Content uploaded by Denis V Andrade
Author content
All content in this area was uploaded by Denis V Andrade on Jan 11, 2018
Content may be subject to copyright.
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 identiable 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 etal. 1982; Nagy 1983; Pough etal. 1992; Nagy etal. 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 quantied 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 sufce 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 inuenced 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 inuence on the metabolic
rate of animals, temperature can easily be identied as the one whose
effects have been largely investigated. This is justiable, as temperature
is widely recognized as the single physical parameter with the most pro-
found impacts on animal function (Huey 1982; Angilletta 2009; Tattersall
etal. 2012). In the case of ectothermic animals, including amphibians and
reptiles, the inuence 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 etal. 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
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
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 etal. 1992; Abe 1995; Carvalho etal.
2010; Gunderson and Leal 2015; Sanders etal. 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 etal.
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 quantied 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 etal. 1992; Rome etal. 1992; Hillman etal. 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 etal. 1992; White etal. 2006; Halsey
etal. 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 etal. 2001), including those
sustaining changes in activity levels (see Halsey etal. 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
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
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 etal. 1992;
Rome etal. 1992; Hillman etal. 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 etal. 2015 for a similar approach
on another subject). Thus, goals of this chapter can be dened 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 behavioraladjustments
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
133Chapter six: Temperature effects on the metabolism
(Huey and Pianka 1977; Seebacher et al. 2005; Pough et al. 2015).
Thermoregulatory costs and benets 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 specic 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 etal.
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 etal. 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 etal. 1972; Seebacher
etal. 1999; Bostrom etal. 2010). Leatherbacks are, indeed, able to keep their
body temperature well elevated above sea water temperature (Paladino
etal. 1990; Casey etal. 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 etal. 2009). Exceptions exist
(Shoemaker et al. 1987, 1989; Tattersall etal. 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
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
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 signicant 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 etal. 2004; Milsom etal. 2012; Sanders etal. 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-
cic 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 etal.
2004; Sanders etal. 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 etal. 2004; Sanders etal. 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 etal. 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
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
135Chapter six: Temperature effects on the metabolism
and Abe 1999; Andrade etal. 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
briey 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 reect 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 etal., 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 etal. 2015).
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
136 Amphibian and reptile adaptations to the environment
at temperatures that the animal never experiences or experiences only
briey 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 etal. 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 etal. 1992; Rome etal. 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 etal. 2015)
and for experimental protocols demanding longer measurement dura-
tions, such as many days. Constant temperature measurements are cer-
tainly adequate to answer specic 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
etal. 2015; Stahlschmidt etal. 2015).
Daily thermal cycles are known to inuence 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
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
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 reects 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).
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
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 etal., 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 etal. (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 etal. 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 inuence 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 etal. 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 etal. 2012; Basson
and Clusella-Trullas 2015), with important interactive consequences for
growth, metabolism, osmoregulation (Davies et al. 2015; Stahlschmidt
etal. 2015), and, potentially, to the evolution of physiological adaptation
and conservation (see Sunday et al. 2014; Agustín et al. 2015; Buckley
etal. 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 etal. 2012; Caillon etal. 2014; Manenti et al.2014;
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
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 etal. 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 etal. 2015; Turriago etal. 2015). For example, Horne
etal. (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 inuence 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
inuenced 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 etal. 2012; Kingsolver etal. 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 etal. 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 inuences 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 specic 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,
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
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 etal. 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 reect 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
inuenced 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 etal., 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). A3 kg tegu lizard,
S. merianae, can withstand signicant temperature differentials up to
12 h due to its larger body mass and remarkable vasomotor response
(Sanders etal. 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
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
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 time0. 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.)
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
142 Amphibian and reptile adaptations to the environment
temperature experienced by the animals, and this effect is magnied
by larger body sizes (see also McNab and Auffenberg 1976; Auffenberg
1981; Tracy 1982; Spotila etal. 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 etal. 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 etal. 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 etal. 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 inuence 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
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
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 conrmed and expanded his pioneering
observations (see Benedict etal. 1932; Hutchison etal. 1966; Brashears and
DeNardo 2013). Since then, the case of brooding pythons incubating their
eggs by means of metabolically derived heat (see Figure6.4) 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 signicant thermogenesis has ever being reported
for amphibians, there are a few other examples in reptiles. Recently, Casey
etal. (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 etal. (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 signicantly 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 etal. 1997; Toledo etal. 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
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
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 etal. 2016.)
