The ontogenetic changes in the thermal properties of blubber from Atlantic bottlenose dolphin Tursiops truncatus
1 Biological Sciences, University of North Carolina at Wilmington, 601 South
College Road, Wilmington, NC 28403, USA
2 Department of Mathematics and Statistics, University of North Carolina at
Wilmington, 601 South College Road, Wilmington, NC 28403, USA
* Author for correspondence (e-mail: pabsta{at}uncw.edu)
Accepted 23 February 2005
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Summary |
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Key words: blubber, thermal conductivity, thermal conductance, lipid, ontogeny, dolphin, Tursiops truncatus, heat flux
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Introduction |
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Insulation may be particularly important to neonatal bottlenose dolphins
that are born into water, which is a fluid medium that conducts heat away from
a body 25 times faster than air at the same temperature
(Parry, 1949;
Schmidt-Nielsen, 1997
;
Scholander et al., 1950
).
Because a neonatal dolphin has a larger surface area to volume ratio than an
adult, heat loss to the environment may be high
(McLellan et al., 2002
;
Worthy and Edwards, 1990
).
Struntz et al. (2004
)
suggested that the blubber of neonatal dolphins may be specialized to provide
enhanced insulation. To date, however, no study has measured changes in the
thermal properties of blubber across an ontogenetic series.
Blubber's thermal properties have been measured across a phylogenetically
diverse sample of cetaceans (Table
1). Thermal conductivity k (W m1
deg.1), a material property, is a quantitive measure of how
well heat moves through a material (McNab,
2002; Schmidt-Nielsen,
1997
) and is, thus, useful for comparing the insulative quality of
blubber across species (Worthy and
Edwards, 1990
). Thermal conductance C (W
m2 deg.1), which is dependent upon the
material thickness, or quantity of blubber, provides an absolute value of heat
transfer across this thermal barrier. Conductivity can be calculated using the
Fourier equation:
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Across cetacean species, blubber's thermal conductivity can vary by more
than fourfold, from 0.06 W m1 deg.1 in
harbor porpoises Phocoena phocoena to as high as 0.28 W
m1 deg.1 in minke whales Balaenoptera
acutorostrata (Table 1). These differences in blubber's quality as a conductive material are likely the
result of differences in lipid and water content, which are highly variable
among species. The lipid content of harbor porpoise blubber can range between
76 and 88% (Worthy and Edwards,
1990), while that of minke whales can range between 42 and 96%
lipid (Kvadsheim et al.,
1996
). Several studies have measured a significant inverse
relationship between lipid content and conductivity as well as a strong
positive relationship between conductivity and water content
(Kvadsheim et al., 1996
;
Worthy and Edwards, 1990
).
Blubber's thermal conductance, which is reliant upon both its conductive
quality and quantity (i.e. thickness), also varies widely across species. For
example, harbor porpoise blubber has a lower conductivity than that of a
pan-tropical spotted dolphin Stenella attenuata
(Table 1), and is twice as
thick (1.50 cm and 0.77 cm, respectively;
Worthy and Edwards, 1990).
Spotted dolphin blubber thus has a conductance value four times greater than,
or an insulative value one quarter of, harbor porpoise blubber.
In Atlantic bottlenose dolphins, blubber thickness and lipid content vary
significantly throughout ontogeny. Blubber lipid content doubles between fetal
(37%) and adult animals (68%) and mean blubber thickness increases over
threefold between these life history categories
(Struntz et al., 2004). These
significant changes in quality and quantity suggest that changes in blubber's
thermal properties across ontogeny may be equal to or greater than differences
reported among species.
Multiple methods have been used to measure blubber's thermal conductivity
and thermal conductance. Parry
(1949) and Scholander et al.
