The effect of heat transfer mode on heart rate responses and hysteresis during heating and cooling in the estuarine crocodile Crocodylus porosus
1 Department of Zoology and Entomology, University of Queensland, St Lucia,
Qld 4072, Australia
2 School of Biological Sciences A08, University of Sydney, Sydney, NSW 2006,
Australia
* Author for correspondence (e-mail: fseebach{at}bio.usyd.edu.au)
Accepted 10 January 2003
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Summary |
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Key words: thermoregulation, reptiles, heart rate, hysteresis, heat transfer, body temperature, crocodiles, Crocodylus porosus
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Introduction |
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Rapid changes in heart rate during the initial stages of heating and
cooling in the heliothermic lizard Pogona barbata (instantaneous
changes of 10 beats min1) indicate a reflex-like response
that is at least partly mediated by the autonomic nervous system
(Seebacher and Franklin,
2001). This rapid response augmented the heart rate hysteresis
seen during heating and cooling in P. barbata and appears to be an
important component of the physiological control of body temperature in this
lizard (Seebacher and Franklin,
2001
). A reflex-like response of heart rate also occurred after
local application of radiant heat to the dorsal surface of the freshwater
crocodile Crocodylus johnstoni, although this was recorded in one
animal only (Grigg and Alchin,
1976
).
During thermoregulation, crocodiles utilise microhabitats that encompass
both terrestrial and aquatic environments and a variety of behavioural
postures (Seebacher and Grigg,
1997; Seebacher,
1999
; Grigg and Seebacher,
2001
). Regulation of body temperature can be achieved by basking
on land, shuttling between land and water, and changing postures while in the
water so that varying proportions of surface area are exposed to the sun
(Seebacher, 1999
). The
amphibious lifestyle of crocodiles has a significant influence on rates of
heat gain and loss and thermoregulation due to the markedly different thermal
characteristics of water and air. It is possible, therefore, that cardiac
responses of crocodiles during heating and cooling are different for different
heat transfer mechanisms experienced by the animals. Additionally, it has been
suggested that thermoregulation in reptiles is facilitated by the
light-sensitive pineal gland and parietal eye
(Tosini and Menaker, 1996
;
Tosini, 1997
;
Cagnacci et al., 1997
), which
may indicate that responses to basking (i.e. exposure to high light intensity)
may be fundamentally different to heating or cooling in the absence of
radiation. Note that crocodilians were considered for a long time to lack a
pineal gland (Tosini, 1997
),
but the recent discovery of a pineal gland in the American alligator
Alligator mississippiensis (Daphne Soares, personal communication)
dispels that notion.
The aim of this study was to investigate the heart rate response of the estuarine crocodile Crocodylus porosus to different heat transfer mechanisms (radiation and convection) and to varying heat loads.
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Materials and methods |
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Experiments were approved by the University of Queensland animal ethics and experimentation committee, Permit No. ZOO/ENT/266/01/URG, and crocodiles were held under the Queensland Parks and Wildlife scientific purposes permit, No. W4/002709/01/SAA.
Experimental setup
Heart rate in C. porosus was measured from electrocardiograms
(ECGs). Pacemaker stainless steel electrodes (Medtronic, Fourmes, France) were
placed under the skin (after application of the local anaesthetic lignocaine)
on the ventral surface just anterior to the heart and at the base of the tail.
