant ones becomes more
pronounced as the temperature interval considered shifts to higher tem-
peratures (Fabrício-Neto etal., unpublished data). One possible explana-
tion for these observations may involve changes in activity level and, thus,
in the accompanying level of metabolism as the temperature increases.
In this regard, Halsey etal. (2015) demonstrated, in insects and crusta-
ceans, that the temperature effect on metabolic rate incorporates changes
in metabolism that were associated with changes in activity level rather
than to temperature per se. We do not know if such observations are valid
for amphibians and reptiles and whether this may explain differences
in metabolism between different thermal regimes. However, it seems
plausible to expect that differences in the level and recurrence of activity
cycles might occur between animals kept under a constant or uctuat-
ing thermal regime and, therefore, affect metabolic measurements (see
Andrade etal. 2008b). Finally, it remains unknown whether submitting
the animals to experimental conditions more diverse from their normal
thermal regimes causes any stress-associated responses, which, in turn,
might inuence the level of metabolic and/or locomotory activity.
Body temperature variation encompasses more complex changes than
could be assessed by experimentally submitting animals to constant lev-
els of different mean temperatures (Vázquez etal. 2015). Also, responses
to complex and more realistic regimes in temperature variation can be
modulated by acclimation processes and shifts in thermoregulatory
behavior (see Chapter 2; see also Angilletta 2009; Huey etal. 2012; Basson
and Clusella-Trullas 2015), with important interactive consequences for
growth, metabolism, osmoregulation (Davies et al. 2015; Stahlschmidt
etal. 2015), and, potentially, to the evolution of physiological adaptation
and conservation (see Sunday et al. 2014; Agustín et al. 2015; Buckley
etal. 2015). Thus, thermal regime, temperature variance, distribution of
thermal microclimates, occurrence of extreme values, and predictability
of temperature changes are all relevant attributes associated with body
temperature variations that have been recently acknowledged as equally
important, sometimes even more relevant, as differences in average val-
ues (see, e.g., Ketola etal. 2012; Caillon etal. 2014; Manenti et al.2014;
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139Chapter six: Temperature effects on the metabolism
Caldwell et al. 2015; Dowd et al. 2015; Ketola and Saarinen 2015; Ma
et al. 2015; Turriago et al. 2015; Vázquez etal. 2015). Indeed, Sears and
Angilletta (2015) showed that both the heterogeneity and spatial structure
of the temperature distribution in the habitat are important components
to understand the potential effects of temperature changes on organismal
performance. Also, responses to temperature may differ with life stages,
and conditions experienced early in life may result in long-lasting later
consequences (Levy etal. 2015; Turriago etal. 2015). For example, Horne
etal. (2014) showed that differences in diel temperature variance during
the embryonic development of the sea turtle Caretta caretta cause signi-
cant phenotypic changes, which potentially inuence their survival. In
the snake Notechis scutatus, Aubret and Shine (2009) observed that raising
juveniles under different temperature treatments makes them adjust to
their respective thermal regimes but, at the same time, decreases their
later potential for adjusting to a sudden shift in ambient conditions. Also
in snakes, Lorioux et al. (2012) found that suboptimal thermal regimes
inuenced hatchling traits in the Children’s python, Antaresia childreni, by
maternal effects. Thus, the basic idea brought into consideration in this
section is that before examining the temperature effects on any biologi-
cal parameter, we should rst question the attributes of the temperature
variation itself and, if possible, determine the thermal history of the study
animals. The recognition that such aspects are of particular relevance in
the realm of conservation physiology (see Chapter 7; Carey 2005; Wikelski
2006; Niehaus etal. 2012; Kingsolver etal. 2015), especially given changes
in the thermal environment, both at global and microhabitats scales, is
one of the most recognizable footprints associated with modern human
activity (IPCC 2014) with some predicted disastrous consequences for bio-
diversity (Sinervo etal. 2010). Therefore, the examination of the energetic
interrelations of animals (i.e., metabolic determinations) under variable
and dynamic thermal conditions and in combination with information
on their previous thermal history may provide a better and more realistic
means to evaluate the consequences of anthropogenic inuences on the
environment and how animals might respond to them.