(1950
) measured thermal
conductivity by placing two pieces of blubber on either side of a hot plate
and measuring the rate of energy (W) used to maintain the plate at a constant
temperature. The surface area and thickness of the blubber sample, and the
temperature differential between the hotplate and environment, were used to
calculate thermal conductivity (Eq. 1). A more recent method of measuring
thermal conductivity relies upon the use of heat flux discs. A heat flux disc
is placed in series with, and usually between, a constant heat source and the
blubber sample. Once steady state is achieved, Eq. 1 can be used to calculate
conductivity (Doidge, 1990
;
Worthy and Edwards, 1990
;
Yasui and Gaskin, 1986
).
Kvadsheim et al. (1994
)
introduced a method to calculate conductivity that does not rely upon a direct
measure of heat flux. Instead, this method uses a standard material, with a
known thermal conductivity, aligned in series with a heat source and blubber
sample. Once the system reaches steady state, the heat flow rate through each
material must be equal (Kreith,
1958
; Kvadsheim et al.,
1994
). The Fourier equation (Eq. 1) can then be used to calculate
the thermal conductivity of blubber by setting equal the heat flow through the
standard material and blubber sample. Each of these methods provides a minimum
value of thermal conductivity and insulation, because they are measuring dead
tissue (i.e. in the absence of convective heat transfer by blood flow) and are
carried out in air, a less thermally conductive medium than water.
Each of these more recent methods has advantages and disadvantages. Heat
flux discs are relatively affordable, convenient to use, and the results are
directly comparable to many previous measurements of blubber's thermal
properties (see Table 1).
However, the placement of the disc on the surface of interest will cause a
local increase in insulation, which may result in measured heat flux values
that are lower than the actual values
(Ducharme et al., 1990). This
`reactive error' varies with both the insulative quality of the material
relative to that of the heat flux disc, and the insulative quality of the
media overlying the disc (usually air or water;
Ducharme et al., 1990
;
Frim and Ducharme, 1993
).
Reactive errors are minimized when the disc's insulation is equal to or lower
than that of the material being tested and when the experiments are conducted
in air (Frim and Ducharme,
1993
; Willis,
2003
). The standard material method avoids these potential heat
flux disc errors and, as reported by Kvadsheim et al.
(1994
), is accurate to within
±4.0%. Because it is a relatively new technique, however, there are
fewer studies that have measured blubber's thermal properties using this
method. In the present study, both the heat flux disc and standard material
methods were used simultaneously, permitting cross-calibration of these
methods as well as an enhanced ability to compare results from previous
studies.
The goals of this study were to (1) measure the thermal conductivity and thermal conductance of Atlantic bottlenose dolphin blubber across an ontogenetic series, (2) correlate these thermal conductivity and conductance values with measures of lipid and water content of blubber, and (3) compare the results of the heat flux disc and standard material methods to permit comparison with previous studies. Measurements were made across life history categories from fetus through adult. Pregnant females and emaciated adults were also included to investigate how blubber's thermal properties vary with the reproductive and nutritional status of the dolphin.
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Materials and methods |
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Each animal was first weighed to the nearest kg (2000 kg capacity scale;
Dillon, Brooklyn, NY, USA) and measured using a standard set of morphometrics
(body and appendage lengths and body girths; see
Norris, 1961). The carcass was
then systematically dissected (McLellan et
al., 2002
) and full depth integumental samples, including
epidermis, dermis and hypodermis (subsequently referred to as blubber
samples), were taken from a dorsal, mid-thoracic site, just caudal to the
pectoral flipper (Fig. 1).
After removal, the blubber samples were notched at the dorso-cranial margin to
maintain orientation and were then either vacuum sealed (Koch 1700, Kansas
City, MO, USA) or wrapped in Saran wrap® and sealed in freezer bags to
prevent desiccation. Samples were stored at 20°C until analyzed.
While these collection and storage methods may influence the thermal
properties of blubber, they permitted standardized sample treatment within
this study and comparison to previously published studies (see
Table 1).
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Lipid and water content
Lipid content was determined using procedures similar to those of Struntz
et al. (2004). Briefly, an
approximately 1 g full-depth blubber sample (excluding the epidermis) was
weighed to the nearest 0.001 g, macerated and dried with approximately 30 g of
sodium sulfate (Na2SO4). The lipid was then extracted
using an accelerated solvent extractor (Dionex, Salt Lake City, UT, USA). The
excess solvent was evaporated (Turbo Vap II, Zymark, Hopkinton, MA, USA) and
the extracted lipid was then reweighed to the nearest 0.001 g.