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
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 etal. 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 etal. 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 etal. 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
etal. 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 etal. 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 specic
experimental setup should be veried. Both the actual measured body
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
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 inuential 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 etal. 2010; Huey etal. 2012; Seebacher
etal. 2014; Bozinovic and Pörtner 2015; Deutsch etal. 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
etal. 2012; Niehaus etal. 2012; Ketola and Saarinen 2015; Kingsolver etal.
2015; Ma etal. 2015; Vázquez etal. 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.
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
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
Scientic and Technological Development (CNPq, grant 302045/2012-0)
and by the São Paulo Research Foundation (FAPESP, grant 2013/04190-9).
References
Abe, A.S. 1983. Observations on dormancy in tegu lizard, Tupinambis teguixin
(Reptilia, Teiidae). Naturalia 8:135–139.
Abe, A.S. 1995. Estivation in South American amphibians and reptiles. Brazilian
Journal of Medical and Biological Research 28:1241–1247.
Agustín, C., Pavão, R., Moreira, C.N., Pinto, A.C.B.C.F., Navas, C.A., and M.T.
Rodrigues. 2015. Interaction of morphology, therma l physiology and burrow-
ing performance during the evolution of fossoriality in Gymnophthalmini
lizards. Functional Ecology 29:515–521.
Andrade, D.V. and A.S. Abe. 1999. Gas exchange and ventilation during dormancy
in the tegu lizard, Tupinambis merianae. The Journal of Experimental Biology
202:3677–3685.
Andrade, D.V., Cruz-Neto, A.P., and A.S. Abe. 1997. Meal size and specic
dynamic action in the rattlesnake, Crotalus durissus (Serpentes, Viperidae).
Herpetologica 53:485–493.
Andrade, D.V., Milsom, W.K., Brito, S.P., Toledo, L.F., Wang, T., and A.S. Abe. 2008b.
Seasonal changes in daily metabolic patterns of tegu lizards (Tupinambis
merianae) placed in the cold (17°C) and dark. Physiological and Biochemical
Zoology 81:165–175.
Andrade, D.V., Sanders, C., Milsom, W.K., and A.S. Abe. 2004. Overwintering in
tegu Lizards. In Barnes, B.M. and H.V. Carey (eds), Life in the Cold: Evolution,
Mechanisms, Adaptation, and Application. Twelfth International Hibernation
Symposium. Institute of Artic Biology, University of Alaska: Fairbanks,
Alaska, pp. 13–22.
Andrade, D.V., Toledo, L.F., Brito, S.P., Milsom, W.K, and A.S. Abe. 2008a. Effects of
season, temperature, and body mass on the standard metabolic rate of tegu
lizards (Tupinambis merianae). Physiological and Biochemical Zoology 81:158 –164.
Andrews, R.M. and F.H. Pough. 1985. Metabolism of squamate reptiles: Allometric
and ecological relationships. Physiological Zoology 58(2):214–231.
Angilletta, M.J. Jr., Niewiarowski, P.H., and C.A. Navas. 2002. The evolution of
thermal physiology in ectotherms. Journal of Thermal Biology 27:249–268.
Angilletta, M.J. 2009. Thermal Adaptation: A Theoretical and Empirical Synthesis.
Oxford University Press: New York.
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
148 Amphibian and reptile adaptations to the environment
Aubret, F. and R. Shine. 2009. Thermal plasticity in young snakes: How will cli-
mate change affect the thermoregulatory tactics of ectotherms? Journal of
Experimental Biology 213:242–248.
Auffenberg, W. 1981. The Behavioral Ecology of the Komodo Monitor. University
Presses of Florida: Gainesville, Florida.
Avery, R.A. 1982. Field studies of body temperature and thermoregulation.
Temperature, physiology, and the ecology of reptiles. In Gans, C. and F.H.
Pough (eds), Biology of the Reptilia, Vol. 12. Academic Press: New York, pp.
93–166.
Bakken, G.S. and M.J. Angilletta. 2014. How to avoid errors when quantifying
thermal environments. Functional Ecology 28:96 –10 7.
