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First published online December 16, 2008
Journal of Experimental Biology 212, 71-77 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.020552
Habitat temperature is an important determinant of cholesterol contents in copepods
1 Department of Biological Sciences, Ohio University, Athens, OH 45701,
USA
2 Mount Desert Island Biological Laboratory, Salisbury Cove, ME 04672, USA
* Author for correspondence (e-mail: hassett{at}ohiou.edu)
Accepted 2 October 2008
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Summary |
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Key words: cholesterol, copepod, zooplankton, temperature adaptation, temperature acclimation
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INTRODUCTION |
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),
limits membrane permeability (Kroes and
Ostwald, 1971) and imparts a suitable working environment for
membrane proteins (Yeagle et al.,
1988). Despite the physicochemical influences of cholesterol, its
distribution in biological membranes is far from homogenous. Cholesterol is
primarily localized to the plasma membrane
(Lange et al., 1989). Even
within the plasma membrane cholesterol associates with sphingolipids and can
concentrate in microdomains, including membrane rafts and caveolae, providing
a platform to organize glycosylphosphatidylinositol-anchored proteins
(Sengupta et al., 2007).
Because of its integral roles in biological membranes, cholesterol is
considered a key constituent for animal growth, and requirements for
cholesterol are likely to be driven largely by its contents in biological
membranes. Crustaceans, like many other invertebrates, are considered unable
to synthesize cholesterol de novo
(Goad, 1981) and therefore
must rely on exogenous sources of sterol for somatic and reproductive growth.
This inability to synthesize cholesterol may be particularly challenging for
many species of copepods since the sterol content and composition of their
phytoplankton diet can vary greatly (e.g.
Ballantine et al., 1979;
Patterson et al., 1993;
Patterson et al., 1994;
Barrett et al., 1995;
Véron et al., 1996).
Cholesterol has been shown, in fact, to be a limiting factor in the growth of
several crustaceans (Von Elert et al.,
2003; Martin-Creuzburg and Von
Elert, 2004; Hassett,
2004). Recently, we have shown that both egg production and
viability are enhanced in copepods fed a diatom diet supplemented with
cholesterol, while at the same time cholesterol contents of biological
membranes are unaffected (Hassett,
2004; Crockett and Hassett,
2005). These results demonstrate that assimilated cholesterol
(beyond what is present in the phytoplankton diet) is utilized for
reproductive growth and that cholesterol levels in membranes are regulated,
presumably in order to preserve membrane physical properties and function.
Cholesterol contents of organisms that live at different body temperature
may require fine-tuning in order to stabilize physical properties of membranes
(Hazel and Williams, 1990;
Crockett, 1998). Like low
temperature, cholesterol orders fluid-phase membranes, leading one to predict
that cholesterol levels rise with temperature in order to counter the
fluidizing influence of elevated temperatures. Temperature has been shown to
affect membrane lipid composition and physical properties in a variety of
crustaceans including crayfish (Pruitt,
1988), amphipods (Lahdes et
al., 2000), crabs (Cuculescu
et al., 1995) and copepods
(Farkas et al., 1988), yet
relatively little work has examined more specifically how cholesterol levels
in crustaceans may be affected by temperature. Since copepods are among the
most abundant animals on earth, and play a central role in marine foodwebs
(Mauchline, 1998), it is
important to understand how temperature may influence the copepod's
requirements for cholesterol.
To determine whether and how cholesterol contents vary with temperature in copepods, we surveyed a range of species within the crustacean subclass Copepoda (order Calanoida). For temperature acclimations, several oceanic and inshore species were used. We examined further the relationship between cholesterol content and habitat temperature by comparing the cholesterol content in nine species of copepods, representing six families, whose maximum habitat temperatures and temperature tolerances span a range of at least twofold. We also evaluated the influence of acclimation temperature on the level of dietary cholesterol necessary to achieve maximum growth.
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MATERIALS AND METHODS |
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Animals used in acclimations were held in one-liter containers for
7–10 days at high (16–25°C) and low (6°C) temperatures in
two refrigerators equipped with BOD-cubator temperature controls (N-Con
Systems, Crawford, GA, USA). Temperatures were selected to reflect the
temperature range of the species in the field, and so were not identical for
each species. In addition to acclimation at cold temperature (6°C),
Aeartia hudsonica and Temora longicornis were acclimated at
18°C, the more warm-tolerant A. tonsa and Eurytemora
affinis at 22°C and 25°C, respectively. C. finmarchicus
CVs (fifth copepodite stage) were acclimated at 6°C and 16°C, whereas
eggs were collected from females acclimated at 6°C and 12°C since egg
production was very low at 16°C. Bradley
(Bradley, 1978) found that
E. affinis acclimated measurably in 3 h, and completely within
2–4 days, so the 7–10 days acclimation period should allow
sufficient time to achieve full acclimation. Experiments with C.
finmarchicus were conducted mid-to-late June, T. longicornis and
A. hudsonica in early July, A. tonsa in late July, all in
2005, and E. affinis in early July 2007. These time periods
correspond to periods of high abundance of these species in the plankton.