The insulated ECG leads were sutured to the skin and secured with tape at the
tail. A small drop of superglue was used to waterproof the holes in the skin
from which the leads exited. Body temperature was measured with a K-type
thermocouple, which was inserted 56 cm into the cloaca. The
experimental animal was then transferred to a custom-built, Perspex chamber
(10 cmx60 cmx60 cm, width x length x height),
which allowed the animal to sit comfortably on the bottom but did not permit
it to turn around. Crocodiles were heated with an infra-red heat lamp
suspended above the Perspex chamber. Radiation from the heat lamp was measured
with a pyranometer (Sol Data, Silkeborg, Denmark) connected to a data logger
(Data Electronics, Melbourne, Australia), and the height of the lamp above the
animal was adjusted so that it delivered 800 kW m2 to the
surface of the animal. The heat from the lamp was similar to the solar
irradiation during basking on a summer morning (F.S., unpublished data). For
control treatments, a cold, fibreoptic light covered with red cellophane was
also positioned above the chamber and directed onto the surface of the
crocodile. Water flow through the experimental chamber could be adjusted
remotely and, when water was used as a treatment, depth was adjusted to half
of the height of the crocodile in a lying position, and flow rate was set at
3cms1. A thermocouple was also placed in the water in the
chamber to record water temperature. The experimental chamber (and animal) was
located in an isolated controlled temperature room set at 23°C, which was
monitored by a remote video camera. Physiological data collection, lamps and
water flow were controlled from an adjoining room, preventing disturbance to
the animals.
The ECG and thermocouple leads were directed to a computer data acquisition system. ECG leads were connected to a high-gain AC amplifier (BioAmp; AD Instruments, Sydney, Australia) that was coupled to a four-channel PowerLab (AD Instruments). The signals from the thermocouples (body and water temperatures) were also directed to the PowerLab. The PowerLab was connected to a Toshiba laptop computer and its output was displayed using Chart software (AD Instruments). Sampling rate was set at 100 Hz, and Chart software calculated heart rate in real-time. Heart rate, body temperature and water temperature were recorded continuously during experimentation.
Treatments
The effects of heating and cooling on the heart rate and body temperature
of C. porosus via a radiant heat source (lamp) and by convective
transfer from flowing water were investigated. Five treatments (see below)
were applied in random order to each of the six experimental animals. Heart
rate, body temperature and ambient temperature were recorded for 10 min prior
to the treatments to obtain baseline resting values.
Cold light control (CLC)
This treatment examined the potential effects of light, rather than heat,
on heart rate. A fibreoptic light emitting red light was switched on for 10
min, then switched off, and recording of heart rate continued for another 10
min.
Cold water control (CWC)
This treatment examined the effect of water flow on heart rate. The
experimental chamber was emptied of water and the animal allowed to rest
undisturbed for 3060 min before water flow to the chamber was turned
on. Water temperature was equal to body temperature, and recording of heart
rate was continued for 10 min.
Hot water (HW)
This treatment examined the effect of convective heat transfer from heated
water flowing past C. porosus. Water at 2325°C was
directed past C. porosus in the experimental chamber, and heart rate
was recorded for 10 min before the water temperature was increased to
35°C. When body temperature reached 3133°C, the water was
switched back to 23°C until body temperature returned to its initial value
(approximately 23°C).
Heat lamp dry (HLD)
This treatment tested the effect of irradiation from a heat lamp under dry
conditions (i.e. no water in the chamber). The heat lamp was switched on until
body temperature reached 3233°C and then, simultaneously, the heat
lamp was switched off and water flow to the chamber (at 2325°C) was
turned on.
Heat lamp wet (HLW)
This treatment investigated the effect of irradiation from a heat lamp
while C. porosus was half-immersed in flowing water (at
2325°C). Heating was applied until body temperature reached
equilibrium (typically 2628°C), after which the heat lamp was
switched off and animals were allowed to cool to their initial body
temperature.
Statistical analysis
To eliminate short-term variation in heart rate resulting from breathing
bradycardia, for example, heart rates used in statistical analyses were
averaged within 1°C body temperature bins. Additionally, in order to
eliminate intrinsic differences between individual study animals, heart rate
data used in statistical analyses (but not in figures) were transformed by
dividing heart rates during heating and cooling by resting heart rates
measured prior to the treatments.
