L
Journal of Experimental Marine Biology and Ecology 247 2000 113–129
www.elsevier.nl locate jembe
The ability to feed in hypoxia follows a seasonally dependent pattern in shore crab Carcinus maenas
A. Legeay, J.-C. Massabuau
` UMR
5805, Laboratoire d’Ecophysiologie et Ecotoxicologie des Systemes Aquatiques, ´
Universite Bordeaux I and CNRS , Place du Dr B. Peyneau, 33120 Arcachon, France
Abstract
The ability of the adult shore crab Carcinus maenas, native to the Bay of Arcachon SW France, to feed in hypoxia was determined at various seasons. Crabs previously kept at field
temperature were fed after a 5-day fasting period at 158C. Their blood oxygenation and pH regulation strategy and also their gill anatomy were analysed. From May to October, C
. maenas
21
feed at levels of O partial pressure p
in the water, pwO 5 2 kPa 1 mg l , without
2 O
2
2
switching to their anaerobic metabolism. In March–April, before the main moulting period, the same food intake at pwO 5 4 kPa induced a systematic blood lactate increase associated with
2
some mortality. An analysis performed at pwO 5 4 kPa at that time showed that in intermoult
2
crabs the development of a coating of foreign material over the gill cuticle interfered with O -supply, preventing the small arterial p
increases from 0.7 to 1 kPa which occurred at other
2 O
2
seasons. This led to a cellular hypoxia despite a systematic postprandial blood-pH alkalinisation which favoured O -loading at gill level and increased arterial O concentration. In March–April,
2 2
alkalinisation appeared at pwO values 6 kPa and from May to at least July at pwO 2 kPa.
2 2
Results are discussed in terms of season-related physiological performance, as hypoxic events mainly occur during the hot season.
2000 Elsevier Science B.V. All rights reserved.
Keywords : Oxygen; Gill; Biological rhythm; Respiration; Blood O
transport; Feeding; Metabolism;
2
Crustaceans; Lactate
1. Introduction
For two centuries, there has been a clear dynamic increase in the population of the European shore crab Carcinus maenas due to human activities. The crab is native to
Europe and was first reported in the western Atlantic in 1817 Cohen et al., 1995; it has
Corresponding author. Tel.: 1 33-5-5622-3925; fax: 1 33-5-5654-9383. E-mail address
: massabuauecotox.u-bordeaux.fr J.-C. Massabuau 0022-0981 00 – see front matter
2000 Elsevier Science B.V. All rights reserved.
P I I : S 0 0 2 2 - 0 9 8 1 0 0 0 0 1 4 2 - 8
114 A
. Legeay, J.-C. Massabuau J. Exp. Mar. Biol. Ecol. 247 2000 113 –129
now invaded coastal communities in the North Pacific as well as in Australia and South Africa Fulton and Grant, 1900; Hutchings et al., 1989; Le Roux et al., 1990; Cohen et
al., 1995. Due to its potential for extensive ecosystem alteration, it is today considered in a large body of literature as a ‘pest’ species. In response to this concern, it is
fundamental that we improve our knowledge of its potential to colonise new ecosystems and gain a better understanding of its ability to successfully face hypoxic events, as this
is a clear advantage during inter-species competition.
The main aim of the present work was to study the ability of Carcinus maenas to feed in hypoxic waters and to gain more insights into the physiological adaptations that allow
or limit this ability. After feeding, the shore crab’s O consumption increases by a factor
2
¯ 2 due to the specific dynamic action of food SDA; Brody, 1945; Beamish, 1974; Jobling, 1981; Houlihan et al., 1990. This is a severe physiological challenge to solve in
hypoxia. In a previous paper we reported that the SDA 24 h after feeding was systematically associated with blood acidosis in normoxia and with blood alkalosis in
hypoxia Legeay and Massabuau, 1999. We suggested that in hypoxia, the alkalosis could favour O
loading at the gill level via a pH-induced increase in hemocyanin
2
affinity Truchot, 1992. In contrast, in normoxia, the acidosis could favour O
2
unloading at the cellular level via a pH-induced decrease in hemocyanin affinity. The present study was carried out at various seasons from 1995 to 1997 in adult
intermoult C . maenas native to the Bay of Arcachon South-western France. Important-
ly, experiments were performed in laboratory conditions using procedures which brought about a respiratory behaviour close to that found in the natural habitat Massabuau and
Forgue, 1996. We report here that the performance of adult intermoult C . maenas in
hypoxia varies with the season in relation to the moulting cycle. In summer, C . maenas
that had moulted in the last 2–4 months could feed in a water p as low as 2–3 kPa
O
2
21
1–1.5 mg l at 158C with only a minor switch to anaerobic metabolism. In contrast,
in winter, with the water temperature in the Bay at its lowest in March–April, intermoult C
. maenas are least resistant to hypoxia. An analysis of gill morphometry, blood oxygenation status and associated blood pH changes shows how the development of a
coating of foreign material on the gill cuticle, which reaches a maximum in adult specimens before moulting in March–April, modifies its strategy and capacity to adapt
to hypoxia at various seasons. Results are discussed in terms of the ecological performance of C
. maenas in relation to the time of year. Unspecialised readers could read with interest Principles of Respiratory Physiology Dejours, 1981 to improve their
understanding of the fundamental but subtle physiological changes that are presently described.
For reference, 1 kPa 5 7.5 mmHg. In water equilibrated with air, the O fraction is
2
21 and p 5 21 kPa. Seawater with a 3-kPa p
is approximately 14–15 O
O O
2
2 2
saturated.
2. Materials and method
