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First published online February 15, 2008
Journal of Experimental Biology 211, 798-804 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.014621
Temperature–oxygen interactions in Antarctic nudibranch egg masses
1 Division of Biological Sciences, University of Montana, Missoula, MT 59812,
USA
2 Department of Biological Sciences, Clemson University, Clemson, SC 29634,
USA
* Author for correspondence (e-mail: art.woods{at}mso.umt.edu)
Accepted 8 January 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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500 µm diameter). Consequently,
Antarctic embryos occurred at much lower densities, with very low metabolic
densities.
Key words: Antarctica, Southern Ocean, McMurdo Sound, oxygen, diffusion, egg mass, nudibranch, marine, temperature, global warming, size, polar gigantism, Tritonia
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Clarke and Johnston, 1999;
Woods, 1999;
Peck and Conway, 2000;
Peck, 2002;
Pörtner, 2001;
Pörtner, 2002). Thus,
ecthotherms in cold environments may be released from some constraints on
physiology and form experienced at warmer temperatures.
The Southern Ocean is one of the coldest, most stable marine environments
on Earth (Sidell, 2000) and
represents a unique environment for investigating metabolic consequences of
low temperature. Sea temperatures near the Ross Ice Shelf at McMurdo Station
are approx. –1.9°C year round
(Littlepage, 1965), and have
been <5°C for at least 10–14 MY
(Sidell, 2000). Oxygen levels
are high throughout the water column
(Littlepage, 1965). This
combination of conditions may have released Antarctic ectotherms from
O2-imposed constraints commonly experienced by warmer-temperature
organisms. Several examples support this idea, including low erythrocyte
counts of Antarctic notothenioid fish
(Eastman, 1993), evolutionary
loss of respiratory proteins in some Antarctic icefish
(Ruud 1954;
Cocca et al., 1995), and
gigantism of many Southern Ocean invertebrates
(Chapelle and Peck, 1999).
Here we examine O2 supply–demand relationships in
gelatinous egg masses of Antarctic nudibranchs (Mollusca). Gelatinous masses
may serve a number of functions: retention of embryos in favorable
microhabitats, chemical or structural protection from predation, reduction of
the vulnerable planktonic larval phase, and protection from physical threats
(Pechenik, 1979;
Rumrill 1990;
Rawlings, 1999; Woods and
DeSilets, 1999; Przeslawski,
2004). In temperate waters, metabolism by embryos can establish
steep O2 gradients in egg masses. Hypoxia or anoxia has been
observed directly, or inferred from developmental asynchrony of embryos, in
egg masses of frogs (Seymour and Bradford,
1995; Seymour et al.,
1995; Mitchell and Seymour,
2003), fish (Taylor,
1971), mollusks (Booth,
1995; Cohen and Strathmann,
1996; Moran and Woods,
2007), crustaceans
(Fernández et al.,
2003) and polychaetes
(Strathmann, 2000), and may
reduce the quality of juveniles, kill embryos directly
(Strathmann and Strathmann,
1995), or increase mortality by prolonging development and
exposure to benthic predators (Pechenik,
1999). These effects are important because early-stage survival
and performance strongly influence population dynamics in marine and aquatic
systems (Thorson, 1946;
Strathmann, 1985;
Roughgarden et al., 1987;
Pechenik, 1999; Underwood and
Keough, 2000; Moran and Emlet,
2001).
The preceding paper (Woods and Moran,
2008) described a numerical model capable of predicting full
spatial and temporal profiles of oxygen in egg masses. The work reported here
tests predictions of the model in two ways. The first focuses on intraspecific
effects: as an egg mass is warmed, O2 gradients should become
steeper – i.e. central O2 levels should be depressed. This
effect should be especially strong in Antarctic egg masses, because recent
studies suggest that metabolism in polar organisms can be much more
temperature sensitive than in temperate or tropical organisms. Peck and
Prothero-Thomas (Peck and Prothero-Thomas,
2002), for example, found that in larvae of the Antarctic sea star
Odontaster validus, O2 consumption rates increased by a
factor of nearly 1.5 over a temperature range between –0.5 and 2.0°C
(Q10 of 4.4). Likewise, Bosch et al.
(Bosch et al., 1987) and
Stanwell-Smith and Peck (Stanwell-Smith
and Peck, 1998) found that the effect of temperature on
developmental rate in polar echinoderms was much stronger than for temperate
or tropical species: Q10 values of 10–15 between
–2°C to +2°C, far outside the normal biological range
(2–3). A counterexample is provided by the data reported in the previous
paper (Woods and Moran, 2008)
on another polar echinoderm, Sterechinus neumayeri, which showed that
it had a low Q10 (1.5).