Animals were fed daily with stabilized, concentrated
Tetraselmis–Nannochloropsis cultures (Reed
Mariculture, Campbell, CA, USA) and water was changed every other day.
Although the sterol composition of the
Tetraselmis–Nannochloropsis diet is not known with
certainty, cholesterol is the dominant sterol in Nannochloropsis
(Patterson et al., 1994), and
is abundant, and sometimes dominant, in different strains of
Tetraselmis (Patterson et al.,
1993). Other sterols are dominated by 24-methylenecholesterol and
24-methylcholesterol (Tetraselmis) and 24-ethylcholesterol
(Nannochloropsis), which are 
5 sterols that may be
de-alkylated to cholesterol (Prahl et al.,
1984). At the end of the acclimations, animals were concentrated,
sorted for dead or moribund individuals, separated on a 60 µm Nitex screen,
and frozen over liquid nitrogen for later analysis of cholesterol and protein
content.
For the growth rate experiment Eurytemora affinis females and
males were held in 20 liter carboys and fed for 5 days on the
Tetraselmis–Nannochloropsis culture. Adults were then
concentrated and transferred to a clean carboy with filtered seawater. Animals
were held overnight and newly hatched nauplii were separated and raised in 250
ml containers in two small, Peltier-cooled incubators (Incufridge;
Revolutionary Science Inc, Lindstrom, MN, USA) at 6°C and 25°C at 20
p.p.t. salinity, with one incubator for each temperature. Animals for the
growth experiment were fed the cyanobacterium Synechococcus bacillus
(CCMP 1261, cell dimensions of 4–8 µmx2 µm) supplemented
with cholesterol over a range of concentrations. Cultures were obtained from
the Center for the Culture of Marine Phytoplankton, Bigelow Laboratory,
Boothbay Harbor, MA, USA) and maintained on K medium
(Keller et al., 1987) at
20°C. S. bacillus was added at approximately 500 µg
cholesterol l–1, estimated from literature values of
cholesterol per cell (Liu et al.,
1999). This food level is in excess of saturating levels of
300µgcholesteroll–1
(Barthel, 1983). The S.
bacillus culture was supplemented at 0.01, 0.05, 0.1, 0.25 and 0.5 µg
cholesterol l–1 (=0.005–0.25% cholesterol by weight),
with two replicates at each concentration. Preliminary experiments indicated
that no growth occurred on a S. bacillus diet in the absence of
supplementation, so a pure cyanobacterium diet was not used in the subsequent
experiment. In addition, the preliminary experiment indicated that growth
rates reached a maximum at lower cholesterol concentrations at 6°C, so a
treatment at 0.025 µg cholesterol l–1 was substituted for
the 0.25 µgl–1 in the cold treatment. The use of a
cyanobacterium (with its characteristic absence of cholesterol) allows control
of the cholesterol content without the confounding factor of temperature,
which can alter sterol composition. The diet was supplemented with cholesterol
using a modification of the method of Von Elert et al.
(Von Elert et al., 2003).
Cholesterol was dissolved in ethanol using ultrasonic homogenization (50 W
disintegrator with a 3 mm diameter probe at full power for 30 s). After adding
the cholesterol to an algal suspension (to yield a supplementation of
0–0.25% of algal dry mass), the suspension was stirred on a rotating
platform for 30 m to incorporate the cholesterol.
An initial subsample was taken for size distribution at the start of the experiment. Subsamples were taken after 4 days and 45–90 individuals were digitally photographed for measurement of prosome length. Images were analyzed with ImageJ v. 1.38 (NIH public domain software; http://rsb.info.nih.gov/ij/), using a stage micrometer for calibration, and growth rate calculated as length increment (µm) day–1.
Sample preparation and cholesterol analyses
To expand the scope of the work to include larger numbers of species and
sample sizes, whole-animal cholesterol contents were measured. Animals were
homogenized, prior to storage in liquid nitrogen (Acartia hudsonica,
Calanus finmarchicus CV) or after freezing (Acartia tonsa, C.
finmarchicus eggs, Temora longicornis, Eurytemora affinis, Calanus
glacialis, Paraeuchaeta norvegica, Centropages spp.), using a 100 µl
ground-glass homogenizer with 25 mmol l–1 Hepes (pH 7.6) as
2–5% (w/v). Animals were initially pooled to determine wet mass, and
then the sample was subdivided to yield homogenates of approximately 2 mg wet
mass ml–1. For most species, each subsample consisted of
10–50 individuals. The exceptions were the large P. norvegica
and C. glacialis, for which each sample consisted of two individuals.
