Long-term fasting and realimentation in hypogean and epigean isopods: a proposed adaptive strategy for groundwater organisms
1 Hydrobiologie et Ecologie Souterraines (UMR CNRS 5023), 6 rue Dubois,
Université Claude Bernard-Lyon I, F-69622 Villeurbanne Cedex,
France
2 Station biologique (UMR 6553 CNRS), Université de Rennes I, F-35380
Paimpont, France
* Author for correspondence (e-mail: hervant{at}univ-lyon1.fr )
Accepted 18 April 2002
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Summary |
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Key words: starvation, refeeding, subterranean, surface, crustacean, intermediary metabolism, energy metabolism, digestive physiology, adaptive strategy, food-limited biotope
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Introduction |
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Hervant et al. (1997)
discovered that the hypogean aquatic isopod Stenasellus virei
surviving prolonged fasting (exceeding 200 days) longer than the
surface-dwelling species Asellus aquaticus and most other crustaceans
previously studied. The hypogean amphipods Niphargus virei and N.
rhenorhodanensis and the cave amphibian Proteus anguinus also
showed high tolerance to starvation (Hervant et al.,
1999b
,
2001
). During long-term
fasting in these subterranean species, locomotory, ventilatory and metabolic
rates were drastically reduced, whereas surface-related species exhibited only
slight decreases in these rates and responded with a transitory hyperactivity.
Hervant et al. (1997
)
hypothesized that the ability of hypogean species to survive prolonged
starvation probably involves their entering into a state of temporary torpor,
during which they subsist only on endogenous energy reserves. Unfortunately,
little information is available on the fasting-induced metabolic and
physiological responses of these organisms. Therefore, identifying the changes
in the digestive performance, biochemical composition and energy content of
such organisms under conditions of food limitation and refeeding would improve
our understanding of the competitive abilities of these hypogean species, and
their ability to exist in food-limited biotopes.
This study was designed to examine whether the behavioral and whole-animal
physiological responses (i.e. oxygen consumption) during prolonged food
deprivation and subsequent refeeding that had previously been identified for
the groundwater isopod Stenasellus virei
(Hervant et al., 1997) are
accompanied by specific changes in intermediary and energy metabolism (e.g.
energy allocation patterns, qualitative and/or quantitative changes in body
composition). We recorded some metabolic parameters (ammonia, arginine,
arginine phosphate, glucose, glycerol, glycogen, proteins, triglycerides and
non-esterified fatty acids) during a 180-day fasting period and a subsequent
15-day feeding phase in a subterranean aquatic isopod, Stenasellus
virei. In addition, we investigated the feeding and digestive strategies
(i.e. food-searching behavior and regulation of digestive performance) of this
isopod during refeeding. To generalise the energy strategy for groundwater
organisms, we undertook a parallel study during a 28-day fasting period and a
subsequent 7-day feeding phase in the morphologically similar surface-dwelling
isopod Asellus aquaticus.
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Materials and methods |
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Individuals of both species were acclimated to laboratory conditions for 2
months prior to separating into control and treatment groups. Adults of both
groups (males only) were placed into 400 ml glass flasks (containing 250 ml
water and pieces of fine plastic grid as an artificial substrate) for
experimentation. Water in the flasks was renewed weekly. For both species, the
isopods of the control group were fed as described above. Treatment groups
were deprived of food for 180 days (hypogean species, S. virei) or 28
days (epigean species, A. aquaticus), according to their survival
times while fasting (Hervant et al.,
1997). Following the fasting periods, individuals were refed twice
over a 15-day (S. virei) or 7-day (A. aquaticus) period.
Throughout the study, mortality was considered negligible (<3 %) for both
species.
Sample preparation and metabolite assays
To investigate changes in dry mass, water content and whole-body
metabolites during food deprivation, ten individuals were sampled at intervals
of 0, 15, 30, 60, 90, 120, 150 and 180 days of fasting for S. virei,
and at 0, 7, 15, 21 and 28 days of fasting for A. aquaticus. Control
(fed) organisms were removed as described above (for each point, N=10
individuals). To identify changes in dry mass, water content, digestive
metabolism and whole-body metabolites during recovery from long-term fasting,
individuals were fasted for either 180 days (S. virei) or 28 days
(A. aquaticus), and then refed (see above). Ten refed individuals
were sampled at intervals of 4 and 15 days for S. virei, and at 3 and
7 days for A. aquaticus.