How temperature effects on metabolism translate into temperature
sensitivity of O2 distributions in egg masses depends on an
assumption of the model – that diffusive transport of O2 is
indeed insensitive to temperature. This assumption is derived from theoretical
and empirical studies of molecules diffusing in substances like water. For
molecules in biological structures, such as egg mass gel, the temperature
sensitivity of diffusive transport also depends on temperature sensitivity of
structural properties. For egg masses of both temperate and Antarctic
Tritonia, we directly measured temperature effects on O2
diffusion coefficients (Woods and Moran,
2008), finding negligible increases across the same temperature
ranges that stimulated large increases in metabolic rates, thus confirming the
assumption of temperature-insensitivity of O2 transport. Here we
measure all remaining model parameters – embryo metabolic rates,
diffusion coefficients of O2 and radial profiles of O2
– at both ambient water temperature of McMurdo Sound (–1.8°C)
and slightly warmer temperatures (+1.5–2°C) in egg masses of the
Antarctic dendronotid nudibranch Tritonia challengeriana Bergh 1884.
Using these measurements as parameters, we show that the model (1) accurately
predicts radial O2 profiles in egg masses of T.
challengeriana and (2) explains the puzzling temperature insensitivity of
these profiles.
The second model test is interspecific. We recently published work on
O2 distributions in egg masses of Tritonia diomedea Bergh
1894 (Moran and Woods, 2007),
a temperate congener of T. challengeriana that inhabits subtidal
areas along the West Coast of North America. Between 12 and 21°C, embryo
metabolic rates rose approximately twofold (Q10 2.1–2.5). For
egg masses containing early-cleavage embryos, central O2 levels
were high (60–70% of air saturation) and only slightly affected by
temperature. In egg masses containing veligers, central O2 levels
were lower (0–40% of air saturation) and more sensitive to temperature
– approx. 30% of air saturation at 12°C and <10% at 21°C. The
gross morphology of T. diomedea masses has been described by several
authors (e.g. Hurst, 1967;
Kempf and Willows, 1977;
Lee and Strathmann, 1998), and
we add more detailed descriptions in this study.
Our measurements allow detailed physiological comparisons of Antarctic and
temperate egg masses. The model predicts that O2 constraints
observed T. diomedea (Moran and
Woods, 2007) should disappear at low temperatures in the Southern
Ocean. Specifically, it predicts that Antarctic egg masses will (1) have
higher O2 levels, (2) be thicker (i.e. larger radius), (3) contain
embryos at higher densities, and (4) exhibit tougher, less
O2-permeable egg-mass gel, without incurring an increased
O2 deficit relative to masses of their warmer-water relatives. Our
data supported only the first two predictions, although several additional
observations, particularly on embryo size and density, suggest functional
reasons for deviations from predictions 3 and 4.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). T. diomedea is subtidal and feeds on soft corals
(specifically Ptilosarcus gurneyi and Virgularia sp.)
(McDonald and Nybakken, 1980).
The biology of T. challengeriana is poorly known. Recent studies have
synonymized this species with Tritonia antarctica Bergh 1884
(Wägele, 1995;
Schrödl, 2003), and this
taxon has been reported from the Antarctic Peninsula, Patagonia, the Weddell
Sea, South Georgia, the Falkland Islands, and Signy Island
(Odhner, 1926;
Wägele, 1995;
Barnes and Bullough, 1996;
Schrödl, 2003). Food
sources of T. challengeriana are unknown, though it probably feeds on
octocorals (McClintock et al.,
1994; Barnes and Bullough,
1996). The developmental mode of T. challengeriana is
also unknown, but the large egg size and larval morphology reported here
suggest that it produces crawl-away juveniles or larvae with a short
dispersive period.
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) describes collection and holding methodology.
Egg mass morphology
Egg masses of the two species differed in size and overall morphology, and
measurement techniques varied accordingly. For whole egg masses of T.
challengeriana, which approximated long cylinders, we measured `height'
(the longest diameter) and `thickness' (perpendicular to the height) in two
ways: using calipers to directly measure intact egg masses (T.
challengeriana), and by sectioning egg masses and measuring parameters
from calibrated digital microphotographs.