Levels of cholesterol were determined in triplicate on each subsample using
the cholesterol oxidase-based Amplex Red assay (Invitrogen, Carlsbad, CA, USA)
with a PerkinElmer LS50B fluorometer equipped with a microplate reader. The
addition of cholesterol esterase in the assay allows detection of cholesterol
esters as well. However, only free cholesterol (e.g. membrane-associated
cholesterol) was detectable using this procedure since cholesterol esters were
not at measurable levels. Cholesterol contents were normalized to protein, and
protein contents were measured using the Pierce Micro BCA assay
(Smith et al., 1985) with
bovine serum albumin as standard.
Determination of habitat temperatures
Determining temperature ranges for marine zooplankton can be problematic,
as temperatures vary seasonally, geographically and vertically. Individuals
may be present well outside their seasonal peak abundances and species may be
advected into temperature regimes outside their preferred range. Temperature
tolerances determined experimentally can be difficult to compare between
studies because of methodological differences. To minimize these limitations,
we used two measures to characterize the temperature range of a species, (1)
an estimate of maximum habitat temperature the species is likely to encounter
in its normal range and (2) experimentally derived temperature tolerance.
Temperature tolerance data for T. longicornis, Centropages hamatus
and C. typicus are from Halsband-Lenk et al.
(Halsband-Lenk et al., 2002),
Calanus glacialis and C. finmarchicus from Hirche
(Hirche, 1987) and E.
affinis from Bradley (Bradley,
1976). Bradley
(1976) used a novel,
non-destructive bioassay that is not directly comparable to the others, but
does support the high temperature tolerance of E. affinis. Maximum
habitat temperatures were estimated for Acartia tonsa and A.
hudsonica from Sullivan and McManus
(Sullivan and McManus, 1986)
and for Temora longicornis from Halsband-Lenk et al.
(Halsband-Lenk et al., 2002).
C. finmarchicus is often abundant in the 0–50 m depth range in
the Gulf of Maine (Clarke and Zinn,
1937) and the maximum habitat temperature for this depth was taken
from seasonal data of Gulf of Maine temperatures
(Mountain and Jessen, 1987).
Paraeuchaeta norvegica, a vertically migrating predatory copepod,
inhabits the deep water of the Gulf of Maine and its maximum habitat
temperature was assumed to be the maximum observed in the 50–100 m depth
range. Temperatures at low tide in the estuary where E. affinis was
collected were measured directly in late July. Calanus glacialis is
an Arctic shelf copepod (Hirche and
Kwasniewski, 1997) and is rare in the Gulf of Maine. It has a more
northerly distribution than C. finmarchicus
(Fleminger and Hulsemann,
1977).
Statistical analyses
A two-way ANOVA and a Bonferroni post-hoc test was used to
determine the effect of acclimation temperature and species on cholesterol
content, as well as effect of acclimation temperature and ontogenic stage
(Calanus CV copepodites and eggs). Correlation analyses were used to
assess the relationship between cholesterol content and habitat temperature
(as indicated by maximum habitat temperature or temperature tolerance).
P<0.05 was considered a statistically significant result.
Statistical analyses were performed with Graphpad Prism 5.0 (Graphpad
Software, San Diego, CA, USA).
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RESULTS |
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DISCUSSION |
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). C.
glacialis contained only 4.8 µg cholesterol mg–1
protein whereas C. finmarchicus (collected and acclimated at 6°C)
has 6.2 µg cholesterol mg–1 protein. Acartia
tonsa is distributed widely from the Gulf of Mexico to the Saint Lawrence
River estuary, whereas A. hudsonica has the more northerly
distribution, extending from Chesapeake Bay to Hudson Bay
(Gerber, 2000). Similarly, we
observed higher cholesterol contents in A. tonsa than in A.
hudsonica. Centropages typicus has a broad temperature tolerance enabling
it to extend its distribution from the tropics to the Subarctic (where it
overlaps the more northerly Centropages hamatus)
(Halsband-Lenk et al., 2002).
We found the species with the more common occurrence in warmer waters (C.
typicus) to possess nearly 1.5-times higher levels of cholesterol than
its congener (C. hamatus). Tortanus discaudatus, with its
relatively low cholesterol contents (4.7 µg cholesterol
mg–1 protein), may be somewhat anomalous as this species is
found along the entire Atlantic coast and into the Gulf of Mexico. T.
discaudatus, however, is a late winter/early spring dominant species off
the coast of Maine (Gerber,
2000), and its low cholesterol may correspond with its dominance
in the colder months.