Bartelt, P.E. and C.R. Peterson. 2005. Physically modeling operative temperatures
and evaporation rates in amphibians. Journal of Thermal Biology 30(2):93–102.
Bartholomew, G.A. 1982. Physiological control of body temperature. In Gans,
C. and Pough, F.H. (eds), Biology of the Reptilia, Vol. 12, Physiology C.
Physiological Ecology. Academic Press: London, pp. 167–211.
Basson, C.H. and S. Clusella-Trullas. 2015. The behavior-physiology nexus:
Behavioral and physiological compensation are relied on to different extents
between seasons. Physiological and Biochemical Zoology, 88(4):384–394.
Benedict, F.G. 1932. The Physiology of Large Reptiles with Special Reference to the
Heat Production of Snakes, Tortoises, Lizards, and Alligators. Carnegie Institute
Publications: Washington, DC.
Benedict, F.G., Fox, E.L., and V. Coropatchinsky. 1932. The incubating python: A
temperature study. Proceedings of the National Academy of Sciences of the United
States of America 18(2):209–212.
Bennett, A.F. 1978. Activity metabolism of the lower vertebrates. Annual Review of
Physiology 40:447– 469.
Bennett, A.F. 1980. The metabolic foundations of vertebrate behavior. BioScience
30(7):452–456.
Bennett, A.F. 1982. The energetics of reptilian activity. In Gans, C. and F.H. Pough
(eds), Biology of the Reptilia, Vol. 13. Physiology D. Physiological Ecology.
Academic Press: New York, pp. 155–199.
Bennett, A.F. 1994. Exercise performance in reptiles. Advances in Veterinary Sciences
and Comparative Medicine 38B:113–138.
Bennett, A.F. and P. Licht. 1972. Anaerobic metabolism during activity in lizards.
Journal of Comparative Physiology 81:277–288.
Bennett, A.F. and P. Licht. 1974. Anaerobic metabolism during activity in amphib-
ians. Comparative and Biochemistry Physiology 48A:319–327.
Bennett, A.F. and P.H. Harvey. 1987. Active and resting metabolism in birds:
Allometry, phylogeny and ecology. Journal of Zoology 213:327–363.
Bennett, A.F. and W.R. Dawson. 1976. Metabolism. In Gans, C. and W.R. Dawson
(eds), Biology of the Reptilia, Vol. 5. Physiology A. Academic Press: New York,
pp. 127–223.
Bostrom, B.L., Jones, T.T., Hastings, M., and D.R. Jones. 2010. Behaviour and physi-
ology: The thermal strategy of leatherback turtles. PLoS One 5(11):e13925.
Bozinovic, F. and H.O. Pörtner, 2015. Physiological ecology meets climate change.
Ecology and Evolution 5(5):1025–1030.
Brashears, J.A. and D.F. DeNardo. 2013. Revisiting python thermogenesis:
Brooding Burmese pythons (Python bivittatus) cue on body, not clutch, tem-
perature. Journal of Herpetology 47(3):440–444.
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
149Chapter six: Temperature effects on the metabolism
Brattstrom, B.H. 1963. Preliminary review of the thermal requirements of amphib-
ians. Ecology 44:238–255.
Brattstrom, B.H. 1965. Body temperature of reptiles. The American Midland
Naturalist 73(2):376–422.
Buckley, L.B., Ehrenberger, J.C., and M.J. Angilletta. 2015. Thermoregulatory
behavior limits local adaptation of thermal niches and confers sensitivity to
climate change. Functional Ecology 29:1038–1047.
Caillon, R., Suppo, C., Casas, J., Woods, H.A., and S. Pincebourde. 2014. Warming
decreases thermal heterogeneity of leaf surfaces: Implications for behav-
ioural thermoregulation by arthropods. Functional Ecology 28:1449–1458.
Caldwell, A.J., While, G.M., Beeon, N.J., and E. Wapsta. 2015. Potential for thermal
tolerance to mediate climate change effects on three members of a cool tem-
perate lizard genus, Niveoscincus. Journal of Thermal Biology 52:14–23.
Carey, C. 2005. How physiological methods and concepts can be useful in conser-
vation biology. Integrative and Comparative Biology 45(1):4–11.