Methodological caveats and recommendations
Although metabolic rates are almost always inferred from the determina-
tion of rates of oxygen uptake, I will not discuss specic problems (and
possibilities) associated with respirometry. For this purpose, readers are
referred to Lighton (2008). Herein, I will focus uniquely on some poten-
tial confounding factors intrinsic to the assessment of temperature effects
on metabolic determinations. The recognition of such problems is neither
new nor original (see Benedict 1932; Bartholomew 1982) and, in many
instances, the potential to bias data interpretation is indeed negligible,
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140 Amphibian and reptile adaptations to the environment
as has been traditionally assumed (Bartholomew 1982; Fraser and Grigg
1984). However, as physiological data are being incorporated into predic-
tive scenarios involving changes of a few degrees celsius in environmen-
tal temperatures, minor uncertainties in the assessment of temperature
effects on metabolism may actually become nonnegligible (see similar
discussion in Bakken and Angilletta 2014). This becomes especially true
as the empirical evaluation of temperature effects on organismal func-
tions, as well as the modeling of it, began to be framed on the basis of
scenarios of temperature change of a few degrees over a projected and
dilated time scale. Indeed, the assessment of the effects of minor changes
in body temperature may prove to be an approach more realistically linked
to the predicted alterations in the physical environment (see Kearney and
Porter 2004; Kearney etal. 2009). As a consequence, the reliability of such
approaches will forcedly depend on the accuracy of adequately controlling
and monitoring the body temperature of the animals under examination.
There are few experimental protocols that appear to be as simple
and straightforward as the examination of the temperature effects on
metabolism. Nonetheless, even fewer protocols are haunted by so many
caveats. A most common procedure will be as follows: animals are
placed inside respirometry chambers, chambers are placed inside tem-
perature-controlled environments, measurements are taken, tempera-
ture is changed, measurements are repeated, and any differences found
in the results are assumed to reect differences occurring between the
two temperatures tested. However, controlling the temperature of the
climatic chambers and/or rooms does not ensure that the body tem-
perature of the experimental animal is at that same temperature. Many
factors can contribute to the occurrence of a differential between body
and environmental temperature. Enough time has to be allowed for the
animals to equalize their temperature with the environment and this is
inuenced by the dynamics of temperature change and by body size.
Larger animals will require longer periods to reach thermal equilibria;
moreover, vasomotor adjustments, such as peripheral vasoconstriction,
can extend this period even further (Seebacher et al. 2005). For example,
a rattlesnake with a body mass around 1 kg can take 4–6 h to reach ther-
mal equilibrium as ambient temperature is shifted between 20°C and
30°C, and this period varies with the direction of temperature change
(Fabrício-Neto etal., unpublished data; Figure 6.3). If ambient tempera-
ture is dynamically changed at faster rates (e.g., 12°C/h), this same snake
will never reach thermal equalization (Figure 6.3). A3 kg tegu lizard,
S. merianae, can withstand signicant temperature differentials up to
12 h due to its larger body mass and remarkable vasomotor response
(Sanders etal. 2015). Thus, under protocols focusing on rapid tempera-
ture changes, assumed body temperature (based on the control of ambi-
ent temperature) will be considerably different from the actual body
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141Chapter six: Temperature effects on the metabolism
0
5
10
15
20
25
30
02 468
Temperature (°C)
55
50
45
40
35
30
25
20
Time (h)
20
22
24
26
28
30
32
(a)
(b
)
Time (min)
Temperature (°C) Temperature (°C)
020406080100 120140 160
Figure 6. 3 (a) Body temperature variation of an adult rattlesnake (C. durissus) as
environmental temperature (dotted lines) is changed from 20°C to 30°C (open
squares) and from 30°C to 20°C (open circles). Notice that body temperature
requires many hours to equalize with environmental temperature and that this
time is affected by the direction of temperature change. (b) The body temperature
of the same snake species (open circles and inverted triangles) never reaches equal-
ization if environmental temperature (open squares and triangles) is changed at
a rapid (12°C/h) rate. (a) Depicts mean values of four individual snakes, with dots
10 min apart from each other. (b) Depicts data from one individual snake dur-
ing warming (open circles and squares) and cooling (open triangles and inverted
triangles) trials; dots are 1 min apart; temperature change for both curves start
at 25°C, at time0. All data were recorded from snakes surgically implanted with
temperature data loggers. (Courtesy of R.S.B. Gavira and A. Fabrício-Neto, unpub-
lished data.)