Once removed, control, fasted and refed individuals were immediately
anaesthetized by placing the animals for 5 min into a tricaine methane
sulfonate solution (0.5 gl-1) (Sandoz MS-222), rapidly dissected to
remove the gut content, weighed (wet mass), frozen in liquid nitrogen,
lyophilized (Virtis lyophilisator, Trivac D4B) and then re-weighed (dry mass).
Lyophilized individuals were homogenized (as described in
Hervant et al., 1995) and
stored at -80 °C until body metabolites were assayed. Gut contents were
also lyophilized and weighed (dry digesta mass). In addition, the time until
the first defecation (i.e. passage time) was recorded following refeeding.
Ammonia excretion rates were determined for both species from a sample of
incubation water in which control, fasted or refed animals (N=10)
were held for 12 h, as described (Hervant et al.,
1996,
1997
). The following
metabolites were assayed by standard enzymatic methods as described (Hervant
et al., 1995
,
1996
): ammonia
(NH4++NH3), arginine, arginine phosphate,
glucose, glycerol and glycogen. Total proteins, triglycerides and
non-esterified fatty acids were extracted according to the methods of Elendt
(1989
) and Barclay et al.
(1983
) and then measured using
specific test-kits (B
hringer-Mannheim). All assays were performed using
a Beckman DU-6 spectrophotometer set at 25 °C. The accuracy of each
analysis was tested by assaying the samples with and without an added internal
standard. The sensitivity of all assays was approximately 1 µmol
g-1 dry mass for all metabolites. Enzymes, coenzymes and substrates
used for enzymatic assays were purchased from B
hringer (Mannheim,
Germany) and Sigma Co. (St Louis, USA).
Statistical analyses
Values are presented as means ± S.E.M. Comparisons among means were
conducted with a one-way analysis of variance (ANOVA), using a Bonferroni test
for multiple comparisons as appropriate. For comparisons between means (at the
P<0.05 level) and after verification of normality of values, a
Tukey test was used. Statistical analyses were performed with the StatView
5® software package (Abacus).
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Results |
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Body mass and water content
In control (fed) organisms, dry mass and water content did not vary
significantly between sampling periods (not shown). Fasted animals showed a
slight decrease in mean percentage dry mass (-7% after 180 days in the
hypogean S. virei, -8% after 28 days in the epigean A.
aquaticus), and a small increase (Fig.
1) in mean percentage water content (+8% after 180 days in S.
virei, +5% after 28 days in A. aquaticus), although it was not
significantly different until 120 days in the subterranean species and 21 days
in A. aquaticus. With refeeding, both dry mass and water content
resumed pre-fasting levels in S. virei, while dry mass showed a
slight, but non-significant, recovery for A. aquaticus
(Fig. 1).
|
Digestive responses during refeeding
Time of first defecation (i.e. passage time) did not differ between control
and refed animals, but was significantly longer in S. virei
(8.3±1.0 days) than in A. aquaticus (5.2±0.7 days)
isopods (results not shown). Dry digesta mass (i.e. food intake) was 1.5-fold
greater in refed than in control S. virei, but did not differ between
control and refed A. aquaticus (results not shown).
Effect of fasting and subsequent refeeding on metabolite body
levels in the subterranean S. virei
Arginine phosphate content decreased significantly by day 30 of fasting,
reaching 73% of its initial value (fed level) after 180 days of food
deprivation, and quickly returned to the prefast value during refeeding
(Fig. 2A). During the 180 days
of fasting, only 8.5 µmol g-1 dry mass of arginine phosphate was
metabolized. Arginine content showed a significant increase by day 14 of
fasting (+19%), then dramatically decreased from day 120 to 46% of the control
value after 180 days fasting (Fig.