By contrast, changes in cholesterol content in response to acclimation
temperature (a proxy for more short-term changes in temperature) do not
present such a strong trend among species of copepods, or in other animals.
Our taxa-specific results with temperature acclimations are similar to mixed
results from previous studies in fish and crabs (e.g.
Crockett and Hazel, 1995;
Labbe et al., 1995;
Robertson and Hazel, 1995;
Cuculescu et al., 1995).
Acclimatory responses in cholesterol contents are more likely to depend on the
species in question (this study), particular tissues (e.g.
Robertson and Hazel, 1995;
Labbe et al., 1995;
Cuculescu et al., 1995), the
specific membrane being analyzed (Crockett
and Hazel, 1995), and even the lipid microdomain within the
membrane (Zehmer and Hazel,
2003). When taken together, these studies indicate that changes in
body temperature over timescales of days and/or weeks may, but also may not,
result in adjustments of cholesterol levels. In the instance when cholesterol
content did increase with warm acclimation (Calanus finmarchicus),
the response was consistent with the role of cholesterol in modulating
membrane fluidity.
It is possible that insufficient time was allowed for acclimation of
membrane cholesterol content to occur in Acartia spp.,
Temora and Eurytemora, which were acclimated for 7 days.
However, Bradley (Bradley,
1978) determined that full temperature tolerance in Eurytemora
affinis occurred in 3–4 days, and 7 days represents a significant
portion of the development time of these animals (approximately 15–25
days) (Mauchline, 1998). Since
Calanus finmarchicus demonstrates an acclimation response and has a
development time two to three times longer than the other species used in this
study, we believe it is unlikely that longer acclimation times would yield
different results.
Not only is the association between cholesterol content and habitat temperature more well-defined than that of acclimation temperature, the absolute differences in cholesterol contents are also much greater for copepods adapted to various thermal regimes than differences when copepods are acclimated to cold and warm temperatures. For the species sampled, the highest and lowest maximum habitat temperatures (or temperature tolerances) differ by a factor of at least two, and cholesterol contents follow a similar trajectory – species living at somewhat warmer temperatures (e.g. Acartia tonsa, Centropages typicus) have twice the cholesterol content of those species commonly found in cold-water habitats (e.g. Euchaeta norvegica and Calanus glacialis). These very substantive differences in cholesterol contents stand in sharp contrast to those we observed with the temperature acclimations. Although the temperatures used in laboratory acclimations have a range of 2.5- to 4-fold (i.e. at least as great as the range of habitat temperatures for the species sampled), either there is no significant effect on cholesterol content (Acartia spp., Temora and Eurytemora), or only a relatively modest (10–20%) change occurs (Calanus finmarchicus).
Cholesterol content appears to be subject to habitat temperature in another
crustacean group, and in animals more generally. In the warm-tolerant
cladoceran, Daphnia magna Straus, cholesterol content is
significantly higher (<18 µg cholesterol mg–1 protein;
R.P.H. and E.L.C., unpublished) than in any of the copepods measured in the
present study. By contrast with D. magna, the cold-temperate
cladoceran Pleopis polyphemoides Leuckart has cholesterol contents
that are only about half that of D. magna (8.5 µg cholesterol
mg–1 protein; R.P.H. and E.L.C., unpublished). The suggestion
that body temperature underlies, at least in part, the cholesterol content of
animals has been made previously
(Robertson and Hazel, 1997).
Using data compiled from several studies, including those of two ectotherms
(trout, tortoise), a bird and several mammals, the authors suggest the higher
levels of cholesterol in membranes from endotherms (compared with those levels
found in ectotherms) counter the fluidizing effects of warm body temperatures.
Although in the present work whole-animal cholesterol contents were measured,
it is probable that the cholesterol we have quantified largely reflects
membrane cholesterol since in an earlier study
(Crockett and Hassett, 2005)
similar trends were obtained for crude homogenates and biological membranes.
Taken together, the data from closely related crustaceans (current study) with
those reported from vertebrates, provide compelling evidence for cholesterol's
stabilizing role at different body temperatures.
Elevated cholesterol levels in copepods may enable these animals to extend
their range into warmer habitats since animals with the greatest temperature
tolerances possess the highest cholesterol contents. Cholesterol, however, may
also protect ectothermic animals against cold shock injury, since modulating
the cholesterol content by dietary means confers additional protection in
Drosophila (Shreve et al.,
2007). Cholesterol could also play a part in temperature
tolerances of different populations within a species. Although each copepod
species used in the current study is likely to represent a single population,
population-level differences in temperature tolerances of copepods have been
documented [Acartia tonsa
(González, 1974);
Centropages typicus
(Halsband-Lenk et al., 2002);
as well as the cladoceran Daphnia
(MacIsaac et al., 1985)].
