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Resistance to Freshwater Exposure in White Sea Littorina Spp. I: Anaerobic Metabolism and Energetics

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Resistance to Freshwater Exposure in White Sea Littorina Spp. I: Anaerobic Metabolism and Energetics View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Electronic Publication Information Center J Comp Physiol B (2000) 170: 91±103 Ó Springer-Verlag 2000 ORIGINAL PAPER I. M. Sokolova á C. Bock á H.-O. PoÈ rtner Resistance to freshwater exposure in White Sea Littorina spp. I: Anaerobic metabolism and energetics Accepted: 4 October 1999 Abstract Anaerobic metabolism and changes in the anaerobic capacity of Littorina spp. are discussed in osmotic concentration of extravisceral ¯uid were studied relation to their vertical distribution, size and ecology. in the White Sea periwinkles (Littorina littorea, Littorina saxatilis and Littorina obtusata) during freshwater Key words Salinity stress á Resistance adaptations á exposure. Resistance to hypoosmotic stress increased in Anaerobic metabolism á ATP turnover á Littorina spp. the order: L. obtusata < L. saxatilis < L. littorea. Our data suggest that osmotic shock is not a primary reason Abbreviations ADP adenosine-5¢-diphosphate á AEC for mortality of the periwinkles under these conditions. adenylate energy charge á AMP adenosine-5¢- During environmental anaerobiosis, considerable monophosphate á ATP adenosine-5¢-triphosphate á Arg )1 succinate accumulation (up to 10±19 lmol g wet L-arginine á AWI Alfred-Wegener-Institute for Polar weight), and depletion of phosphagen and ATP pools and Marine Research á dG/dn Gibbs free energy were found in the studied species. Other metabolic end change á EDTA ethylenediaminetetraacetic acid á EF products (alanopine, strombine, lactate, acetate or pro- extravisceral ¯uid á HPLC High Performance Liquid pionate) were not detected. Succinate accumulation and Chromatography á HSD honestly signi®cant _ net ATP breakdown were the fastest in the least resistant dierence á MATP ATP turnover rate á NTA species, L. obtusata, and slowest in the most resistant, nitrilotriacetic acid á PCA perchloric acid á Pi inorganic L. littorea. Rate of ATP turnover decreased during phosphate á PLA phospho-L-arginine á RPLA relative freshwater exposure in L. littorea and L. saxatilis, but amount of phosphagen á RST standardised respiration not in L. obtusata. Our data suggest that dierential rate resistance of three studied Littorina spp. to extreme hypoosmotic stress may be related to their dierent abilities to reduce metabolic rate and ATP turnover Introduction during sustained anoxia. Species-speci®c variations in Salinity is an important environmental factor in¯uenc- ing various life characteristics of marine animals, including molluscs. Adaptation of marine molluscs to changes in salinity is achieved through two dierent Communicated by G. Heldmaier systems which are used alternatively depending on the I. M. Sokolova degree of the environmental disturbance (e.g. Kinne White Sea Biological Station, 1964; Berger 1986; Berger and Kharasova 1997). If Zoological Institute of Russian Academy of Sciences, salinity changes moderately, so-called capacity adapta- Universitetskaya nab., 1, tions play a major part in adjusting to the new osmotic 199034 St. Petersburg, Russia e-mail: [email protected] conditions. In marine molluscs, these adaptations in- Tel.: +7-812-1140097; Fax: +7-812-1140444 volve isoosmotic cell volume regulation through, for C. Bock á H.-O. PoÈ rtner example, shifts of intracellular free amino acid and Alfred-Wegener-Institute for Polar and Marine Research, inorganic ion concentrations (e.g. Lockwood 1976; Ecology and Ecophysiology, Natochin et al. 1979; Taylor and Andrews 1988; Columbusstrasse 30, Hawkins and Hilbish 1992), and changes of oxygen 27568, Bremerhaven, Germany e-mail: [email protected], consumption rates during salinity acclimation (Kinne [email protected] 1971; Berger 1986). Capacity adaptations typically result Fax: +49-0471-4831149 in adjustments which ensure performance of the most 92 important life functions and potentially unlimited sur- allows correlation of changes in anaerobic metabolic vival in the new osmotic environment. In contrast, if rate and energy status with dierential survival during environmental salinity strongly deviates from the opti- prolonged periods of hypoosmotic exposure and to mum, resistance adaptations are evoked. In marine suggest the primary mechanisms of mortality (and/or shelled gastropods these are so called escape responses resistance) under such conditions. (see review in Kinne 1971; Lockwood 1976; Berger The aim of our study was to investigate anaerobic 1986). Under conditions of extremely low or high metabolism in the White Sea periwinkles L. littorea, salinity, snails withdraw into the shell and isolate L. saxatilis and L. obtusata during extreme hypoosmotic themselves inside by tight closure of the shell aperture stress. We followed the time courses of mortality, an- with their operculum. This behavioural response greatly aerobic end-product accumulation and changes in the reduces water and salt exchange between the internal parameters of energy status and also analysed changes in medium of the animal and the unfavourable environ- the osmotic concentration of the extravisceral ¯uid (EF) ment (Avens and Sleigh 1965; Rumsey 1973; Berger in L. littorea during prolonged freshwater exposure. 