2A).
|
Body glycogen content decreased by day 30 of food deprivation in S. virei (Fig. 2B), reaching 83% of its initial content by day 60 (corresponding to a utilization of 53 µmol glycosylic unit g-1 dry mass). Glycogen levels then returned to the pre-fasting level after 120 days fasting. Glycogen content dramatically increased within the first week of refeeding (reaching 121% of the fed value), before returning to the pre-fasting level (Fig. 2B). Moreover, we found no significant change in whole animal glucose content (Fig. 2C) in both fasting and refeeding periods.
Proteins were significantly metabolized after 120 days lack of food, until they reached 80% of the fed level by day 180 (Fig. 2D), corresponding to a utilization of 0.11 g g-1 dry mass. During refeeding, protein content returned to pre-fasting levels by day 15 (Fig. 2D). Moreover, the ammonia excretion rate (NH4++NH3, calculated from its cumulation in the flask water during an incubation period of 12 h) remained constant for 120 d of fasting, followed by a slight increase (Fig. 2D). During refeeding, this rate immediately decreased to 73 % of the initial level (Fig. 2D).
Triglyceride (TG) stores had significantly decreased by day 60 of fasting, and reached 72 % of their initial value after 180 days of food deprivation (Fig. 2E), representing a total utilization of 8.4 µmol g-1 dry mass. With refeeding, TG content rebounded to the pre-fast level (Fig. 2E). In contrast, non-esterified fatty acids (NEFA) levels significantly increased between 60 and 120 days of food deprivation, before returning to the pre-fast level (Fig. 2F). Upon recovery from nutritional stress, NEFA content immediately decreased, before returning to control level (Fig. 2F). During fasting, glycerol content showed a significant increase on day 60 then immediately decreased, reaching 84 % of the fed level after 180 days (Fig. 2F). Refeeding resumed glycerol levels to the control value (Fig. 2F).
Effect of fasting and subsequent refeeding on metabolite body
levels in the epigean A. aquaticus
A. aquaticus showed a significant decrease in arginine phosphate
content by day 14 of fasting, losing 41 % of its initial content by day 28
(Fig. 3A), corresponding to a
total utilization of 6.6 µmol g-1 dry mass. On refeeding,
arginine phosphate content increased, reaching 80 % of its initial amount
within 7 days (Fig. 3A). In
contrast, arginine content showed the opposite response, increasing with
fasting and decreasing with refeeding (Fig.
3A).
|
With fasting, whole-animal glycogen content immediately fell sharply to 33 % of its initial concentration within 28 days (Fig. 3B), corresponding to a utilization of 90 µmol glycosylic unit g-1 dry mass. Refeeding allowed a slow increase in glycogen to 60 % of the initial content within 7 days (Fig. 3B). Body glucose significantly decreased from 14 days fasting and reached 88% of the initial content after 28 days (Fig. 3C). Glucose concentration returned to the fed value during refeeding (Fig. 3C).
Fasting lead to a significant decrease in body protein by day 14 and a total decline of 21 % by day 28 (Fig. 3D), representing a utilization of 0.11 g g-1 dry mass. During refeeding, A. aquaticus protein content slowly increased, reaching 87 % of the pre-fast level within 7 days (Fig. 3D). Ammonia excretion rate increased immediately with fasting, up to 115 % of the pre-fast level by day 28, and subsequently decreased with refeeding (Fig. 3D).
During fasting, TG dramatically and continuously decreased from day 14, reaching 45 % of the initial value by day 28 of the fast, a use of 10.7 µmol g-1 dry mass (Fig. 3E). Refeeding enabled the body TG content to slowly increase to 62 % of its initial content within 7 days (Fig. 3E). Body content of NEFA had significantly increased by day 14 of the fast, but was recovered with refeeding (Fig. 3F). Body glycerol concentration also increased from 14 days of fasting (Fig. 3F), but during refeeding rapidly decreased (Fig. 3F), then returned to the initial level after 7 days.