Although we do not have data on cholesterol content of copepod populations in
waters warmer than the Gulf of Maine, given the trends we observe among
species, we might expect population-level differences in cholesterol content
as well. It is also worth noting that egg development rates of Calanus
finmarchicus differ between samples taken from a Norwegian fjord during
two different years yet raised at the same low temperature (Pederson and
Tande, 1992). The authors attribute the differences to markedly different
temperatures during the overwintering period between the two years
(1–1.5°C in 1980 vs 4–5°C in 1989), and speculate
that the overwintering temperature experienced by C. finmarchicus
could affect the temperature tolerance of the offspring. Our own data indicate
that the cholesterol contents of both CV copepodites (the overwintering stage)
and eggs of C. finmarchicus change during temperature acclimation,
providing at least a partial physiological basis for these observations.
Cholesterol feeding, growth and temperature
Cholesterol supplementation enhances growth of Eurytemora affinis
at either cold (6°C) or warm (25°C) temperature with a higher
incipient limiting concentration at the warmer temperature. Although
temperature effects were not determined, a similar enhancement of growth rates
was also observed in the cladoceran Daphnia galeata when the
cyanobacterial diet was supplemented with cholesterol
(Von Elert et al., 2003). Why
are growth rates limited at a higher cholesterol concentration in
warm-acclimated Eurytemora? Since cholesterol contents of E.
affinis acclimated to 6° and 25°C are comparable
(Fig. 1C), the differences in
the growth curves are not due to different body cholesterol content. It is
quite possible that at 6°C Eurytemora is temperature limited
under these food conditions, and only when cholesterol content is extremely
low does sterol limitation supercede temperature limitation. Thus an increase
in temperature from 6°C to 25°C at other cholesterol concentrations
would shift the animals from temperature-limited to sterol-limited growth.
Changes in the incipient limiting concentration may also be affected by
assimilation and/or processing of cholesterol. Higher growth rates at warm
temperatures necessitate increased demand for cholesterol along with other
elemental nutrients (e.g. C, N, P). Limiting concentrations of cholesterol
relative to these other nutrients should not change, unless these different
dietary components are assimilated or processed differently. If cholesterol is
assimilated less efficiently than other potentially limiting nutrients, the
incipient limiting concentration may increase with ingestion rate, since an
excess of the more efficiently assimilated nutrients will tend to
accumulate.
Although the literature is limited, there is evidence that phytosterols are
assimilated less efficiently than other components of a copepod's diet.
Phytosterol assimilation in Calanus helgolandicus ranges from
negligible up to nearly 60% depending upon the phytosterol in question
(Harvey et al., 1987). By
contrast, fatty acids are assimilated at over 90% efficiency. In the
cladoceran Daphnia galeata growth rates on diets supplemented with
preferred phytosterols (e.g. stigmasterol, sitosterol, ergosterol) are
comparable to those supplemented with cholesterol, whereas supplementation
with other sterols (dihydrocholesterol, lanosterol) yield poor growth rates
(Martin-Creuzburg and Von Elert,
2004).
The effect of environmental conditions (i.e. food concentration and
quality, temperature and salinity) on assimilation of sterols in copepods is
not well understood. Processing of dietary phytosterols will involve both
assimilation and metabolic de-alkylation, both of which can vary
(Knauer et al., 1999;
Harvey et al., 1987;
Teshima, 1971). Cholesterol
and phytosterols are taken up directly by midgut cells in insects
(Canovoso et al., 2001;
Jouni et al., 2002) and
de-alkylation of phytosterols then takes place within the midgut cells, rather
than in the gut lumen. Sterol assimilation in Calanus helgolandicus
is influenced by food concentration, with higher assimilation efficiencies at
low food concentrations (Harvey et al.,
1987), a pattern also observed by Landry et al.
(Landry et al., 1984) for
carbon and nitrogen assimilation efficiency in C. pacificus.
Differences in assimilation efficiency may be ascribed to differences in
residence time in the gut or in rates of uptake into gut cells. Gut residence
times of copepods generally are inversely related to food concentration
(Dagg and Walser, 1987;
Besiktepe and Dam, 2002;
Tirelli and Mayzaud, 2005)
although some studies have not found such a relationship (e.g.