For T. challengeriana, sections (Fig. 2) were cut with a razor blade along the `height' axis, perpendicular to the long axis of the egg mass cylinder. Sections were photographed using a Wild M5A stereomicroscope and Nikon Coolpix 900 digital camera. We measured embryo length (longest diameter), embryo width (perpendicular to longest diameter), egg volume (estimated from length, width, and assuming the shape of a prolate spheroid), capsule length and width, capsule volume (estimated as for embryos), egg mass `height' (longest diameter), mass `width' (perpendicular to longest diameter) and mass wall thickness. We also measured the average thickness of the outer mucous covering of masses (see Fig. 2). All microscopic measures were made in BioSuite (Olympus, Inc.) on calibrated micrographs. On a subset of egg masses we also measured embryo density by counting embryos in mass sections of known length. Segment volume was estimated by multiplying cross-sectional area by section length. Embryo density (mm–3) was calculated by dividing total number of embryos by section volume (mm3). For each mass, average embryo density was calculated from one to three sections.
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Embryo metabolic rates
Rates of O2 consumption by embryos of T. challengeriana
were measured using the end-point determination µBOD method
(Marsh and Manahan, 1999) with
some modification (see Moran and Woods,
2007). Encapsulated embryos were removed from egg masses, placed
in freshly filtered (0.2 µm pore diameter) seawater, and allowed to
acclimate to the experimental temperature for 2 h. They were then pipetted
into temperature-equilibrated glass microrespiration chambers (500–700
µl), and vials were capped and held at the experimental temperature for
5–14 h (total O2 depletion <20% of fully saturated
values). Subsequently, 300 µl of water from each vial was removed with
a temperature-equilibrated gas-tight syringe and injected into a respiration
cell (MC-100, Strathkelvin, Glasgow, UK) containing a Clark-style oxygen
microelectrode (Strathkelvin), kept at temperature with a recirculating water
bath. Per-embryo respiration rate was calculated as the slope of the
least-squares regression line of total respiration per vial plotted against
number of embryos per vial (Marsh and
Manahan, 1999).
Metabolism was measured at three developmental stages and two temperatures.
Because development in T. challengeriana is very long (
1 year;
H.A.W. and A.L.M., unpublished data), we used embryos from field-collected
masses assigned to one of three stages: early (gastrula), mid (unshelled,
ciliated veliger) and late (shelled, ciliated, and with a visible ciliated
foot). For all three stages we compared metabolic rates at two temperatures,
–1.5°C and +1.5°C. The low temperature is close to natural
temperatures (–1.8°C); the warmer temperature (+1.5°C)
represents summer temperatures animals might experience in more northerly
parts of the Antarctic peninsula (Palmer Station LTER sea temperature dataset,
http://pal.lternet.edu/).
Oxygen profiles in egg masses and capsules
PO2 in egg masses of T. challengeriana was
measured using Clark-style O2 microelectrodes (10, 25 or 50 µm
tips; Unisense, Aarhus, Denmark) connected to a picoammeter (model PA2000,
Unisense). Electrodes were calibrated, at experimental temperature, before and
after each set of measurements in seawater bubbled with air or pure
N2. Calibration water was held at constant temperature with a
water-jacketed calibration cell connected to a recirculating water bath.
Picoammeter output was logged once per second. Water temperature was also
logged using a T-type thermocouple connected to a thermocouple meter (TC-1000,
Sable Systems, Las Vegas, NV, USA). Thermcouples were calibrated in a seawater
ice bath (–1.9°C). Pieces of egg masses, or individual egg capsules
(in general, each capsule contained a single embryo), were submerged and
PO2 values were measured as described
(Moran and Woods, 2007).
Paired pieces of egg mass (several cm long, cut ends tied with dental
floss) were equilibrated overnight in air-bubbled seawater at either
–1.5 or +2.0°C (N=7 pairs). Subsequently, pieces were
transferred to the temperature-controlled stage described
(Moran and Woods, 2007) and
pinned onto a piece of Nitex mesh. A micromanipulator was used to position an
oxygen electrode at the egg mass surface, and the tip was advanced in
increments of 0.5 mm to the center of the mass. In separate experiments,
individual egg capsules that had been removed from egg masses were pierced
with a 10 µm tip electrode and lifted from the substrate (to avoid
substrate-induced boundary layers).
Modeling oxygen profiles in egg masses of T. challengeriana
Measurements of egg-mass morphology, embryo metabolic rates, and
O2 diffusion coefficients were used to parameterize the model
developed in the preceding paper (Woods
and Moran, 2008). Our interests were primarily in determining how
similar modeled radial profiles were to measured profiles across temperatures.
All modeling was done in the R statistical package (v2.3.1), as described
previously.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Egg mass morphology – T. diomedea
Morphological data (Table 1)
were consistent with previous descriptions
(Hurst, 1967;
Strathmann, 1985;
Lee and Strathmann, 1998).