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Discussion |
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Body mass and water content during long-term fasting
When animals experience periods of limited food, they have to rely on their
own body reserves to fuel metabolic processes and the maintenance of
homeostasis. The subterranean (i.e. hypogean) S. virei showed lower
magnitudes of response to long-term fasting than the surface-dwelling A.
aquaticus, with a 7.3-fold slower rate of relative mass loss. Some
subterranean amphipods and amphibians and numerous epigean animals display
fasting responses similar to that of S. virei (Hervant et al.,
1999a,
2001
, and references therein).
These results suggest that hypogean organisms utilize their endogenous energy
stores at a relatively low rate.
To maintain the necessary body volume (fixed by the exoskeleton in
Arthropods) and internal turgidity during fasting, the lost tissue mass (used
as metabolic fuel) must be replaced by water
(Dall, 1974;
Wilcox and Jeffries, 1976
;
Stuck et al., 1996
). Both
isopod species followed this pattern, displaying a significant (but low)
increase in water content and a corresponding decrease in percentage dry mass
during food deprivation.
Metabolic responses to long-term fasting
The capacity to withstand periods of inadequate/poor nutrition depends on
the presence (i) of endogenous nutritive stores, and (ii) the necessary
adaptive responses (i.e. adjustments in behavior, physiology, and/or energy
and intermediary metabolism) to ensure that these stored metabolites are
utilized efficiently. A general energy-conserving physiological response to
starvation is a lowering of standard metabolic rate (SMR)
(Fuglei et al., 2000). For both
species, experimental data on fasting-induced changes in body composition
indicated significant utilization of phosphagen (arginine phosphate),
glycogen, triglycerides (TG) and proteins reserves.
Fed S. virei possesses large glycogen reserves, 2.3-fold greater
than fed A. aquaticus, and significantly higher than those usually
found in epigean crustaceans (reviewed in
Hervant et al., 1996). In
addition, the hypogean species possessed significantly greater arginine
phosphate (x2.2) and TG (x1.5) reserves than A.
aquaticus, allowing them to fuel their metabolism for a much longer time
while fasting, thus prolonging their survival. For groundwater species, energy
stores at the beginning of a fast have to be sufficient to allow survival for
an unpredictable duration, but paradoxically, should not be too large, because
body reserves are energetically costly to transport and might reduce mobility,
thus increasing the risk of predation and/or reducing food-searching
abilities. Consequently, energy stored during periods of food abundance must
always be adjusted to the highest tolerable nutritional stress for hypogean
species feeding infrequently. The loss of energy during long-term fasts will
therefore be reduced to a minimum. It has been found that the relative
metabolic rate of S. virei while fasting (i.e. the metabolic rate
during fasting divided by that before fasting) is considerably lower than that
of A. aquaticus (Hervant et al.,
1997
), so approximately 50% of the metabolic energy dissipated by
the well-fed subterranean species was saved by the starving one, whereas under
these conditions no energy was saved by the epigean crustacean. Hervant et al.
(1997
,
1999b
,
2001
) observed similar
responses for epigean and hypogean amphipods and salamanders. In addition, fed
groundwater species often possessed low resting metabolic and activity rates
(Hüppop, 1985
;
Hervant et al., 1997
).
Although lowering metabolic rate may lead to a reduction in motility,
increasing the risk of predation, hypogean animals usually suffer little from
predatory pressure. Indeed, subterranean organisms can survive during long
periods of food deprivation at a low energetic cost. Moreover, S.
virei metabolized phosphagen, proteins and TG at low rates under
conditions of food deprivation (5.1-8.2 times lower than the epigean A.
aquaticus), metabolizing glycogen only at the beginning of the fast, but
then, surprisingly, later resynthesizing it. This drastic reduction in energy
use (which was initially low) sustains their metabolic reserves for as long as
possible, therefore increasing survival time under fasting conditions.
Studies that have addressed the effects of fasting on crustaceans have
demonstrated both qualitative and quantitative changes in body composition
(reviewed in Stuck et al.,
1996). The relative importance of metabolic reserves and their
order of utilization varies among species (reviewed in
Hervant et al., 1999b
). Some
species actually switch from one stored metabolite to another as prolonged
starvation continues (Mayzeau,
1976
; Elendt, 1989
;
Hervant et al., 1999b
).