Ellis and Small, 1989). Longer
gut residence times may allow more efficient assimilation of phytosterols
observed in C. helgolandicus at low food concentrations
(Harvey et al., 1987),
particularly if phytosterols are more difficult to assimilate. Gut residence
times also are inversely related to temperature
(Dam and Peterson, 1988), and
similarly may lead to less efficient assimilation of cholesterol at high
temperatures due to rapid gut transit, consistent with results observed with
Eurytemora affinis (Fig.
2). One might then expect sterol limitation to be more pronounced
when some combination of low algal sterol content, warm temperatures, and high
algal concentrations occur.
Conclusions
The positive relationship in copepods between cholesterol content and
habitat temperature points to a significant role for temperature in setting
cholesterol levels in animals more generally than has been previously
recognized. Our results, combined with comparisons made for ectothermic and
endothermic vertebrates (Robertson and
Hazel, 1997), are strong evidence for cholesterol stabilizing
membranes over a wide range of body temperatures. For copepods, and many
invertebrates that must acquire sterol exogenously, an animal's demand for
dietary sterol is likely to vary with temperature. Given the taxa-specific
responses to temperature acclimation, however, it is not possible to
generalize about how temperature changes over the short-term affect
cholesterol content, and hence cholesterol demand, in copepods. Although
elevated temperature increases the proportion of dietary cholesterol needed to
maximize growth rates in Eurytemora affinis, the cholesterol content
of Eurytemora is not altered, indicating that either growth rates at
low temperature are temperature limited except at very low cholesterol
concentrations, or cholesterol assimilation and/or turnover is(are)
temperature-dependent process(es).
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Ballantine, J. A., Lavis, A. and Morris, R. J. (1979). Sterols of the phytoplankton: effects of illumination and growth stage. Phytochemistry 18,1459 -1466.[CrossRef]
Barrett, S. M., Volkman, J. K., Dunstan, G. A. and Leroi, J. M. (1995). Sterols of 14 species of marine diatoms (Bacillariophyta). J. Phycol. 31,360 -369.[CrossRef]
Barthel, K. (1983). Food uptake and growth efficiency of Eurytemora affinis (Copepoda: Calanoida). Mar. Biol. 74,269 -274.[CrossRef]
Besiktepe, S. and Dam, H. G. (2002). Coupling of ingestion and defecation as a function of diet in the calanoid copepod Acartia tonsa. Mar. Ecol. Prog. Ser. 229,151 -164.[CrossRef]
Bloom, M. and Mouritsen, O. G. (1988). The evolution of membranes. Can. J. Chem. 66,706 -712.[CrossRef]
Bradley, B. P. (1976). The measurement of temperature tolerance: verification of an index. Limnol. Oceanogr. 21,596 -599.
Bradley, B. P. (1978). Increase in the range of
temperature tolerance by acclimation in the copepod Eurytemora affinis.Biol. Bull. 154,177
-187.
Canovoso, L., Jouni, Z. E., Karnas, K. J., Pennington, J. E. and Wells, M. A. (2001). Fat metabolism in insects. Annu. Rev. Nutr. 21,23 -46.[CrossRef][Medline]
Clarke, G. L. and Zinn, D. J. (1937). Seasonal
production of zooplankton off Woods Hole with special reference to Calanus
finmarchicus. Biol. Bull.
73,464
-487.
Conover, R. J. (1988). Comparative life histories of the genera Calanus and Neocalanus in high latitudes of the northern hemisphere. Hydrobiologia 167/168,127 -142.[CrossRef]
Crockett, E. L. (1998). Cholesterol function in plasma membranes from ectotherms: membrane-specific roles in adaptation to temperature. Am. Zool. 38,291 -304.
Crockett, E. L. and Hazel, J. R. (1995). Cholesterol levels explain inverse compensation of membrane order in brush border but not homeoviscous adaptation in basolateral membranes from the intestinal epithelia of rainbow trout. J. Exp. Biol. 198,1105 -1113.[Medline]
Crockett, E. L. and Hassett, R. P. (2005). A cholesterol-enriched diet enhances egg production and egg viability without altering cholesterol content of biological membranes in the copepod Acartia hudsonica.Physiol. Biochem. Zool. 78,424 -433.[CrossRef][Medline]
Cuculescu, M., Hyde, D. and Bowler, K. (1995). Temperature acclimation of marine crabs: changes in plasma membrane fluidity and composition. J. Therm. Biol. 20,207 -222.[CrossRef]
Dagg, M. J. and Walser, W. E. (1987). Ingestion, gut passage, and egestion by the copepod Neocalanus plumchrus in the laboratory and in the subarctic Pacific Ocean. Limnol. Oceanogr. 32,178 -188.