Carvalho, J.E., Navas C.A., and I.C. Pereira. 2010. Energy and water in aestivating
amphibians. In Navas, C.A. and J.E. Carvalho (eds), Aestivation: Molecular
and Physiological Aspects. Springer-Verlag: Berlin, pp. 141–169.
Casey, J.P., James, M.C., and A.S. Williard. 2014. Behavioral and metabolic contri-
butions to thermoregulation in freely swimming leatherback turtles at high
latitudes. The Journal of Experimental Biology 217:2331–2337.
Congdon, J.D., Dnhamn, A.E., and D.W. Tinkle. 1982. Energy budgets and life
history of reptiles. In Gans, C. and F.H. Pough (eds), Biology of the Reptilia,
Volume 13. Physiology D. Physiological Ecology. Academic Press: New York,
pp. 233–271.
Dabruzzi, T.F., Sutton, M.A., and W.A. Bennett. 2012. Metabolic thermal sensitiv-
ity optimizes sea krait amphibious physiology. Herpetologica 68(2):218–225.
Davies, S.J., McGeoch, M.A., and S. Clusella-Trullas. 2015. Plasticity of thermal
tolerance and metabolism but not water loss in an invasive reed frog.
Comparative Biochemistry Physiology 189:11–20.
Deutsch, C., Ferrel, A., Seibel, B., Pörtner, H.O., and R.B. Huey. 2015. Climate change
tightens a metabolic constraint on marine habitats. Science 348:1132–1135.
di Prampero, P.E. 1985. Metabolic and circulatory limitations to
V
O2max at the
whole animal level. Journal of Experimental Biology 115:319–331.
Dowd, W.W., King, F.A., and M.W. Denny. 2015. Thermal variation, thermal
extremes and the physiological performance of individuals. Journal of
Experimental Biology 218:1956–1967.
Else, P.L. and A.J. Hulbert. 1981. Comparison of the “mammal machine” and the
“reptile machi ne”: Energy production. American Journal of Physiology 240:R3–R9.
Else, P.L. and A.J. Hulbert. 1985. An allometric comparison of the mitochondria
of mammalian and reptilian tissues: The implications for the evolution of
endothermy. Journal of Comparative Physiology 156:3–11.
Farmer, C.G. 2000. Parental care: The key to understanding endothermy and
other convergent features in birds and mammals. American Naturalist
155(3):326 –334.
Farmer, C.G. 2003. Reproduction: The adaptive signicance of endothermy.
American Naturalist 162(6):826–840.
Feder M.E. and S.J. Arnold. 1982. Anaerobic metabolism and behavior during
predatory encounters between snakes (Thamnophis elegans) and salamanders
(Plethodon jordani). Oecologia 53:93–97.
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
150 Amphibian and reptile adaptations to the environment
Fraser, S. and G.C. Grigg. 1984. Control of thermal conductance is insignicant to
thermoregulation in small reptiles. Physiological Zoology 57(4):392–400.
Fray, W., Ackman, R.G., and N. Mrosovsky. 1972. Body temperature of Dermochelys
coriacea: Warm turtle from cold water. Science 177:791–793.
Gates, D.M. 1980. Biophysical Ecology. Dover Publications, Inc.: Mineola, New York.
Gatten, R.E., Miller, K., and R.J. Full. 1992. Energetics at rest and during locomo-
tion. In Feder, M.E. and W.W. Burggreen (eds), Environmental Physiology of
the Amphibians. The University of Chicago Press: Chicago, USA, pp. 314–377.
Gavira, R.S.B. and D.V. Andrade. 2013a. Temperature and thermal regime effects
on the specic dynamic action of Bothrops alternatus (Serpentes, Viperidae).
Amphibia-Reptilia 34:483–491.
Gavira, R.S.B. and D.V. Andrade. 2013b. Meal size effects on the postprandial
metabolic response of Bothrops alternatus (Serpentes: Viperidae). Zoologia
30:291–295.
Gillooly, J.F., Brown, J.H., West, G.B., Savage, V.M., and E.L. Charnov. 2001. Effects
of size and temperature on metabolic rate. Science 293:2248–2251.