Treatments were compared by a three-factor analysis of variance (ANOVA) with body temperature used as a co-variate; the factors were `treatment' (three levels: HLD, HLW and HW), `heating/cooling' (two levels) and `crocodile' (six levels). The error d.f. for the co-variate was 171 (including heart rate measurements at different body temperatures), but, for comparisons between `treatments' and `heating/cooling', probabilities were calculated with `crocodile' as the level of replication, i.e. error d.f. = 30. In the CLC treatment, heart rates measured while the cold light was on were compared with the periods preceding and following this interval by one-way ANOVA with `crocodile' as the level of replication. Similarly, in the CWC treatment, heart rates measured during the period while the water was on were compared with resting heart rates in the preceding period by one-way ANOVA. The effect of surface heat loads on changes in heart rate was compared among treatments by a one-way analysis of co-variance (ANCOVA) with `treatment' as factor and `surface heat load' as co-variate.
Note that in all statistical analyses we assumed that heart rates between temperature bins were independent. This was warranted because temperature had only a very minor effect on heart rate, and `body temperature' was used as a co-variate.
Calculations of heat load
Heat loads experienced at the animal surface were calculated by solving
heat transfer equations for heat rate (see
Incropera and DeWitt, 1996).
The experimental treatments represent step function changes in steady-state
thermal conditions. In the different treatments, the relative importance of
heat transfer mechanisms (convection in air, convection in water, radiation
and conduction) varied so that the heat load experienced by the animals
differed, resulting in either heating or cooling. In order to estimate heat
transfer by the different mechanisms, the total animal surface areas were
calculated by the `polynomial' method
(Seebacher et al., 1999
;
Seebacher, 2001
), and the
relative surface areas exposed to different heat transfer mechanisms in each
treatment were estimated from direct observations. In all water treatments
(i.e. all cooling episodes, CWC, HLW and HW treatments), the water level was
adjusted so that half the crocodile's body was submerged and, therefore, half
the animal surface area experienced convective heat exchange with water; note
that, while in water, the ventral surface of the animals was never firmly
pressed against the substrate so that it was assumed to exchange heat by
convection. The upper half of the body would exchange heat by free convection
with air; there was no air flow in the constant temperature room, and the
animals were more or less motionless during the treatments so that free
convection conditions were assumed. Radiation from the heat lamp is absorbed
by the silhouette area of the animal, which is 33% of the total surface area
exposed (Muth, 1977
). Hence,
in the HLW treatment, 50% of the animal surface was exposed to air, and, of
this proportion, 33% would have absorbed radiation. In the HLD treatment, 33%
of the animal surface was in contact with the ground while 67% exchanged heat
by convection with air, and, of this 67%, 33% (the silhouette area) absorbed
radiation from the heat lamp. Moreover, the total exposed area would emit and
absorb thermal radiation with the environment.
Convection coefficients (h) for free convection conditions can be
estimated by:
![]() | (1) |
![]() | (2) |
![]() | (3) |
Coefficients for forced convection in water were calculated for a cylinder
with cross flow (Churchill and Bernstein,
1977). Reynolds numbers describe the ratio of inertial and viscous
forces (Re=vL/
, where v is fluid velocity and L is the
characteristic dimension of solid), and the Prandtl number represents the
ratio of the momentum and thermal diffusivities (Pr=
/
). For
cylinders with cross flow, the following single comprehensive equation exists,
which relates dimensionless numbers for a wide range of flow patterns, i.e.
for a wide range of Re and Pr (Churchill
and Bernstein 1977
):
![]() | (4) |
The heat rate at the animal surface can be calculated from the surface
energy balance (Incropera and DeWitt,
1996):
![]() | (5) |
![]() | (6) |
![]() | (7) |
![]() | (8) |
In comparisons with heat load, heart rates were expressed as the change in heart rate with temperature, i.e. the second derivative. Conceptually, these units resemble Q10, although the advantage is that they can be expressed as both positive and negative numbers. In addition, the `rapid response' periods during which body temperature remained stable (see below) were not included in the analysis of surface heat loads.