Dam, H. G. and Peterson, W. T. (1988). The effect of temperature on the gut clearance rate constant of planktonic copepods. J. Exp. Mar. Biol. Ecol. 123, 1-14.[CrossRef]
Ellis, S. G. and Small, L. F. (1989). Comparison of gut evacuation rates of feeding and non-feeding Calanus marshallae. Mar. Biol. 103,175 -181.[CrossRef]
Farkas, T., Storebakken, T. and Bhosle, N. B. (1988). Composition and physical state of phospholipids in calanoid copepods in India and Norway. Lipids 23,619 -612.[CrossRef]
Fleminger, A. and Hulsemann, K. (1977). Geographical range and taxonomic divergence in North Atlantic Calanus (C. helgolandicus, C. finmarchicus, and C. glacialis). Mar. Biol. 40,233 -248.[CrossRef]
Gerber, R. P. (2000). An Identification Manual to the Coastal and Estuarine Zooplankton of the Gulf of Maine Region. Brunswick, ME: Acadia Productions.
Goad, L. J. (1981). Sterol biosynthesis and metabolism in marine invertebrates. Pure Appl. Chem. 53,837 -852.[CrossRef]
González, J. G. (1974). Critical thermal maxima and upper lethal temperatures for the calanoid copepods Acartia tonsa and A. clausi. Mar. Biol. 27,219 -223.[CrossRef]
Halsband-Lenk, C., Hirche, H. J. and Carlotti, F. (2002). Temperature impact on reproduction and development of congener copepod populations. J. Exp. Mar. Biol. Ecol. 271,121 -153.[CrossRef]
Harvey, H. R., Ederington, M. C. and McManus, G. B. (1987). Lipid composition of the marine ciliates Pleuronema sp. and Fabrea salina: shifts in response to changes in diet. J. Euk. Microbiol. 44,189 -193.[CrossRef]
Hassett, R. P. (2004). Supplementation of a diatom diet with cholesterol can enhance copepod egg production rates. Limnol. Oceanogr. 49,488 -494.
Hazel, J. R. and Williams, E. E. (1990). The role of alterations in membrane lipid-composition in enabling physiological adaptation of organisms to their physical environment. Prog. Lipid Res. 29,167 -227.[CrossRef][Medline]
Hirche, H. J. (1987). Temperature and plankton. II. Effect of respiration and swimming activity in copepods from the Greenland Sea. Mar. Biol. 94,347 -356.[CrossRef]
Hirche, H. J. and Kwasniewski, S. (1997). Distribution, reproduction and development of Calanus species in the Northeast Water in relation to environmental conditions. J. Mar. Syst. 10,299 -317.[CrossRef]
Jouni, Z. E., Zamora, J. and Wells, M. A. (2002). Absorption and tissue distribution of cholesterol in Manduca sexta. Arch. Insect Biochem. Physiol. 49,167 -175.[CrossRef][Medline]
Keller, M. D., Selvin, R. C., Claus, W. and Guillard, R. R. L. (1987). Media for the culture of oceanic ultraphytoplankton. J. Phycol. 23,633 -638.
Knauer, J., Barrett, S. M., Volkman, J. K. and P. C., Southgate. (1999). Assimilation of dietary phytosterols by the Pacific oyster Crassostrea gigas spat. Aquac. Nutr. 5,257 -266.[CrossRef]
Kroes, J. and Ostwald, R. (1971). Erythrocyte membranes-effects of increased cholesterol content on permeability. Biochim. Biophys. Acta 249,647 -650.[Medline]
Labbe, C., Maisse, G., Müller, K., Sachowski, A. and Kaushik, S. and Loir, M. (1995). Thermal acclimation and dietary lipids alter the composition, but not fluidity, of trout sperm plasma membrane. Lipids 30,23 -33.[CrossRef][Medline]
Lahdes, E., Balogh, G., Dodor, E. and Farkas, T. (2000). Adaptation of composition and biophysical properties of phospholipids to temperature by the crustacean, Gammarus spp. Lipids 35,1093 -1098.[CrossRef][Medline]
Landry, M. R., Hassett, R. P., Fagerness, V., Downs, J. and Lorenzen, C. J. (1984). Effect of food acclimation on assimilation efficiency of Calanus pacificus. Limnol. Oceanogr. 29,361 -364.
Lange, Y., Swaisgood, M. H., Ramo, B. V. and Steck, T. L.
(1989). Plasma membranes contain half the phospholipids and 90%
of the cholesterol and sphingomyelin in cultured human fibroblasts.
J. Biol. Chem. 264,3786
-3793.
Liu, H., Bidigare, R. R., Laws, E., Landry, M. R. and Campbell, L. (1999). Cell cycle and physiological characteristics of Synechococcus (WH7803) in chemostat culture. Mar. Ecol. Prog. Ser. 189,17 -25.[CrossRef]
MacIsaac, H. J., Hebert, P. D. N. and Schwartz, S. S. (1985). Inter- and intraspecific variation in acute thermal tolerance of Daphnia. Physiol. Zool. 58,350 -355.