Water content was determined by excising an approximately 1 cm x1 cm square through the depth of the sample and weighing it prior to and after freeze-drying (Labconco 4.5, Kansas City, MO, USA). Samples were weighed each day until the mass of the sample was stable (±0.005 g) for 2 consecutive days (total time=5 days).
Measurement of thermal properties
Blubber's thermal properties were measured using an experimental set-up
that was similar to those of previous studies and that integrated both the
standard material (Kvadsheim et al.,
1994) and heat flux disc (e.g.
Worthy and Edwards, 1990
)
methods. Tests were conducted in a dual compartment heat flux chamber (68
quart, Coleman Cooler, Albany, NY, USA) with a lower, highly insulated
compartment, and an upper, chilled compartment, which were separated by a wood
platform (Fig. 2). The heat
source consisted of a two-part aluminum box. The lower portion was a sealed,
hollow box into which heated water (35°C) from a water bath (RE-120 Lauda
Ecoline, Brinkmann Instruments, Inc., Toronto, Ontario, Canada) was circulated
to provide a constant heat source. The upper portion was an open platform upon
which the standard material and blubber sample were placed. The insulated
lower chamber ensured a constant water temperature and unidirectional heat
flow through the standard material. The upper chamber was cooled with ice
packs stacked upon the wood platform and cooled to between 16 and 19°C.
This temperature was monitored with a thermocouple mounted 5 cm above the
sample.
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An elastomer (Plastisol vinyl, Carolina Biological Supply, Burlington, NC, USA) (k=0.109 ± 0.01 W m1 deg.1) was used as the standard material and was placed flush against the heated surface of the aluminum box. Depending upon the size of the available blubber sample, an approximately 4 cm x4 cm to 15 cm x15 cm blubber sample was used. The thickness of the blubber sample, including epidermis, dermis and hypodermis, was measured on each of its four sides (Absolute Digimatic calipers, Mitutoyo, Tylertown, MS, USA) and the mean of these values was used in thermal calculations. The blubber sample was placed in series, with the deep hypodermis in contact with the elastomer. The standard material and blubber were surrounded by insulating foam plates to ensure unidirectional heat flow through these materials (Fig. 2).
Temperatures were measured using copper-constantan (T-Type) thermocouples (Omega Engineering, Inc, Stamford, CT, USA) placed on the superficial surface of the epidermis (probes 13), between the blubber and the standard material (probes 46), and between the standard material and the surface of the heat source (probes 79; Fig. 2). The mean temperature of the three probes at each surface was used in the thermal calculations. In addition, to monitor temperature changes within the blubber, thermocouples 10 and 11 (Fig. 2) were placed at deep and superficial positions within the blubber sample.
Heat flux was measured directly using two heat flux discs [HA 13-18-19-P (C), Thermonetics Corp., San Diego, CA, USA]. One disc was placed on the superficial surface of the epidermis and the other was placed between the standard material and hypodermis (Fig. 2). The discs will be identified as the superficial and deep discs, respectively. The specific disc that was placed at the deep or superficial position was determined using a random schedule. To ensure complete contact between the superficial heat flux disc and the sample, thin strips of medical adhesive tape (Nexcare Advanced Holding Power, 3M, St Paul, MN, USA) were used to secure the disc. The tape was only in contact with the outer silicone edge of the disc and did not touch the thermopile surface. The superficial disc was visually inspected to ensure that it was flush against the epidermis.
All eleven thermocouples and the two heat flux discs were wired to a Fluke Hydra data logger (model 2625A, Fluke Inc., Everett, WA, USA) and the outputs in °C and mV, respectively, were recorded at 1 min intervals. These data were downloaded to a laptop computer for later analysis. The experiment was concluded once the heat flux values at the superficial and deep surfaces were stable (±5 W m2) for 30 min (Fig. 3). Once steady state was achieved, temperature values measured at all positions varied only 0.16±0.13°C (mean ± S.D.). Heat flux readings were converted into W m2 using the calibration coefficient provided by the manufacturer.