Gleeson, T.T. 1991. Patterns of metabolic recovery from exercise in amphibians
and reptiles. Journal of Experimental Biology 16 0 :187– 2 0 7.
Gregory, P.T. 1982. Reptilian hibernation. In Gans, C. and F.H. Pough (eds), Biology
of the Reptilia, Vol. 13, Physiology D. Physiological Ecology. Academic Press:
New York, pp. 53–154.
Gunderson, A.R. and M. Leal. 2015. Patterns of thermal constraint on ectotherm
ac tivit y. American Naturalist 185(5): 653–664.
Halsey, L.G., Mattews, P.G.D., Rezende, E.L., Chauvaud, L., and A.A. Robson. 2015.
The interactions between temperature and activity levels in driving meta-
bolic rate: Theory, with empirical validation from constrasting ectotherms.
Oecologia 177:1117–1129.
Hedrick, M.S., Hancock, T.V., and S.S. Hillman. 2015. Metabolism at the max: How
vertebrate organisms respond to physical activity. Comprehensive Physiology
5:1677–1703.
Hillman, S.S., Withers, P.C., Drewes, R.C., and S.D. Hillyard. 2009. Ecological and
Environmental Physiology of Amphibians. Oxford University Press: Oxford,
UK.
Horne, C.R., Fuller, W.J., Godley, B.J., Rhodes, K.A., Snape, R., Stokes, K.L., and
A.C. Broderick. 2014. The effects of thermal variance on the phenotype of
marine turtle offspring. Physiological and Biochemical Zoology 87(6):796–804.
Huey, R.B. 1982. Temperature, physiology, and the ecology of reptiles. In Gans,
C. and F.H. Pough (eds), Biology of the Reptilia, Vol. 12. Academic Press: New
York, pp. 25–74.
Huey, R.B. and E.R. Pianka. 1977. Seasonal variation in thermoregulatory behavior
and body temperature of diurnal Kalahari lizards. Ecology 58:1066–1075.
Huey, R.B. and M. Slatkin. 1976. Cost and benets of lizard thermoregulation.
Quarterly Review of Biology 51(3):363–384.
Huey, R.B. and R.D. Stevenson. 1979. Integrating thermal physiology and ecology
of ectotherms: A discussion of approaches. American Zoologist 19:357–366.
Huey, R.B., Kearney, M.R., Krockenberger, A., Holtum, J.A.M., Jess, M., and S.E.
Williams. 2012. Predicting organismal vulnerability to climate warming:
Roles of behaviour, physiology and adaptation. Philadelphia Transactions of
the Royal Society B 367:1665 –1679.
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
151Chapter six: Temperature effects on the metabolism
Hutchison, V.H. and R.K. Dupré. 1992. Thermoregulation. In Feder, M.E. and W.W.
Burggreen (eds), Environmental Physiology of the Amphibians. The University
of Chicago Press: Chicago, IL, pp. 206–249.
Hutchison, V.H., Dowling, H.G., and A. Vinegar. 1966. Thermoregulation
in a brooding female Indian python, Python molurus bivittatus. Science
151:694–696.
IPCC. 2014. In Field, C.B., Barros, V.R., Dokken, D.J., Mach, K.J., Mastrandrea, M.D.,
Bilir, T.E., Chatterjee, M. etal. (eds), Climate Change 2014: Impacts, Adaptation,
and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working
Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate
Change. Cambridge University Press: Cambridge, UK, New York, p. 1132.
Kearn, P., Cramp, R.L., and C.E. Franklin. 2015. Physiological responses of ecto-
therms to daily temperature variation. Journal of Experimental Biology
218:3068–3076.
Kearney, M. and W.P. Porter. 2004. Mapping the fundamental niche: Physiology,
climate and the distribution of a nocturnal lizard. Ecology 85(11):3119–3131.
Kearney, M., Shine, R., and W.P. Porter. 2009. The potential for behavioral ther-
moregulation to buffer “cold-blooded” animals against climate warming.
Proceedings of the National Academy of Sciences 106:3835–3840.
Ketola, T. and K. Saarinen. 2015. Experimental evolution in uctuating environ-
ments: Tolerance measurements at constant temperatures incorrectly pre-
dict the ability to tolerate uctuating temperatures. Journal of Evolutionary
Biology 28:800–806.