The epigean A. aquaticus demonstrated a monophasic response to food deprivation, characterized by an immediate, linear and large decrease in all of its energy reserves. In contrast, prolonged fasting by S. virei was characterized by three successive phases: (1) an immediate, but low, depletion of both glycogen and arginine phosphate stores (days 15-60), followed by (2) the utilization of triglycerides associated with glycogen resynthesis (days 60-120) and finally (3) a slow depletion (days 120-180) of both proteins (demonstrated by a slight increase in ammonia excretion rate) and lipids, always associated with a glycogen resynthesis.
In food-limited groundwater species, the rapidly usable carbohydrates and
phosphagen stores served only as initial metabolic fuels, before being
replaced by lipid reserves. The glycogen de novo synthesis observed
in S. virei after day 60 may be a result of an increased
conversion/utilization of amino acids (originating from proteolysis) and/or
glycerol (from lipolysis) to glycogen, by glyconeogenesis. This hypothesis is
supported by the decrease in both arginine (originating from the utilization
of arginine phosphate) and glycerol observed with fasting in this animal.
Moreover, the existence of a high glyconeogenic capability has been
demonstrated recently in the subterranean crustacean Niphargus virei
(Hervant et al., 1999a). In
contrast, the epigean A. aquaticus did not show high glyconeogenic
conversion rates of amino acids and/or glycerol during food deprivation.
If the utilized amounts of glycogen, proteins and lipids are completely
oxidized to CO2 and H2O, then the energy provided by
each metabolite can be derived (Elendt,
1989). In the hypogean species, lipids (representing approximately
60% of the energy consumed during the 180 days fasting period) and proteins
(40% of energy consumed) were the most metabolized substrates in terms of
total energy, while glycogen did not contribute to energy production. The
epigean A. aquaticus had a different energy strategy: proteins
(representing approximately 50% of the energy losses during the 28 day fasting
period) and total lipids (45% of energy loss) were the most metabolized
stores, whereas glycogen reserves, although dramatically depleted, seemed not
to be preferentially used (5% of energy loss). The calculated reduction of
total energy content was only 34J g-1 dry mass day-1 for
S. virei, versus 190J g-1 dry mass day-1 for
A. aquaticus. Our data are in agreement with the metabolic rates
given by Hervant et al. (1997
,
2001
) for fed and starved
hypogean and epigean amphipods and salamanders.
These results demonstrate that the groundwater crustacean S. virei
(i) has lower energetic requirements and is better adapted to long-term food
shortage than the surface-dwelling A. aquaticus, and (ii)
preferentially utilizes lipids in order to save carbohydrates and phosphagens
(the two main fuels metabolized during oxygen deficiency in crustaceans;
Zebe, 1991) and, like some
mammals (Newsholme and Stuart,
1973
; Fuglei et al.,
2000
), cave amphibians
(Hervant et al., 2001
) and
birds (Le Maho, 1984
), to save
proteins (and therefore muscular mass) for as long as possible. Thus, this
species can successfully withstand a hypoxic period subsequent to (or
associated with) an initial nutritional stress, and can rapidly resume
searching for food during short-term, sporadic, nutrition events.
Metabolic and digestive responses to refeeding
When food is available once more, it is ecologically very advantageous for
organisms to quickly and completely restore the energy reserves that were
depleted during nutritional stress, especially in harsh and unpredictable
biotopes such as numerous groundwater systems. Refeeding resulted in a partial
restoration of body stores within A. aquaticus, and in complete
restoration within S. virei. For both species, the resynthesized body
materials replaced the `excess' water accumulated during fasting.