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The experimental set-up was calibrated using control materials (white pine wood, polystyrene foam; Dow Chemical, Midland, MI, USA) with known thermal conductivities. Additionally, experiments with the control materials were performed to determine if sample depth or surface area influenced thermal measurements.
Statistics
For thermal conductivity, conductance and insulation values, an analysis of
covariance (ANCOVA; SAS Inc., Cary, NC, USA; P=0.05) was used with
life history category and sample area as factors. Sample area was included to
account for variation in the measurements that was a result of differences in
the dimensions of the blubber sample. If significant differences were present,
a Ryan's Q-test was used to determine which groups were different
from one another. A one-way analysis of variance (ANOVA) (P=0.05) was
performed to determine if there were significant differences between life
history categories in blubber thickness, lipid content, and water content. A
TukeyKramer Honestly Significant Difference Test was used to identify
significantly different groups.
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Results |
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Blubber lipid content increased linearly with body length in fetuses (r2=0.65; P=0.028) and increased steadily from fetal through juvenile life history categories (Fig. 4B, Table 3). Although not a significant trend, lipid content declined between juvenile and adult life history categories. The blubber of pregnant females had a lipid content similar to that of juvenile animals, which represented an increase of 27% compared to adults. The blubber of emaciated adults contained significantly less lipid than all life history categories except fetuses (Table 3).
Across life history categories, blubber thickness was not a good predictor of lipid content (Fig. 5). Rather, the relationship between lipid content and blubber thickness displayed life history category-specific trends. In fetal and adult animals, lipid content increased linearly with blubber thickness (r2=0.91; P=0.0034 and r2=0.96; P=0.0008, respectively). Although not a significant trend, blubber lipid content of sub-adults tended to increase with blubber thickness (r2=0.54; P=0.097). Blubber thickness and lipid content were not correlated in neonatal, juvenile, or pregnant animals. There was no clear relationship between lipid content and blubber thickness in emaciated adults, however, both of these measures were highly reduced from adult values (Fig. 5, Table 3).
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Water content was less variable across life history categories (Table 3). The blubber of fetuses and emaciated adults, which had significantly lower lipid contents, contained significantly more water than all other life history categories (F=14.84; P<0.001).
Comparison of standard material and heat flux methods
Both the standard material method and the heat flux method (using outputs
of either the superficial or deep disc) yielded thermal conductivity values
for the control materials that were similar to their commercially reported
values. For polystyrene foam and white pine wood, thermal conductivity values,
reported as mean ± standard error
(S.E.D.), were determined to be
0.033±0.0014 W m1 deg.1 (reported
value 0.03 W m1 deg.1; Dow Chemical
Company) and 0.11± 0.0025 W m1
deg.1 (reported value 0.104 W m1
deg.1, Liley,
1996), respectively. These values indicate a maximum error of 10%
for conductivity values in the range of polystyrene foam, but error was
minimized to 6% for materials with conductivity values similar to wood.
Blubber thermal conductivity values calculated with the standard material method and with the output of the superficial heat flux disc were similar (F=0.05; P=0.81) and yielded overall mean conductivity values that were within 2.0% of each other (Fig. 6A,B). The results of both of these methods though, were significantly different from the values obtained from the deep heat flux disc measurements (F=31.8; P<0.001) (Fig. 6C). On average, conductivity values of whole blubber calculated with the deep disc were 57% higher than those obtained with the other two methods. The differences between the deep and superficial heat flux measurements are described in more detail below.
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For all subsequent analyses, the conductivity values obtained by the
standard material method were used. The standard material method was chosen
because recent studies (Kvadsheim et al.,
1994,
1996
) have extensively
calibrated a similar system.