Overall, T. diomedea had narrower egg cords than T.
challengeriana. Mass coverings of T. challengeriana were tough
and translucent whereas those of T. diomedea were transparent and
jelly-like. T. diomedea also had substantially smaller embryos, many
more embryos per capsule, and much higher embryo densities than T.
challengeriana (Table
1).
Embryo metabolic rates – T. challengeriana
Metabolic rates increased with both embryo age and temperature
(Fig. 3). O2
consumption ranged from 3.4–51.1 pmol embryo–1
h–1 and respiration rates were highly temperature-sensitive;
for the three developmental stages we examined, Q10 values of
respiration rate ranged from 9.6 to 30.0, depending on developmental stage.
Respiration rates of T. diomedea are given elsewhere
(Moran and Woods, 2007).
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).
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;
Yanigasawa, 1975;
Palumbi and Johnson, 1982).
Under all combinations of embryo age and temperature, simulated profiles
showed high levels of O2 throughout the egg masses
(Fig. 5), similar to observed
radial profiles (Fig. 4).
Early- and mid-stage embryos in colder conditions had almost no central
O2 depression, and the warmer conditions led to only slight
additional O2 depression. Late-stage embryos showed a larger but
still modest effect of temperature.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Intraspecific effects of warming on oxygen in egg masses
Metabolic rates of Antarctic species can be quite sensitive to temperature
(Bosch et al., 1987;
Stanwell-Smith and Peck, 1998;
Peck and Prothero-Thomas,
2002), though the degree of sensitivity varies among species. The
strong effect of temperature on O2 consumption by embryos of T.
challengeriana – coupled to temperature insensitivity of
O2 diffusion coefficients
(Woods and Moran 2008) –
suggested that egg-mass O2 profiles should be affected by even
small changes in temperature. This prediction, however, was refuted by both
direct measurement (Fig. 4) and
model simulation (Fig. 5). A
resolution can be found in the very low metabolic density (per embryo
metabolic rate x embryo density) of T. challengeriana egg
masses. In particular, low metabolic density gave trivially small
O2 drawdown under cold (natural) conditions, and even large
factorial increases in O2 consumption caused little additional
drawdown (Fig. 5). An
implication is that increasing sea temperatures could increase development
rates without offsetting costs from hypoxia. For example, if metabolic rate
and development rate are coupled, a 3°C rise in temperature could halve
time to hatching. Whether this increase would be beneficial is unclear;
generation times would shorten but shifts in hatch timing could result, e.g.
in mismatches with seasonal food availability
(Rivkin 1991;
Both et al., 2006).
Interspecific differences between Antarctic and temperate Tritonia species
The temperature difference between the Antarctic site (shallow subtidal
near McMurdo Station) and the temperate site (Friday Harbor Labs) is
10–14°C. The model predicts that, all else being equal, Antarctic
egg masses will have higher O2 levels, be thicker, contain embryos
at higher densities, and exhibit tougher egg-mass gel that is less permeable
to O2, without incurring increased O2 deficits. Only two
of these four predictions were supported.
The supported predictions were O2 levels in the egg mass and egg
mass size. At ambient environmental temperatures (–1.5°C), egg
masses of T. challengeriana contained high O2 levels
(Fig. 4) across all stages of
development. Warming induced slightly steeper O2 gradients, but
levels never dropped below 17 kPa (75% of air saturation). By contrast,
warming egg masses of the temperate T. diomedea gave areas of extreme
hypoxia and anoxia (Moran and Woods,
2007). High O2 in egg masses of T.
challengeriana were attributable to moderate per-embryo O2
demand at Antarctic temperatures coupled to very low embryo density.
Supporting the prediction that Antarctic egg masses should be large, we found
that egg masses of T. challengeriana were on average twice the
diameter of those of T. diomedea (radii of 1.5 and 0.8 mm,
respectively). This pattern is consistent with the phenomenon of polar
gigantism (Chapelle and Peck,
1999), and may be related to release from O2
constraints.
Support for both predictions – higher O2 levels and larger
egg-mass size – suggests, however, that size of Antarctic masses has not
increased to the extent that would be permitted by relief from O2
constraints. The model offers a way to evaluate this idea quantitatively. For
example, the model indicates that an egg mass of T. challengeriana
containing mid-stage embryos could be sixfold thicker (18 mm) and still have
some O2 at its center. Under conditions of higher O2
demand, i.e. late stage embryos at +1.5°C, egg masses could still be two-
to threefold thicker before the onset of central anoxia. At their actual
sizes, therefore, it appears that natural masses are `overconstructed' with
regard to O2 supply to embryos (see also
Seymour and Bradford, 1995).