Ketola, T., Kellerman, V., Kristensen, T.N., and V. Loeschcke. 2012. Constant,
cycling, hot and cold thermal environments: Strong effects on mean viabil-
ity but not on genetic estimates. Journal of Evolutionary Biology 25:1209–1215.
Kingsolver, J.G., Higgins J.K., and K.E. Augustine. 2015. Fluctuating temperatures
and ectotherm growth: Distinguishing non-linear and time-dependent
effects. Journal of Experimental Biology 218:2218–2225.
Kleiber, K. 1961. The Fire of Life: An Introduction to Animal Energetics. Wiley: New York.
Kleiber, M. 1947. Body size and metabolic rate. Physiological Review 27:511–541.
Levy, O., Buckley, L.B., Keitt, T.H., Smith, C.D., Boateng, K.O., Kumar, D.S., and M.J.
Angilletta. 2015. Resolving the life cycle alters expected impacts of climate
change. Proceedings of the Royal Society B 282:201508 3 7.
Lighton, J.R.B. 2008. Measuring Metabolic Rates: A Manual for Scientists. Oxford
University Press: Oxford, UK.
Lorioux, S., DeNardo, D.F., Gorelick, R., and O. Lourdais. 2012. Maternal inu-
ences on early development: Preferred temperature prior to oviposition has-
tens embryogenesis and enhances offspring traits in the Children’s python,
Antaresia childreni. Journal of Experimental Biology 215:1346–1353.
Lowell, B.B. and B.M. Spiegelman. 2000. Towards a molecular understanding of
adaptive thermogenesis. Nature 404:652–660.
Ma, G., Hoffman, A.A., and C.S. Ma. 2015. Daily temperature extremes play an
important role in predicting thermal effects. Journal of Experimental Biology
218:2289–2296.
Manenti, T., Sørensen, J.G., Moghadam, N.N., and V. Loes chcke. 2014. Pred ictability
rather than amplitude of temperature uctuations determines stress resis-
tance in a natural population of Drosophila simulans. Journal of Evolutionary
Biology 27:2113–2122.
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
152 Amphibian and reptile adaptations to the environment
McNab, B.K. 2002. The Physiological Ecology of Vertebrates: A View from Energetics.
Comstock/Cornell University Press: Ithaca, New York.
McNab, B.K. and W. Auffenberg. 1976. Temperature regulation of the komodo
dragon, Varanus komodoensis. Comparative and Biochemistry Physiology 55A:
345–350.
Méndez-Narváez, J., Flechas, S.V., and A. Amézquita. 2015. Foam nests provide
context-dependent thermal insulation to embryos of three leptodactylid
frogs. Physiological and Biochemical Zoology 88(3):246–253.
Milsom, W.K., Sanders, C., Leite, C.A.C., Abe, A.S., Andrade, D.V., and G.J.
Tattersall. 2012. Seasonal changes in thermoregulatory strategies of tegu
lizards. In Ruf, T., Bieber, C., Arnold, W., and E. Millesi (eds), Living in a
Seasonal World: Thermoregulatory and Metabolic Adaptations. Springer-Verlag:
Berlin, pp. 317–324.
Nagy, K.A. 1983. Ecological energetics. In Huey, R.B., Pianka, E.R., and T.W.
Schoener (eds), Lizard Ecology. Harvard University Press: Cambridge, pp.
24–54.
Nagy, K.A., Girard, I.A., and T.K. Brown. 1999. Energetics of free-ranging mam-
mals, reptiles, and birds. Annual Review of Nutrition 19:247–277.
Navas, C.A. and L. Otani. 2007. Physiology, environmental change, and anuran
conservation. Phyllomedusa 6(2):83 –103.
Newman, A.E., Edmunds, N.B., Ferraro, S., Heffell, Q., Merrit, G.M., Pakkala, J.J.,
Schilling, C.R., and S. Schorno. 2015. Using ecology to inform physiology
studies: Implications of high population density in the laboratory. American
Journal of Regulatory and Integrative Comparative Physiology 308:R449–R454.
Nichelmann, M. and B. Tzschentke. 1995. Thermoneutrality: Traditions, prob-
lems, alternatives. In Nagasaka, T. and A.S. Milton (eds), Body Temperature
and Metabolism. IPEC: Tokyo, pp. 77–82.