Thermal properties of blubber
Thermal conductivity of blubber remained similar in fetal through sub-adult
life history categories but increased significantly in adult animals
(F=6.93; P<0.001;
Table 3;
Fig. 6A). The conductivity of
blubber from pregnant females was significantly less than that of adults while
that of emaciated adults was significantly greater than all other life history
categories (Table 3,
Fig. 6A). There was a
significant inverse relationship between thermal conductivity and lipid
content (F=5.8; P=0.021) and a significant positive
relationship between thermal conductivity and water content (F=4.83;
P=0.034) (Fig.
7A,B).
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The mean thermal insulation (inverse of conductance) between life history categories varied significantly (F=12.66; P<0.001; Table 3). Insulation increased from fetal through sub-adult categories but declined in adult animals. Pregnant females had a significantly higher mean insulation value compared to fetuses, neonates, adults and emaciated adults. Emaciated animals had significantly less insulation than juveniles, sub-adults and pregnant females.
Differences in heat flux values across blubber thickness
For blubber samples, there was a substantial difference between heat flux
values recorded by the deep and superficial heat flux discs. The deep disc
consistently recorded higher values (mean of difference=46.8 W
m2; range=9.987.2 W m2) than the
superficial disc, and, thus, yielded thermal conductivity values that were
higher than those reported for the other two methods
(Fig. 6). This result is in
contrast to that for the control materials, polystyrene foam and white pine
wood, where deep and superficial heat flux values were similar to each other.
For the foam, the mean difference between the superficial and deep discs was
3.45 W m2 (range=3.56.2 W m2) and
for the wood, the mean was 10.25 W m2 (range=5.314.7
W m2).
In blubber, sample thickness was significantly correlated with the difference in heat flux between the deep and superficial discs (F=11.91; P=0.0014) (Fig. 8). To determine if this difference was due simply to heat loss to the sides of the blubber sample, experiments using increasing layers of polystyrene foam or wood were performed. For these control materials, there was no pattern of increased heat loss with increased material depth (foam: F=0.85; P=0.42; wood: F=4.26; P=0.28) (Fig. 8). There was a weak, non-significant relationship between the surface area of the blubber sample and the heat flux difference (F=3.54; P=0.067). There was no relationship between the surface area of the foam sample and the difference in heat flux (F=5.8; P=0.137). Thus, in contrast to the control materials, there existed a substantial difference between the energy entering the deep surface of the blubber and that leaving the sample at its superficial surface per unit time. There was no relationship between the magnitude of this difference in heat flux and life history category (F=1.74; P=0.14), lipid content (F=1.49; P=0.23), or water content (F=0.06; P=0.81).
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Discussion |
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Blubber's quality, quantity, and thermal properties
Fetal blubber underwent continuous growth throughout gestation, with both
thickness and lipid content increasing rapidly. This growth pattern, similar
to that observed by Struntz et al.
(2004), prepares the animal
for birth into water, a highly conductive medium. In contrast with pinnipeds,
which are born on land, cetaceans must be fully capable of maintaining thermal
homeostasis in water at the time of birth. Thus, blubber, their primary
thermal barrier, must be of an appropriate thickness and quality to minimize
heat loss.
Fig. 9 illustrates how blubber's thickness, lipid content, conductivity, and insulation values varied across life history categories. Between fetal and juvenile life history categories, both lipid content and blubber thickness increased. Blubber's thermal conductivity, which is independent of thickness, remained stable between these life history categories. In contrast, thermal insulation, a measure of both blubber quality (i.e. conductivity) and quantity (i.e. thickness), increased threefold. The results suggest that neonatal blubber is not specialized to provide enhanced insulation, but rather that fetal, neonatal and juvenile life history categories represent a period of continual blubber growth blubber's thermal conductivity remains static but its thermal insulation increases as a result of increased blubber quantity.