The food-limited S. virei resynthesized phosphagen, proteins and
TG with high production rates, significantly higher (1.2- to 1.4-fold) than in
the frequently feeding A. aquaticus. For S. virei, these
resynthesis rates were 11.0- to 15.5-fold greater than utilization rates
(calculated during the whole nutritional stress in starved animals), while
A. aquaticus only showed a moderate increase (1.2- to 2.3-fold) in
these `recovery indicators'. Cave amphipods and salamanders also showed high
resynthesis rates (Hervant et al.,
1999b,
2001
). As a consequence, the
rate at which fat stores were deposited while groundwater organisms fed was
largely higher than fat accumulation rates measured in numerous wild mammals
and birds, including antarctic penguins, which experience prolonged periods of
anorexia on land and hyperphagia at sea (reviewed in
Groscolas and Robin, 2001
).
In S. virei, as in other subterranean species
(Hervant et al., 2001), body
glycogen content displayed a large but transitory increase during refeeding,
its concentration strongly exceeding the control level during the first week
of refeeding. This response may represent an adaptation for the rapid storage
of food energy to be mobilized later for the synthesis of body materials such
as TG and proteins.
The ability to maintain and rapidly restore high levels of metabolic stores
for use during food deficiency (and/or lack of oxygen;
Malard and Hervant, 1999)
allows groundwater organisms to fuel successfully an ensuing unpredictable
fasting (and/or hypoxic) period and, therefore, to increase their competitive
abilities.
Secor (2001) stated that
the regulation of digestive performance is an adaptive response of feeding
habits. Hervant et al. (1997
)
showed that immediately after the onset of refeeding, both species presented a
large (and transitory) overshoot in oxygen consumption. This increase in
metabolism was probably due to the added cost of digestive metabolism,
together with any additional cost of upregulating the digestive tract
(Secor, 2001
). We suspect that
both crustaceans regulate their digestive performance, especially the
infrequently feeding S. virei, which exhibits a larger post-feeding
metabolic response than the frequently feeding A. aquaticus
(Hervant et al., 1997
). Secor
(2001
) noted that infrequently
feeding amphibians and reptiles possess lower SMR and experience a greater
increase in metabolic rate during digestion than frequent feeders. The
preliminary results presented by Hervant et al.
(1997
,
2001
) reinforced this general
hypothesis.
Compared to A. aquaticus, fasted S. virei consumed 50% more food upon refeeding, leading to an acceleration in the resynthesis of depleted body stores. It was felt that if the intestine was going to significantly upregulate performance in the subterranean isopod, it would do so in response to this large digestive load. This feeding behavior appears to be a good adaptive response to an extreme biotope, often simultaneously unpredictable (concerning food and oxygen) and energy-poor, in which infrequent meals must be optimally utilized.
From the observed passage times, digestion rates appeared slower in the
food-limited groundwater species than in the frequently feeding epigean
species, probably maximizing assimilation of available nutrients. The
`digestive efficiency' (defined in this study as the gain in body mass per
gram of O2 consumed and per day, and calculated from the extra
O2 consumed beyond SMR during realimentation) (data in
Hervant et al., 1997) was
1.2-fold higher in the infrequently feeding S. virei than in A.
aquaticus. Hypogean and epigean amphipods and salamanders also showed a
high digestive efficiency (Hervant et al.,
1999b
,
2001
). There is obviously a
selective advantage for an animal in such an harsh environment to use the
available food energy optimally.
During refeeding, both species show a large hyperactivity
(Hervant et al., 1997),
corresponding to an active food-searching behavior. The preferential
degradation of lipids as fuel for metabolism and the protein sparing observed
during fasting may preserve essential functions such as locomotion
(Fuglei et al., 2000
). This
protein sparing may be of prime necessity for subterranean organisms so that
they can rapidly resume locomotory activity (e.g. food searching activity)
when food becomes available again. This could be crucial, particularly in
habitats where food competition occurs: animals whose locomotory capabilities
are rapidly restored may have a significant advantage (by their higher ability
to compete for limited food resources) for further population growth. Due to
the higher muscular protein content and sensitivity to the presence of
potential food generally shown by hypogean organisms
(Uiblein et al., 1992
;
Hervant et al., 2001
),
nutrient detection was economical, more efficient and more rapid in S.
virei (contact after a few seconds) than in A. aquaticus (a few
minutes). This faster reaction may also be explained by a lower metabolic
depression in active muscles than in other tissues, as shown for numerous
fasted mammals and birds (Fuglei and
Oritsland, 1999
).