Niehaus, A.C., Angilletta, M.J., Sears, M.W., Franklin, C.E., and R.S. Wilson. 2012.
Predicting the physiological performance of ectotherms in uctuating ther-
mal environments. Journal of Experimental Biology 215:694–701.
Paladino, F.V., O’Connor, M.P., and J.R. Spotila. 1990. Metabolism of leatherback
turtles, gigantothermy, and thermoregulation of dinosaurs. Nature 344:
858–860.
Pinder, A.W., Storey, K.B., and G.R. Ultsch. 1992. Estivation and hibernation.
In Feder, M.E. and W.W. Burggreen (eds), Environmental Physiology of the
Amphibians. The University of Chicago Press: Chicago, IL, pp. 250–274.
Pough, F.H. 1983. Amphibians and reptiles as low-energy systems. In Aspey, W.P.
and S.I. Lustick (eds), Behavioral Energetics: The Cost of Survival in Vertebrates.
Ohio State University Press: Columbus, Ohio, pp. 141–188.
Pough, F.H., Magnusson, W.E., Ryan, M.J., Wells, K.D., and T.L. Taigen. 1992.
Behavioral energetic s. In Feder, M.E. and W.W. Burggreen (eds), Environmental
Physiology of the Amphibians. The University of Chicago Press: Chicago, IL,
pp. 395–436.
Pough, F.H., Andrews, R.M., Crump, M.L., Savitzky, A.H., Wells, K.D., and M.C.
Brandley. 2015. Herpetology. 4th Ed. Sinauer: Sunderland, USA.
Rome, L.C., Stevens, E.D., and H.B. John-Alder. 1992. The inuence of temperature
and thermal acclimation on physiological function. In Feder, M.E. and W.W.
Burggreen (eds), Environmental Physiology of the Amphibians. The University
of Chicago Press: Chicago, IL, pp. 183–205.
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
153Chapter six: Temperature effects on the metabolism
Ruben, J.A. 1976. Aerobic and anaerobic metabolism during activity in snakes.
Journal of Comparative Physiology 109(2) :14 7–15 7.
Sanders, C.E., Tattersall, G.J., Reichert, M., Andrade, D.V., Abe, A.S., and W.K.
Milsom. 2015. Daily and annual cycles in thermoregulatory behavior and
cardio-respiratory physiology of black and white tegu lizards. Journal of
Comparative Physiology 185(8):905–915.
Schmidt-Nielsen, K. 1984. Scaling: Why Is Animal Size so Important? Cambridge
University Press: Cambridge.
Sears, M.W. and M.J. Angilletta. 2015. Costs and benets of thermoregulation
revisited: Both the heterogeneity and spatial structure of temperature drive
energetic costs. American Naturalist 185(4):E94–E102.
Seebacher, F. and R. Shine. 2004. Evaluating thermoregulation in reptiles: The fal-
lacy of the inappropriate applied method. Physiological Biochemical Zoology
77(4):688–695.
Seebacher, F., Grigg, G.C., and L.A. Beard. 1999. Crocodiles as dinosaurs:
Behavioural thermoregulation in very large ectotherms leads to high and
stable body temperatures. Journal of Experimental Biology 202:77–86.
Seebacher, F., White, C.R., and C.E. Franklin. 2005. Physiological mechanisms
of thermoregulation in reptiles: A review. Journal of Comparative Physiology
175:533–541.
Seebacher, F., White, C.R., and C.E. Franklin. 2014. Physiological plasticity
increases resilience of ectothermic animals to climate change. Nature Climate
Change 5:61–66.
Shoemaker, V.H., Baker, M.A., and J.P. Loveridge. 1989. Effect of water balance
on thermoregulation in waterproof frogs (Chiromantis and Phyllomedusa).
Physiological Zoology 62:133–146.
Shoemaker, V.H., McClanahan, L.L., Withers, P.C., Hillman, S.S., and R.C.
Drewes. 1987. Thermoregulatory response to heat in the waterproof frogs
Phyllomedusa and Chiromantis. Physiological Zoology 60:365–372.