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The juvenile life history category represented a transitional period in blubber's development, in which lipid content peaked and blubber thickness values were similar to those of adults. Between juvenile and adult life history categories, blubber lipid content decreased steadily and adult blubber had a significantly higher conductivity than all non-emaciated categories. The insulation of adult blubber was also significantly less than that of sub-adults, due to a decrease in blubber quality, rather than quantity. Thus, two distinct patterns describe ontogenetic changes in the thermal properties of blubber. Dolphins that were either completely or partially dependent on their mother's milk increased blubber quantity but maintained similar blubber quality. Dolphins that were nutritionally independent maintained relatively stable blubber quantity, and rather varied the quality of the blubber layer.
Interestingly, the blubber of neonatal and juvenile animals had the same
insulation value as that of adult dolphins. This result suggests that the
mass-specific metabolic rates of these young animals could be higher than
those of adult dolphins to compensate for the relatively higher rates of heat
loss resulting from their larger surface area to volume ratios. Across
mammalian species, mass-specific metabolic rates scale to body
mass0.25 (Kleiber,
1961) and young animals are known to have relatively higher
mass-specific metabolic rates compared to adult animals of the same species
(reviewed in Lavigne et al.,
1986
). To estimate the relative metabolic rates of neonatal and
adult dolphins in this study, the heat flux value (W m2,
from the superficial disc) for each dolphin was multiplied by the surface area
(m2) of the dolphin (see Table
4 for methods of estimating surface area). The resulting metabolic
rate was then divided by the mass of the animal to obtain a mass-specific
metabolic rate.
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The results of these calculations indicate that the mass-specific metabolic
rate of neonatal bottlenose dolphins is approximately three times higher than
that of adult dolphins. This result is consistent with experimentally derived
values for newborn harbor seals Phoca vitulina
(Miller and Irving, 1975), and
pups of California sea lions Zalophus californianus
(Thompson et al., 1987
) and
northern fur seals Callorhinus ursinus
(Donohue et al., 2000
), which
ranged between 2.4 and 4 times higher than mass-specific metabolic rates
predicted by Kleiber (1961
)
for adults of similar body mass. Noren
(2002
) also found that
northern elephant seal Mirounga angustriostris pups had metabolic
rates 0.91.6 times those predicted by Kleiber
(1961
) for adult animals.
The estimated mass-specific metabolic rate for neonates in this study,
though, is 9% lower, and the adult value 38% lower, than those values
predicted by Kleiber (1961).
The calculated adult metabolic rate is also considerably lower than the
resting metabolic rate for this species (0.392±0.01 l O2
h1 kg1; measured by
Williams, 1999
). There are
multiple reasons why the mass-specific metabolic rates measured in this study
may be low. First, only the post-cranial body surface area was calculated
the appendages and head were excluded. Second, blubber thickness is
not uniform across the cetacean body (e.g.
Doidge, 1990
;
Koopman, 1998
), and because
these calculations were made with heat flux values at one body site, errors
associated with differences in blubber thickness are likely to occur. Finally,
the calculated metabolic rates in this study used heat flux values that were
measured in air and on inert tissue in the absence of blood flow. These
calculated metabolic rates do, however, illustrate the relative differences in
the cost of endothermy in animals of varying body size as well as represent an
estimated minimum metabolic rate for bottlenose dolphins.
The thermal properties of blubber were also influenced by morphological and compositional differences associated with changing reproductive and nutritional status. Blubber from pregnant females had lipid contents similar to juveniles, and blubber thicknesses that were similar to adults, which resulted in an overall insulation value that was higher than that of adults. Blubber layers of sub-adult and pregnant females had the highest insulation values of any life history category, suggesting that these categories may represent a maximal insulation value for bottlenose dolphins.
Emaciation profoundly impacted blubber's thermal properties. The insulation
value of emaciated blubber was substantially lower than that of adults. With a
low blubber insulation value, emaciated animals likely experience relatively
higher rates of heat loss to the environment compared to non-emaciated adults,
and their metabolic rates may, thus, be higher. In the emaciated state,
blubber's dual roles of providing insulation and storing metabolic energy are
in direct opposition. Fasting marine mammals rely upon both lipid and protein
catabolism (e.g. Noren et al.,
2003; Worthy and Lavigne,
1987
), but as lipid is depleted for utilization as energy, the
thermal insulation of the blubber layer is compromised and, therefore, the
rate of heat loss to the environment is increased. The metabolic rate of the
animal may increase to compensate for the increased heat loss and in turn,
more lipid is depleted to meet the increased demand. In this way, the
potential for a positive feed-back loop exists and declining nutritional and
health status is potentially accelerated by the opposing thermal and metabolic
demands on the blubber.