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Results |
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|
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In the control treatments, heart rate was not significantly different while the cold light was on (CLC) compared with the preceding or following periods (F2,15=0.46, P=0.64; Fig. 3). Similarly, the cold water (CWC) treatment, i.e. exposing the crocodiles to water at the same temperature as their body temperature, did not elicit a significant change in heart rate (F1,10=0.02, P=0.89; Fig. 3).
|
Although heart rate changed significantly with body temperature, Q10 values associated with the heart rate response varied considerably with time during the heating or cooling phases (Fig. 4A). In fact, Q10 values were exceedingly high when the heat source was switched on or off. For example, when the heat lamp was switched off in the HLD treatment (Fig. 4A), heart rate changed with a Q10 of 4627 this is, of course, a nonsensical value that reflects that heart rate changed while body temperature remained nearly stable. During these `rapid response' periods when heat was first applied or removed, heart rate changed dramatically while body temperature remained nearly constant (Fig. 4B,C). In the later phases of heating and cooling, heart rate changed with body temperature, representing a Q10 of 23 (Fig. 4A).
|
Changes in heart rate outside the `rapid response' periods are a function
of the heat load experienced at the animal surface. In all three treatments,
changes in heart rate per °C body temperature (HR; measured in
beats min1 deg.1) changed sigmoidally with
heat load [
HR=(0.575+0.203W)/(1+0.0168W0.00108W2);
r2=0.92; Fig.
5A]. Hence, heart rate increased or decreased very rapidly when
the animal experienced large positive (above 25 W) or negative (below
15 W) heat loads, respectively. Between 15 W and 25 W, the
increase in heart rate with increasing heat load was linear
(Fig. 5B). Over this linear
range, heart rate increased significantly with increasing heat load (ANCOVA
F1,31=23.31, P<0.0001), but changes during the
HW treatment were significantly less than during the two heat lamp treatments,
which did not differ from each other (F2,31=6.43,
P<0.01; Fig. 5B).
During the HW treatment, changes in heart rate increased according to
HR=1.07+0.11W (r2=0.43), and during the HLW
and HLD treatments (data from both treatments combined)
HR=1.90+0.38W
(r2=0.70; Fig.
5B).
|
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Discussion |
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It is generally accepted that physiological performance is sensitive to
changes in body temperature and that there is a distinct performance peak that
coincides with a narrow range of optimal body temperatures. Performance may
cease altogether outside the boundaries of acceptable body temperatures, which
are defined by the critical thermal minima and maxima
(Huey, 1982;
Huey and Bennett, 1987
;
Angiletta et al., 2002
). Such
thermal dependence is presumably a function of underlying biochemical
processes whose rate is temperature dependent, although their thermal
sensitivity may change as a result of acclimatisation (phenotypic changes) or
adaptation (genotypic changes) (St Pierre
et al., 1998
; Crawford et al.,
1999
; Guderley and Leroy,
2001
). If performance were directly related to fitness, it could
be expected that temperature-sensitive physiological functions proceed at
optimal rates at those body temperatures that are achievable by
thermoregulating animals (Bennett et al.,
1992
; Leroi et al.,
1994
), and adaptive changes in thermal optima within and between
species have been shown to occur along altitudinal and latitudinal gradients
(Crawford and Powers, 1992
;
Pierce and Crawford, 1997
;
Ståhlberg et al., 2001
).
Our data, however, indicate that despite their importance in controlling rates
of heating and cooling (Seebacher,
2000
; Seebacher and Franklin,
2001
), changes in heart rate are to a large extent independent of
body temperature. It seems more plausible that the mechanisms controlling
heart rate during heating and cooling evolved as a correlated response to
selection pressures favouring optimal performance of temperature-sensitive
rate function. Hence, commonly accepted models used to explain evolutionary
relationships between body temperature and physiological performance
(Huey and Bennett, 1987
;
Angiletta et al., 2002
) may not
be applicable to cardiac function in heliothermic reptiles.