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142 Amphibian and reptile adaptations to the environment
temperature experienced by the animals, and this effect is magnied
by larger body sizes (see also McNab and Auffenberg 1976; Auffenberg
1981; Tracy 1982; Spotila etal. 1992).
Even when animals are allowed enough time to reach thermal equi-
librium with their surroundings, body temperature may not be exactly
the same of the environment (see Sunday etal. 2014). Although that might
be accurate for most ectothermic organisms, in most instances, particu-
larly for small-bodied reptiles (Fraser and Grigg 1984), there are cases
in which temperature differentials will occur. Live animals are contin-
uously engaged in different physiological processes and have thermal
properties inherently different from the physical medium surrounding
them, which, in turn, affect their rates of heat exchange and ultimately
their body temperature (see a similar criticism for determining opera-
tive body temperatures in Seebacher and Shine 2004). Amphibians, in
general, have a highly permeable skin that makes them particularly sus-
ceptible to elevated rates of evaporative water loss (Hillman etal. 2009).
As water evaporates, the heat required for the phase change, that is, the
heat of vaporization, is taken up from the surface of the material where it
happens to occur (the animal skin in this case) causing its temperature to
decrease by evaporative cooling. Thus, animals with high rates of evapo-
rative water loss, such as amphibians, will usually exhibit a body sur-
face temperature cooler than the surrounding medium (Brattstrom 1963;
Bartelt and Peterson 2005). This effect will be greater at low air humidity
and high temperatures, following an increase in the potential for water
to vaporize (see Gates 1980). Whether the evaporative cooling happening
on the surface of the animal’s body will affect core body temperature will
depend on other components involved in thermal equilibration (Tracy
1975, 1976; Hillman etal. 2009). In the case of reptiles, with generally low
rates of cutaneous evaporative water loss, evaporative cooling will occur
mainly from the evaporation from the respiratory surface and will have,
supposedly, low potential to inuence body temperature (Bartholomew
1982).
A relatively frequent misconception about the attributes of ectother-
mic organisms is the false belief that they do not produce heat. In other
words, only true endotherms are capable of thermogenesis. In fact, as long
as an organism is alive (and actually for a short decay period after its
death) and energy is transformed from one form to the other, part of this
energy will be dissipated as heat (see Kleiber 1961). Therefore, amphib-
ians and reptiles do generate heat all the time, but as their metabolic rate
is normally orders of magnitude lower than a typical endotherm, the
amount of heat metabolically derived is, in most instances, negligible
for the regulation of their body temperature (Pough 1983). That is, under
ordinary conditions, the body temperature of amphibians and reptiles is
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143Chapter six: Temperature effects on the metabolism
largely dictated by the availability of thermal niches in the environment,
which are explored by behavioral thermoregulation and a few physiologi-
cal adjustments. However, as far back as 1832, we have been informed by
a report from Lamarre-Picquot to the French Academy of Sciences that
some python species coil around their eggs while brooding and endog-
enously elevate their body temperature, possibly for the sake of providing
a more propitious environment for the developing embryos. Although the
report of Lamarre-Picquot was largely discredited by the French Academy,
numerous subsequent studies conrmed and expanded his pioneering
observations (see Benedict etal. 1932; Hutchison etal. 1966; Brashears and
DeNardo 2013). Since then, the case of brooding pythons incubating their
eggs by means of metabolically derived heat (see Figure6.4) has become
“the rule to illustrate the exception” that even organisms belonging to a
group readily recognized as ectotherms can, under certain circumstances,
exhibit thermogenesis of a magnitude great enough to affect body tem-
perature (Bartholomew 1982). As for the matter considered in this chap-
ter, this adaptation means, once again, that we cannot assume, by default,
that the body temperature of reptiles will always be equal to that of the
environment.
Although no case of signicant thermogenesis has ever being reported
for amphibians, there are a few other examples in reptiles. Recently, Casey
etal. (2014) showed that leatherback turtles, Dermochelys coriacea, can keep
their body temperature up to 10°C above water temperature, but this
depends greatly on endogenous heat production, which, in turn, requires
metabolic rates estimated to be approximately 3 times greater than resting
metabolic rates. Tattersall etal. (2004) used infrared thermography to fol-
low heat production in digesting rattlesnakes, C. durissus. Like many other
snake species, C. durissus experience a massive increase in metabolism
while digesting their food and, as a thermodynamic side effect, generate
enough heat to impact signicantly their body temperature (Figure 6.4).