Across life history categories, blubber thickness was generally not a good predictor of lipid content. For a given blubber thickness, lipid content could vary by more than 50%. In an extreme example, emaciated individuals, WAM 533 and WAM 591, had similar blubber thicknesses; however, their blubber lipid content was 41% and 3.3%, respectively. Reducing the thickness of this tissue may be detrimental to blubber's other functions such as streamlining the body. Interestingly, in the life history categories where lipid content was highly reduced (fetuses and emaciated animals), water content was significantly higher. The replacement of lipid with water may be a potential mechanism for maintaining the structural integrity of the tissue despite fluctuations in its lipid content. However, increasing the water content of blubber may compromise its thermal integrity because blubber's thermal conductivity was positively related to its water content and inversely related to its lipid content.
Phylogenetic and methodological comparisons of blubber's thermal properties
The ontogenetic changes in blubber's thermal properties observed in this
study are nearly as great as those observed across a broad range of cetaceans
(Table 1; note that both sample
size and range of life history categories for many of these species were
limited). For all non-adult bottlenose dolphins, blubber thermal conductivity
values were similar to that of harbor porpoise and beluga whale
Delphinapterus leucus blubber. Thus, relatively small bodied, young
dolphins possessed blubber of the same thermal quality as northern temperate
to polar species. In contrast, conductivity of adult bottlenose dolphin
blubber was more similar to that of large baleen whales and tropical
delphinids (Table 1). However,
direct comparisons of absolute thermal conductivity values may be complicated
by differences in experimental methods.
This study simultaneously utilized two common methods of determining the
thermal conductivity of blubber. The standard material method
(Kvadsheim et al., 1994)
relies upon the physical principle that under steady state conditions, the
rate of heat flow through materials placed in series will be equivalent
(Kreith, 1958
). The use of a
heat flux disc permits the direct measure of the rate of energy entering or
leaving a given material (e.g. Worthy and
Edwards, 1990
). In this study the thermal conductivity values
calculated using the standard material method and the heat flux values from
the superficial disc yielded values that were very similar. In contrast,
conductivity values calculated using heat flux values from the deep disc were
more than 50% higher. In most previous studies that have used the heat flux
method, the disc has been placed deep to the blubber
(Worthy, 1991
;
Worthy and Edwards, 1990
;
Yasui and Gaskin, 1986
). Thus,
comparisons between values obtained with deep heat flux measurements and those
obtained by either the standard material method or superficial heat flux
values, must be made with caution. A discussion of the potential explanation
for this pattern is presented here.
The observed difference in the rate of energy entering and leaving the
surfaces of the integument, which was significantly correlated with sample
thickness, may be attributable to several factors. First, heat loss to the
sides of the blubber could cause a reduction in heat flux measured at the skin
surface. The results of calibrations with foam and wood, however, suggest that
changing the thickness of the sample did not affect the difference between
superficial and deep heat flux values in these control materials. Second, the
reactive error (Ducharme et al.,
1990) of the superficial heat flux disc may reduce the heat flux
value at this surface. However, as discussed previously, this error is
expected to be low because the ratio between the insulative quality of the
tissue and disc is low (Rblubber/Rheat flux
disc ranged between 6.02 and 21.7;
Frim and Ducharme, 1993
). The
maximum reactive error can be calculated using the correction factors provided
by Frim and Ducharme (1993
) and
a maximum heat flux value (in this study maximum heat flux=142.7 W
m2). The maximum error attributable to reactive error in
this study was calculated as 8 W m2. Because the difference
between the deep and superficial heat flux measurements could be as high as
87.2 W m2 and was usually near 50 W m2, it
is unlikely that the observed difference in heat flux values is the result of
this source of experimental error. Instead, the difference in heat flux may be
indicative of a previously undescribed property of the integument its
capacity to store heat. We hypothesize that this function may be attributable
to its ability to undergo temperature dependent phase change.