The heart rate response appears to be elicited, at least in part, by the
heat load experienced at the animal surface, which indicates that, rather than
being an onoff response, the control mechanisms act in an analogue
manner and their magnitude depends on environmental stimuli. Interestingly, in
`unnatural' heating situations (e.g. hot water), heart rate hysteresis was
evident, but the patterns of heart rate were different from the heat lamp
treatments. Heat loads experienced during the HW treatment were similar to
those during the HLD treatment, but the mechanisms by which heat was exchanged
differed. These data indicate that there exists a heat-sensitive control
mechanism that triggers a heart rate response before body temperature changes.
It seems likely, therefore, that the heart rate response is at least partly
controlled locally at the animal surface. Prostaglandins are a possible
mechanism that may control cardiac response during heating and cooling
(Robleto and Herman, 1988)
via the baroreflex, by contraction or dilation of capillary beds,
and/or by directly stimulating the heart. The baroreflex is likely to play a
role in modulating heart rate, particularly in crocodiles
(Altimiras et al., 1998
); it
has been demonstrated that peripheral blood flow changes in response to heat
(Grigg and Alchin, 1976
;
Smith et al., 1978
), and this
response in blood flow may precede the response in heart rate
(Morgareidge and White,
1972
).
The difference between heat lamp and hot water treatments indicates,
however, that there may be additional control mechanisms operating. In many
reptiles, thermoregulatory responses are thought to be controlled by the
light-sensitive pineal gland (Tosini,
1997). Crocodilians were long believed not to possess a pineal
gland (Tosini 1997
), but a
pineal-like organ was recently discovered in the American alligator (Daphne
Soares, personal communication). The fact that, in our study, the heart rate
response differed between radiant heating and convective heating in water
(although the hysteresis effect was apparent in all experimental treatments)
indicates that light-sensitive mechanisms may play a role in controlling
cardiac response during heating and cooling. Furthermore, the body
surface/region over which heat is transferred may also modulate the response
of the heart. During radiant heating, the dorsal surface of the crocodile was
chiefly responsible for the transfer of heat, whereas during convective
heating, it was the ventral and lateral surfaces of the crocodile that were
involved in the transfer of heat. Along with the involvement of the pineal
gland, our results also suggest that the heat transferred across the dorsal
surface (as opposed to the ventral and lateral surfaces) could augment the
cardiac response to heating and cooling.
Many reptiles use an array of postures while thermoregulating
behaviourally. In particular, crocodiles in the wild alter the relative
proportions of body surface area exposed to different heat transfer mechanisms
to regulate body temperature (Seebacher,
1999; Grigg et al.,
1998
; Seebacher et al.,
1999
). Our experimental treatments mimicked some typical
thermoregulatory postures observed in thermoregulating crocodiles
(Seebacher, 1999
), and our
data indicate that the placement of the animal within its biophysical
environment determines the magnitude of the physiological mechanisms used to
control rates of heating and cooling.
There were marked `rapid responses' in heart rate of C. porosus to
the initial stages of heating and cooling. Similar responses were recorded by
Seebacher and Franklin (2001)
in Pogona barbata. However, a number of studies investigating changes
in heart rate in reptiles with heating and cooling have failed to show this
initial rapid response period (Dzialowski
and O'Connor, 2001
). We believe that this reflex response could
have been masked by the methods used by previous investigators, where animals
were often restrained when heated and cooled. For example, Dzialowski and
O'Connor (2001
) tied their
lizards to doweling. It is well known that restraint activates the adrenergic
(release of catecholamines) and cholinergic systems in reptiles
(Lance and Elsey, 1999
) and,
given that Seebacher and Franklin
(2001
) identified a role of
the adrenergic and cholinergic systems in the control of heart rate during
thermoregulation in Pogona barbata, activation of the stress axes may
override or mask the rapid cardiac response. We recommend that in future
studies where the heart rate responses of reptiles to heating and cooling are
investigated, experiments are conducted with unrestrained animals.
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Acknowledgments |
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