Sinervo, B., Méndez-de-la-Cruz, F., Miles, D.B., Heulin, B., Bastiaans, E., Cruz,
M.V., Lara-Resendiz, R. et al. 2010. Erosion of lizard diversity by climate
change and altered thermal niches. Science 328:1496–1501.
Spotila, J.R., O’Connor, P.O., and G.S. Bakken. 1992. Biophysics of heat and mass
transfer. In Feder, M.E. and W.W. Burggreen (eds), Environmental Physiology
of the Amphibians. The University of Chicago Press: Chicago, IL, pp. 55–80.
Stahlschmidt, Z.R., Jodrey, A.D., and R.L. Luoma. 2015. Consequences of complex
environments: Temperature and energy intake interact to inuence growth
and metabolic rate. Comparative Biochemistry Physiology 18 7:1–7.
Suarez, R.K. 2012. Energy metabolism. Comprehensive Physiology 2:2527–2540.
Sunday, J.M., Bates, A.E., Kearney, M.R., Colwell, R.K., Dulvy, N.K., Longino, J.T.,
and R.B. Huey. 2014. Thermal-safety margins and the necessity of thermo-
regulatory behavior across latitude and elevation. Proceedings of the National
Academy of Sciences 111(15):5610–5615.
Tattersall, G.J., Eterovick, P.C., and D.V. Andrade. 2006. Tribute to R.G. Boutilier:
Skin colour and body temperature changes in basking Bokermannohyla alva-
rengai (Bokermann, 1956). Journal of Experimental Biology 209:1185–1196.
Tattersall, G.J., Leite, C.A.C., Sanders, C., Cadena, V., Andrade, D.V., Abe, A.S.,
and W.K. Milsom. 2016. Seasonal reproductive endothermy in tegu lizards.
Science Advances 2(1):e1500951.
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016
154 Amphibian and reptile adaptations to the environment
Tattersall, G.J., Milsom, W.K., Abe, A.S., Brito, S.P., and D.V. Andrade. 2004. The
thermogenesis of digestion in rattlesnakes. Journal of Experimental Biology
207:579–585.
Tattersall, G.J., Siclair, B.J., Withers, P.C., Fields, P.A., Seebacher, F., Cooper, C.E., and
S.K. Maloney. 2012. Coping with thermal challenges: Physiological adapta-
tions to environmental temperatures. Comprehensive Physiology 2:2151–2202.
Toledo, L.F., Abe, A.S., and D.V. Andrade. 2003. Temperature and meal mass
effects on the post-prandial metabolism and energetics in a boid snake.
Physiological Zoology 76:240–246.
Tracy, C.R. 1975. Water and energy relations of amphibians: Insights from
mechanistic modelling. In Gates, D.M. and R. Schmerl (eds), Perspectives in
Biophysical Ecology. Springer-Verlag: Berlin, pp. 325–346.
Tracy, C.R. 1976. A model of the dynamic exchanges of water and energy
between a terrestrial amphibian and its environment. Ecological Monographs
46(3):293–326.
Tracy, C.R. 1982. Biophysical modeling in reptilian physiology and ecology. In
Gans, C. and F.H. Pough (eds), Biology of the Reptilia, Vol. 12. Academic Press:
New York, pp. 275–321.
Turriago, J.L., Parra, C.A., and M.H. Bernal. 2015. Upper thermal tolerance in
anuran embryos and tadpoles at constant and variable peak temperatures.
Canadian Journal of Zoology 93:267–272.
Underwood, H. 1984. Endogenous rhythms. In Gans, C. and D. Crews (eds), Biology
of the Reptilia, Vol. 18, Physiology E. Academic Press: New York, pp. 229–297.
Vázquez, D.P., Gianoli, E., Morris, W.F., and F. Bozinovic. 2015. Ecological and
evolutionary impacts of changing climatic variability. Biological Reviews doi:
10.1111/brv.12216.
White, C.R., Phillips, N.F., and R.S. Seymour. 2006. The scaling and temperature
dependence of vertebrate metabolism. Biological Letters 2(1):125–127.
Wikelski, M. and S.J. Cooke. 2006. Conservation physiology. Trends in Ecology and
Evolution 21(1):38–46.
© 2016 by Taylor & Francis Group, LLC
Downloaded by [University of California, San Diego (CDL)] at 13:58 17 July 2016