Phase change materials are defined as latent thermal storage materials that
use chemical bonds to store and release heat
(Suppes et al., 2003). These
materials are currently being investigated for use in residential and
commercial buildings as a means of increasing energy efficiency (Nikolic et
al., 2002; Sari, 2003
;
Sari and Kaygusuz, 2001
;
Sari et al., 2003
;
Suppes et al., 2003
). For a
phase change material to efficiently store and release heat, four requirements
must be met (Nikolic et al., 2002; Sari,
2003
; Sari and Kaygusuz,
2001
; Sari et al.,
2003
; Suppes et al.,
2003
) First, the melting point of the material must be in an
appropriate temperature range for the desired application (e.g. near room
temperature for building materials). Second, the material must have a
relatively large latent heat plateau (i.e. the range of temperatures over
which a material will change phase), to maximize the amount of heat that may
be stored. Third, the material must not stratify in the liquid phase, which
would result in an inability to properly solidify when the environmental
temperature is reduced. Finally, an intermittent heat load must be present to
deliver and absorb heat from the material.
There is substantial evidence to support the classification of the
integument, and specifically the blubber layer, as a phase change material.
First, many of the fatty acids found in blubber are classified as phase change
materials and have melting points in the range of mammalian body temperatures
(Sari, 2003;
Sari and Kaygusuz, 2001
;
Sari et al., 2003
;
Suppes et al., 2003
). Suppes
et al. (2003
) classified
palmitic (C16:0), steric (18:0), oleic (C18:1), linoleic (C18:2), linolenic
(C18:3) and arachidic (C20:0) fatty acids as excellent phase change materials.
All of these fatty acids have been identified in cetacean blubber
(Koopman et al., 1996
).
Mixtures of these fatty acids yield phase change materials with melting points
between 29° and 38°C (Suppes et
al., 2003
), which include the range of mammalian body
temperatures. Second, these fatty acids also satisfy the requirement that the
material has a relatively large latent heat plateau, with latent heat values
generally greater than 180 J g1
(Suppes et al., 2003
). Third,
their stratification in blubber may be prevented by their containment in
adipocytes as well as the highly structured nature of adipocytes in the
blubber tissue. Finally, cetaceans are known to have fine vascular control to
their appendages and to the periphery of their body
(Elsner et al., 1974
;
Kvadsheim and Folkow, 1997
;
Ling, 1974
;
Meagher et al., 2002
;
Pabst et al., 1999b
;
Scholander and Schevill,
1955
). Intermittent heat loads could be applied to the blubber
through shunting of warm blood to the blubber layer, followed by periods of
vasoconstriction. Future studies are needed to fully characterize blubber's
potential phase change properties as well as investigate the possible
functions that may be associated with such a property.
Conclusion
Blubber's thermal properties were influenced by morphological and
compositional changes that occurred across ontogeny, and in individuals of
differing reproductive and nutritional status. In nutritionally dependant life
history categories, changes in blubber's thermal properties were characterized
by stable blubber quality and increased blubber quantity. In nutritionally
independent animals, blubber quantity remained stable while blubber quality
varied. The ontogenetic differences in thermal conductivity and thermal
insulation were as large as those reported across temperate to tropical
cetacean species. This study also demonstrated that thermal conductivity
values determined by the standard material method and by a heat flux disc
placed deep to the blubber can differ markedly. Thus, caution should be used
when comparing absolute conductivity values of blubber across studies.
Finally, blubber's fatty acid composition, coupled with the differences in
heat flux values measured at the deep and superficial surfaces of the sample
under steady state conditions, suggest that dolphin blubber may be a phase
change material. The functional consequences of this previously undescribed
feature of the dolphin's integument warrant further study.
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References |
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