Several processes may explain this pattern. First, laboratory experiments were
performed in full O2 saturation with stirring; in the field,
O2 concentrations and flow may be lower. Respiration by other
neighboring organisms may draw local oxygen levels down further. Direct field
measurements of O2 concentration in egg masses in situ
would constitute a good test. Second, egg-mass cords often fold back on
themselves or are laid in closely apposed spirals (see
Fig. 1). Third, Antarctic
embryos themselves may be more sensitive to low O2 availability
than are temperate embryos. Fourth, morphological constraints in the adult
reproductive tract may preclude generating larger-diameter egg masses. None of
these possibilities has been tested.
Now consider the unsupported predictions, embryo density and gel
impermeability. Contrary to expectation, we found that embryos in Antarctic
species were 23-fold less dense than their temperate congener (9.2
embyros mm–3 compared with 215.2 embryos
mm–3 for T. diomedea). A likely proximate
explanation stems from embryo sizes of the two species. Embryos of T.
challengeriana were >32-fold larger (by volume) than embryos of T.
diomedea, and single embryos were contained in very large (500 µm
diameter) egg capsules. Masses of T. challengeriana also had stiffer,
thicker (183 µm) egg-mass walls, and tightly packed capsules within.
We calculated the packing density of embryos by measuring the volume of the
internal cavity of each mass and the volume of embryos contained in it, and
found that T. challengeriana capsules filled an estimated 83.0%
(±8.0%) of available space. The theoretical maximum packing of jammed
disordered ellipsoids is 74% (Donev
et al., 2004); thus, while capsules were somewhat flexible and
could clearly be packed at high densities, embryos could not occur at much
higher densities without reduction in capsule size. The functional role of
large capsules is unknown, but their size places a limit on embryo density
that is lower than the theoretical limit imposed by O2
supply–demand dynamics in our model.
The second prediction, that Antarctic egg masses would use O2
surplus to construct especially tough egg-mass gel that was less
oxygen-permeable, was also rejected. The logic was that (1) predation is
important in Antarctic ecosystems; (2) slow-developing embryos would need
substantial protection, i.e. tough egg-mass walls, if they were to survive to
hatching; and (3) construction of tough walls would result in reduced
permeability to O2. Egg mass walls of T. challengeriana
indeed appeared tougher than those of T. diomedea. However, direct
measurement of O2 diffusion coefficients (D) in intact egg
masses of T. challengeriana
(Woods and Moran, 2008) showed
that D was almost as high as in pure seawater. Egg-mass wall
toughness may be irrelevant to predation risk if masses are chemically
defended, as some Antarctic adult nudibranchs appear to be
(Bryan et al., 1998).
Physiology of Antarctic egg masses: conclusions and caveats
Antarctic egg masses were thicker (2x) than those of a temperate
congener and had high O2 levels throughout, at least under
laboratory conditions. In addition, embryos in the Antarctic masses were much
larger (32x) than the temperate congener. It is possible that large
embryo size is facilitated by release from O2 constraints. In this
aspect, our focus on egg-mass size may be too narrow; perhaps the appropriate
organizational level is on embryos and the O2 gradients surrounding
them (Seymour and White,
2006). We are presently developing new analyses to evaluate this
idea.
An obvious caveat is that our conclusions are drawn in part from a
two-species comparison, so that firm evolutionary conclusions are impossible
(Garland and Adolph, 1994). We
focused instead on developing detailed physiological and morphological
datasets grounded in a modeling context. Our evolutionary conclusions are thus
subject to additional, ongoing studies of larger species sets.
A second caveat concerns implicit connections between O2 and
egg-mass structure and function. Other factors unrelated to O2 may
also be at work. For example, predation plays an important role in structuring
Antarctic benthic ecosystems (Dearborn,
1977; Dayton et al.,
1994; McClintock,
1994; McClintock et al.,
2005). High predation rates on early life-history stages are
thought to select against strategies in which reproductive effort is packaged
into few, large clutches rather than more numerous, smaller ones
(Smith and Fretwell, 1974).
Thus, production of thick masses in the Antarctic, which our model suggests is
physiologically possible, might be disadvantageous because of the high
probability that a parent's entire reproductive output could be consumed by a
single predator (although parents could avoid this problem by producing short,
thick masses). Likewise, if predation rates on Antarctic masses are high, any
reduction of internal O2 concentrations may be detrimental if it
prolongs development and increases vulnerability to predation.
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Acknowledgments |
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