A proposed adaptive strategy for food-limited groundwater
organisms
Mendez and Wieser (1993),
reviewing numerous studies on fishes, pointed out that selection might have
favored a sequential energy strategy in response to long-term fasting and
subsequent refeeding, such that four successive phases (referred to as stress,
transition, adaptation and recovery) can be distinguished on the basis of
changes in oxygen consumption and spontaneous activity. Hervant et al.
(2001
) demonstrated the
existence of a similar energy strategy in hypogean and epigean salamanders,
based on behavioral, respiratory, haematological and metabolic responses. To
provide a hypothetical model (i.e. a sequence of events) representing the
responses of subterranean animals to long-term food stress, this nomenclature
was also employed in the present study.
During the stress phase (days 0-15), both species increased locomotor
activity (and therefore SMR; data in
Hervant et al., 1997) at
first, reflecting an increased food searching behavior.
During the transition phase (days 15-30 in A. aquaticus; days
15-60 in S. virei), both isopods responded to continued food
deprivation by a reduction in SMR and spontaneous activity. Both reductions
were more drastic in S. virei than in A. aquaticus. During
this second phase, S. virei only catabolized carbohydrates and
phosphagen stores, while A. aquaticus largely used all four stored
metabolites. In addition, the subterranean isopod S. virei rapidly
resynthesized its glycogen content (by the glyconeogenesis pathway:
Hervant et al., 1999a).
During the adaptation phase in S. virei (after 60 days of
fasting), energy metabolism shifted from a carbohydrate-dominated to a
lipid-dominated form. At the end of this third period, metabolism
progressively shifted from a lipid-dominated to a lipid/protein-dominated
form, suggesting that the hypogean crustacean studied could not prolong total
cessation of protein metabolism after a 120-day food stress. For S.
virei, the adaptation phase was characterized by stable metabolic and
activity rates that remained at the reduced, minimal, levels reached at the
end of the transition phase (data in
Hervant et al., 1997). In
contrast, no significant adaptation period was observed in the epigean A.
aquaticus; this species seemed to directly enter a `critical', lethal,
phase (as defined by Le Maho,
1984
).
During the recovery phase, both crustaceans responded to renutrition by an increase in both oxygen consumption and spontaneous activity (i.e. active food-searching behavior), and rapidly resynthesized all four energy reserves. Both adaptive responses were more efficient and more rapid in the groundwater species.
Based on the results of this study, we propose a general model of adaptive
strategy for groundwater organisms, involving the ability to withstand
long-term fasting and the efficient use of consumed food. Adaptation to
prolonged fasting included (i) a `sit-and-wait' behavior, i.e. a period of
depressed metabolism during which the subterranean species subsisted on a
high-energy reserve (mainly lipid stores), and (ii) the possession of low
energetic requirements and large body stores. In addition, hypogean species
displayed high recovery abilities during refeeding, showing optimal
utilization of available food energy and therefore rapid restoration of the
body reserves depleted during nutritional stress. All hypogean species studied
(Hervant et al., 1997;
1999b
;
2001
; this study) appeared
better adapted to long-term food deprivation and to unpredictable, short-term,
energy inputs than surface-dwelling species. These adaptations allow
subterranean organisms to tolerate a prolonged reduction in food availability
by maximizing the length of time that metabolism can be fuelled by a given
food ration and/or a given energy reserve. This supports the suggestion by
Hoffmann and Parson (1991
)
that difficulties in obtaining food in stressful environments may select for
conservative energy use.
These adaptive responses might be considered for numerous subterranean organisms as an efficient energy-saving strategy in a harsh and unpredictable environment where fasting (and/or hypoxic) periods of variable duration alternate with sporadic feeding events (and/or normoxic periods). Therefore, food-limited (and/or hypoxia tolerant) groundwater species appear to be good examples of animals representing a low-energy system.
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Acknowledgments |
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References |
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