1986). A similar response is typical for bivalves (Kinne Additionally, we compared the routine metabolic rates 1971; Lockwood 1976). However, the resistance re- under normoxic control conditions in the three studied sponse provides only limited survival of the organism, species. and if the period of extreme salinity stress persists, This investigation intended to answer the following considerable mortality is observed. questions: Reasons for the mortality of shelled gastropods and 1. Could osmotic shock alone account for the mortality bivalves under conditions of extreme salinity have long onset in periwinkles during freshwater exposure? been debated in the literature (e.g. Akberali et al. 1977; 2. Are there any species-speci®c dierences in the time Berger 1986). Principally, two dierent causes of mor- courses of anaerobic end-product accumulation and tality have been suggested: (1) osmotic shock due to the changes of intracellular energy status of the peri- gradual gain or loss of salts and/or water in a strongly winkles during prolonged freshwater exposure? hyper- or hypoosmotic medium, and (2) unfavourable 3. Do anaerobic and aerobic metabolic rates (the latter changes of the acid-base and/or energy status of the as assessed by routine oxygen consumption) dier in animal due to sustained environmental anaerobiosis in the studied Littorina spp.? the isolated state. There are some data suggesting that 4. Does dierential resistance to fresh water correlate the ®rst mechanism is of less (if any) importance in some with variations in the rate of anaerobic metabolism intertidal molluscs (Littorina saxatilis, Mytilus edulis, (i.e. rate of end-product accumulation) and ATP Berger 1980) and the freshwater bivalve Anodonta turnover in the periwinkles? grandis (Byrne and McMahon 1991), whereas in Mya arenaria and Macoma baltica the osmotic shock due to marked dilution of the internal milieu was named among the probable causes of the mortality onset (Golikov and Materials and methods Smirnova 1974; Khlebovich 1974; Berger 1980). At the same time, there is no evidence for or against the second Sampling of the periwinkles hypothesis, as there are no data on changes of the acid- Sampling was performed in July 1996 and August 1997 in the base and/or energy status of the organism during Chupa Inlet of Kandalaksha Bay in the White Sea (66°20¢N, exposure to extreme salinities. 33°40¢E). Water temperature in the ®eld was 10±15 °C, salinity 25± Three closely related gastropod species ± Littorina 27&. L. saxatilis and L. obtusata were collected from the macro- saxatilis, Littorina obtusata and Littorina littorea ± are phyte belt and gravel patches in the middle and lower intertidal common inhabitants of White Sea intertidal and upper zone, and L. littorea was sampled from stones and pebbles in the lower intertidal to upper subtidal zones. Prior to incubation all subtidal zones. The periwinkles are convenient objects snails were kept for 2±5 days in recirculating aquaria with natural for the study of resistance adaptations to extremely low sea water (salinity 26±27&) at 7.7 0.6 °C. Aquaria were equip- salinities. L. saxatilis inhabits the high intertidal zone ped with gravel bottom ®lters and air-pumps. Only adult snails were where it spends prolonged periods of air exposure in a used for the experiments. Shell diameters varied between 7±10 mm in L. saxatilis, 8±11 mm in L. obtusata and 22±26 mm in L. littorea. state of dormancy (McMahon 1990), L. obtusata lives in the middle and low littoral, mostly in the brown mac- rophyte (Fucus vesiculosus and Ascophyllum nodosum) Respiration rate canopy, and L. littorea occupies lower intertidal and subtidal horizons. In the White Sea, Littorina spp. may Measurements of routine respiration rate were performed by closed system respirometry (Lyzen et al. 1990). Animals were taken out of experience prolonged periods of extreme hypoosmotic the aquaria, placed individually into air-tight glass bottles half- stress, especially during spring ice-melting when surface ®lled with natural sea water (salinity 26±27&, temperature 7.7 water salinity can drop drastically (down to 2&) for as 0.6 °C) and left for 30 min to reduce the eect of handling. After long as a fortnight (Babkov and Lukanin 1985). These this, the bottles were carefully drained using
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