Numerous groundwater ecosystems are characterized by
severely limited food supplies during most of the year because
of the lack of autotrophic production and sporadic
allochthonous input. Due to the temporal and spatial patchiness
of food availability in most groundwater biotopes, periods of
prolonged starvation are common events in the life of
subterranean (i.e. hypogean) organisms (Poulson, 1964;
Hüppop, 1985, 1986; Hervant et al., 1997). The ability to
withstand and recover from long periods of nutritional stress
is a critical adaptation for survival of any organism in food-
limited systems. Therefore, several hypogean species are
thought to have evolved behavioral, physiological and/or
metabolic adaptations that allow them to exploit harsh
subterranean environments successfully. However, needs and
life styles differ considerably between hypogean species
(Danielopol and Rouch, 1991) and so their adaptations to food
limitation might also differ. Although instantaneous ecological
consequences of poor nutrition are sometimes hard to
distinguish, the reproductive potential of animals may become
reduced and the effects will be manifested at the population
level through a smaller amount of offspring or reduced survival
capacity of the young.
The subterranean aquatic crustaceans Niphargus
rhenorhodanensis and N. virei can survive without feeding for
periods well in excess of 1 year (Gibert and Mathieu, 1980;
Mathieu and Giber, 1980). In a previous paper (Hervant et al.,
1997), it was pointed out that both hypogean amphipod species
and the hypogean isopod Stenasellus virei are better adapted
to lack of food than surface-related species and all crustaceans
previously studied, with survival times exceeding 200 days.
During long-term starvation, the locomotory, ventilatory and
metabolic rates were drastically lowered in subterranean
3587 The Journal of Experimental Biology 202, 3587–3595 (1999)
Printed in Great Britain © The Company of Biologists Limited 1999
JEB2182
The effects of long-term starvation and subsequent
refeeding on intermediary and energy metabolism were
investigated in two subterranean aquatic crustaceans,
Niphargus rhenorhodanensis and Niphargus virei, and in
a morphologically similar surface-dwelling species,
Gammarus fossarum. The metabolic response to prolonged
food deprivation was monophasic in G. fossarum, showing
an immediate, linear and large decline in all of the energy
reserves. In contrast, both subterranean organisms
displayed successive periods of glucidic, proteo-glucidic
then lipidic-dominant catabolism during food deprivation.
In both subterranean species, lipids (51 % of the energy
consumed during a 180-day starvation period) and proteins
(44 %) were the most metabolized substrates in terms of
total energy, whereas glycogen (5 %) contributed little
energy. G. fossarum displayed a different energetic
strategy: proteins comprised 56 % of the energy losses
during a 28-day starvation period, total lipids some 39 %
and glycogen reserves only 5 %. We propose an energy
strategy for food-limited subterranean crustaceans
involving the possession of (1) higher amounts of stored
arginine phosphate, triglycerides and glycogen and (2)
lower utilization rates of stored metabolites than G.
fossarum and numerous other surface-dwelling
crustaceans, making the fueling of food deprivation
possible for a longer time. In addition, these species had a
faster and more efficient assimilation of available nutrients
during recovery from food deprivation, enabling
preparation for a new nutritional stress. These specific
adaptive responses might be considered, for N. virei and N.
rhenorhodanensis, as an efficient energy-saving strategy
for an environment where extended starvation periods
alternate with sporadic feeding events, therefore improving
their competitive advantages.
Key words: intermediary metabolism, energy metabolism, starvation,
catabolism, refeeding, amphipod, Niphargus rhenorhodanensis,
Niphargus virei, Gammarus fossarum.
Summary
Introduction
COMPARATIVE STUDY ON THE METABOLIC RESPONSES OF SUBTERRANEAN
AND SURFACE-DWELLING AMPHIPODS TO LONG-TERM STARVATION AND
SUBSEQUENT REFEEDING
FRÉDÉRIC HERVANT
1,
*, JACQUES MATHIEU
1
AND HERVÉ BARRÉ
2
1
Hydrobiologie et Ecologie Souterraines (ESA CNRS 5023) and
2
Physiologie des Régulations Energétiques,
Cellulaires et Moléculaires (UMR CNRS 5578), Université Claude Bernard-Lyon I, F-69622 Villeurbanne Cedex,
France
*e-mail: hervant@cismsun.univ-lyon1.fr
Accepted 27 September; published on WWW 29 November 1999