Thus, it means that those interested in the effects of temperature on the
postprandial metabolic response and energetics of snake digestion cannot
assume, as I myself did in the past (Andrade etal. 1997; Toledo etal. 2003;
Gavira and Andrade 2013b), that the body temperature of the experimen-
tal animals will remain constant and equal to ambient. In fact, as early
as 1932, Benedict in his classical book on the physiology of large reptiles
mentioned that “as a result of digestion not only is the snake’s [python]
rectal temperature above the environmental temperature, but likewise its
skin temperature” (Benedict 1932).
If brooding pythons and digesting snakes can be regarded as odd
examples of transient bouts of thermogenic activity, only relevant for
studies focusing on such phenomena, the seasonal thermogenesis by tegu
lizards, S. merianae, cannot. This lizard has recently been shown to use
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144 Amphibian and reptile adaptations to the environment
22.0
23
24
25
26
27
28
29
30
31
25.0
26
27
28
29
30.0
Temperature (ºC)
23.2
24
25
26
(a)
(b)
(c)
26.6
32.0
Figure 6.4 Thermogenesis affects the body temperature of some reptile species
under different circumstances as revealed by infrared imaging technology (see
text for details). (a) Depicts a brooding python, Python bivittatus, coiled around
her recently laid eggs. (Courtesy of R.S.B. Gavira.) (b) A rattlesnake, C. durissus,
approximately 24 h after been fed with a rat meal equaling to 20% of its own body
mass. (Courtesy of G.J. Tattersall; see also Tattersall et al. 2004.) (c) Depicts an
adult tegu lizard, S. merianae, whose body temperature is still higher than ambi-
ent even after the animal has spent the night retreated in its burrow. (Courtesy of
G.J. Tattersall; see Tattersall etal. 2016.)
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145Chapter six: Temperature effects on the metabolism
metabolically derived heat production for a nely tuned body tempera-
ture control that enables them to avoid an excessive nightly body tempera-
ture drop during the reproductive season (Tattersall etal. 2016). Tegus are
heliothermic lizards meaning that they have to dedicate part of their day-
time hours to bask in order to elevate body temperature, a thermoregula-
tory behavior very common for lizards (Huey 1982). Of course, the time an
animal has to invest in basking each morning will depend on the initial
body temperature in which he engages on this behavior. Thus, regulat-
ing nighttime body temperature may represent quite an advantage for
quickly reaching the activity body temperature (around 35–37°C for this
species; Sanders etal. 2015) during daily early morning basking (Huey
and Slatkin 1976). As happens in other ectotherms, tegus are capable of
remarkable reductions in heart rate and peripheral vascular resistance
shortly after they cease their daily activity and, therefore, “save” some of
the heat from 1 day (through the night) to the next (Andrade etal. 2004;
Milsom et al. 2012). However, heat dissipation calculations showed that
changes in conductance alone would not be enough for keeping the night-
time differential observed between the body temperature of tegus and the
temperature of the surroundings (as much as 6°C). Also, tegus were capa-
ble of maintaining elevated body temperature even when they were pre-
vented from basking for many days in a row, further demonstrating the
endogenous origin of the heat affecting body temperature (see Tattersall
etal. 2016; Figure 6.4). Therefore, this case illustrates that an unsuspected
medium-bodied lizard (adult body mass typically varying from 2 to 4 kg)
is able to endogenously elevate its body temperature well above ambi-
ent for an extended period of its life cycle. This response, supposed to
be linked to changes in thermoregulatory compromises associated with
reproduction, has important evolutionary implications (see discussions in
Farmer 2000, 2003; Tattersall etal. 2016). For our immediate interest, the
tegus’ case reiterates the importance of verifying the body temperature of
our experimental subjects during metabolic measurements.
In summary, the similarity between ambient temperature and the
body temperature of amphibians and reptiles should not be indiscrimi-
nately presumed. Since controlling the body temperature of the animals
via the control of ambient temperature may be challenging or even unfea-
sible under certain circumstances, the one “golden rule” here is to monitor,
in as much detail and as accurately as possible, the actual body tempera-
ture of the animals while they are being measured. This can be conve-
niently done with the use temperature dataloggers surgically implanted
or ingested (or forcibly ingested) by the experimental animals. Ideally,
this should be done simultaneously with the metabolic measurements.