Martin-Creuzburg, D. and Von Elert, E. (2004). Impact of ten dietary sterols on growth and reproduction of Daphnia galeata. J. Chem. Ecol. 30,483 -500.[CrossRef][Medline]
Mauchline, J. (1998). The biology of calanoid copepods. Adv. Mar. Biol. 33, 1-710.[CrossRef]
Mountain, D. G. and Jessen, P. F. (1987). Bottom waters of the Gulf of Maine, 1978-1983. J. Mar. Res. 45,319 -345.
Patterson, G. W., Tsitsa-Tzardis, E., Wikfors, G. H., Gladu, P. K., Chitwood, D. J. and Harrison, D. (1993). Sterols of Tetraselmis (Prasinophyceae). Comp. Biochem. Physiol. 105B,253 -256.[CrossRef]
Patterson, G. W., Tsitsa-Tzardis, E., Wikfors, G. H., Ghosh, P., Smith, B. C. and Gladu, P. K. (1994). Sterols of eustigmatophytes. Lipids 29,661 -664.[CrossRef][Medline]
Pedersen, G. and Tande, K. S. (1992). Physiological plasticity to temperature in Calanus finmarchicus: reality or artifact? J. Exp. Mar. Biol. Ecol. 155,183 -197.[CrossRef]
Prahl, F. G., Eglinton, G., Corner, E. D. S., O'Hara, S. C. M. and Forsberg, T. E. V. (1984). Changes in plant lipids during passage through the gut of Calanus. J. Mar. Biol. Assoc. UK 64,317 -334.
Pruitt, N. L. (1988). Membrane lipid composition and overwintering strategy in thermally acclimated crayfish. Am. J. Physiol. 254,R870 -R876.[Medline]
Robertson, J. C. and Hazel, J. R. (1995). Cholesterol content of trout plasma membranes varies with acclimation temperature. Am. J. Physiol. 269,R1113 -R1119.[Medline]
Robertson, J. C. and Hazel, J. R. (1997). Membrane constraints to physiological function at different temperatures: does cholesterol stabilize membranes at elevated temperatures? In Global warming: Implications For Freshwater and Marine Fish (ed. C. M. Woods and D. G. McDonald), pp. 25-49. Cambridge: Cambridge University Press.
Sengupta, P., Baird, B. and Holowka, D. (2007). Lipids rafts, fluid/fluid phase separation, and their relevance to plasma membrane structure and function. Semin. Cell Dev. Biol. 18,583 -590.[CrossRef][Medline]
Shreve, M., Yi, S.-X. and Lee, R. E. (2007). Increased dietary cholesterol enhances cold tolerance in Drosophila melanogaster. Cryo. Letters 28, 33-37.[Medline]
Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J. and Klenk, D. C. (1985). Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85.[CrossRef][Medline]
Sullivan, B. K. and McManus, L. T. (1986). Factors controlling seasonal succession of the copepods Acartia hudsonica and A. tonsa in Narragansett Bay, Rhode Island: temperature and resting egg production. Mar. Ecol. Prog. Ser. 28,121 -128.[CrossRef]
Teshima, S. I. (1971). Bioconversion of β-sitosterol and 24-methylcholesterol to cholesterol in marine crustacea. Comp. Biochem. Physiol. 39,815 -822.[CrossRef][Medline]
Tirelli, V. and Mayzaud, P. (2005).
Relationship between functional response and gut transit time in the calanoid
copepod Acartia clausi: role of food quantity and quality.
J. Plankton Res. 27,557
-568.
Véron, B., Billard, C., Dauguet, J. C. and Hartmann, M. A. (1996). Sterol composition of Phaeodactylum tricornutum as influenced by growth temperature and light spectral quality. Lipids 31,989 -994.[CrossRef][Medline]
Von Elert, E., Martin-Creuzburg, D. and Le Coz, J. R. (2003). Absence of sterols constrains carbon transfer between cyanobacteria and a freshwater herbivore (Daphnia galeata). Proc. R. Soc. Lond., B, Biol. Sci. 270,1209 -1214.[Medline]
Yeagle, P. L., Young, J. and Rice, D. (1988). Effects of cholesterol on (Na+, K+)-ATPase ATP hydrolyzing activity in bovine kidney. Biochemistry 27,6449 -6452.[CrossRef][Medline]
Zehmer, J. K. and Hazel, J. R. (2003). Plasma
membrane rafts of rainbow trout are subject to thermal acclimation.
J. Exp. Biol. 206,1657
-1667.
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