If this approach is not possible or recommended under a given protocol,
at least the expected body temperature of the animals under that specic
experimental setup should be veried. Both the actual measured body
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146 Amphibian and reptile adaptations to the environment
temperature and the environmental temperature should be reported in
any paper dealing with the metabolic effects of temperature.
Concluding remarks
Temperature is reputed as the single physical factor most inuential to any
living organism and, as such, temperature effects on an enormous diver-
sity of animal functions have kept generations of biologists busy through-
out history. In the last few decades, for the sad reason of human-induced
changes in the climate of our planet (IPCC 2014), the study of temperature
effects over particular biological systems, and whole ecosystems as well,
has gained urgent relevance. In this context, theoretical and empirical
efforts have been summoned under a conservationist multidisciplinary
approach in an attempt to understand and predict potential problems
and outcomes related to animal function under a rapidly changing world
(e.g., Navas and Otani 2007; Sinervo etal. 2010; Huey etal. 2012; Seebacher
etal. 2014; Bozinovic and Pörtner 2015; Deutsch etal. 2015). While many
of these problems and outcomes are yet to be determined, studies focus-
ing on the metabolic correlates of temperature on animals, particularly on
ectotherms, can provide an integrative denominator irrefutably relevant
for animal life, which is energy ux. In this sense, the central goal of the
present chapter is to promote discussion on how our measurements on
that front can gain more accuracy and relevance.
The cases discussed in this chapter reiterate the importance of incor-
porating thermal biology onto metabolic determinations for the particular
case of amphibians and reptiles and, more generally, to other ectothermic
organisms. The potential caveats resulting from the nonappreciation of
this issue were illustrated by the mismatch between the choice of experi-
mental temperatures and the thermal biology in tegu lizards. The rel-
evance of considering other aspects of the thermal environment, besides
the averaged mean temperature, was approached by discussing the
effects of thermal regime on the digestion of snakes. In this context, there
is a growing perception that the potential consequences of temperature
variability on the stress and performance of organisms that normally
experience uctuating temperature regimes can only be poorly predicted
from the extrapolation of studies carried out under thermal conditions
dissociated from the thermal biology of the studied organisms (Ketola
etal. 2012; Niehaus etal. 2012; Ketola and Saarinen 2015; Kingsolver etal.
2015; Ma etal. 2015; Vázquez etal. 2015). Finally, by showing that the body
temperature of amphibians and reptiles can be considerably different
from the ambient, I hope to have fostered a more rigorous control and/
or monitoring of body temperature during the execution of metabolic
measurements and the incorporation of such information in the resulting
publications.
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147Chapter six: Temperature effects on the metabolism
Acknowledgments
I am in debt to my colleagues and students for sharing my mistakes but,
most importantly, for always being open to questioning and helping to
nd ways to get around them. Our many discussions, often happening in
front of an experimental setup in the lab, helped mold the views expressed
in this chapter. Rodrigo S. B. Gavira and Ailton Fabrício-Neto kindly per-
mitted the use of published and unpublished data and helped with the
gures. Glenn J. Tattersall and Rodrigo S. B. Gavira provided valuable
and insightful comments on a previous version of the chapter. During
the writing of this chapter, I was supported by the National Council for
Scientic and Technological Development (CNPq, grant 302045/2012-0)
and by the São Paulo Research Foundation (FAPESP, grant 2013/04190-9).
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... Allostatic mediation is critical to optimizing individual fitness in the environment (Ricklefs & Wikelski, 2002), but the efficacy at which allostasis operates may hinge upon the environmental conditions themselves (Huey & Stevenson, 1979;Huey, 1982). For ectothermic reptiles reliant on thermal heat exchange, environmental temperature can govern determinants of survival (e.g., locomotor performance, immunocompetence; Angilletta, 2009;Angilletta et al., 2002;Butler et al., 2013) seemingly through changes in metabolic activity (de Andrade, 2016). Considering environmental temperature varies over space (e.g., microhabitats) and time (e.g., days, seasons), frequent shifts in body temperature (T body ) are liable to occur in reptiles (Blouin-Demers & Weatherhead, 2001;Huey & Kingsolver, 1989;Huey & Pianka, 1977;Peterson, 1987). ...
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