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Effects of Temperature and Photoperiod on Glucose, Glycerol and Glycogen Concentrations in Helix Pomatia Linnaeus, 1758 in Spring and Autumn

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Effects of Temperature and Photoperiod on Glucose, Glycerol and Glycogen Concentrations in Helix Pomatia Linnaeus, 1758 in Spring and Autumn Vol. 19(3): 155–163 doi: 10.2478/v10125-011-0021-8 EFFECTS OF TEMPERATURE AND PHOTOPERIOD ON GLUCOSE, GLYCEROL AND GLYCOGEN CONCENTRATIONS IN HELIX POMATIA LINNAEUS, 1758 IN SPRING AND AUTUMN ANNA NOWAKOWSKA*,MICHA£ CAPUTA, JUSTYNA ROGALSKA Department of Animal Physiology, Institute of General and Molecular Biology, N. Copernicus University, Gagarina 9, 87-100 Toruñ, Poland; *corresponding author (e-mail: [email protected]) ABSTRACT: One of the variables oscillating seasonally in Helix pomatia L., described in our previous paper, was their rudimentary cryoprotection provided by modest increases in haemolymph glucose and glycerol concen- trations in autumn and early spring, respectively. Because factors governing cryoprotective responses are un- known, we decided to investigate the effects of spring and autumn acclimation of H. pomatia to different ther- mal and photoperiod conditions on the changes in haemolymph concentrations of glucose and glycerol and on the glycogen level in selected organs. Neither acclimation to short-day photoperiod nor low ambient tem- perature evoked increase in glucose and glycerol concentration in spring and autumn. Both acclimation vari- ants decreased hepatopancreatic glycogen level. The rudimentary freeze-tolerance in H. pomatia seems to be a combined effect of cold and short-day photoperiod and might also be affected by their nutritional and repro- ductive status. The effect of exposure to frost-bite is also likely to be involved. KEY WORDS: overwintering, freeze-tolerance, acclimation, cryoprotectants, land snails, Helix pomatia INTRODUCTION Entering winter torpor in land snails is frequently supercool (STOREY &STOREY 1988). Freeze-tolerance related to decrease in ambient temperature (LAZA- depends on accumulation of polyols and sugars which RIDOU-DIMITRIADOU &SAUNDERS 1986), shortening prevent intracellular ice formation. Synthesis of of light phase, and low air humidity during autumn. cryoprotectants prior to entering winter torpor is well However, before the onset of winter some preparatory known in some invertebrates (LI et al. 2002) and ver- changes, such as local migration, burrowing under- tebrates (LAYNE 1995). Elevated synthesis of these ground, calcareous epiphragm formation, decrease substances is associated with hormonal changes in in- in body water content (BIANNIC &DAGUZAN 1993, sects (WATANABE &TANAKA 1999), with seasonal BIANNIC et al. 1994), and changes in activity of some changes in lizards (GRENOT et al. 2000, VOITURON et enzymes (BIELAWSKI &KÊSA 1986) have been re- al. 2000, 2002) and is affected by extracellular ice for- ported. Despite the decreased ambient temperature mation in frogs (STOREY &STOREY 1985, STOREY in winter, torpid land snails are able to increase activ- 1987). ities of their glycolytic enzymes (MICHAELIDIS et al. According to some authors freeze tolerance in 2008). land snails depends on their size (ANSART &VERNON In the temperate zone, where the ambient tem- 2004), emptying of their gut (ANSART et al. 2002) and perature drops below the freezing point in winter, decreasing their body water content (NICOLAI et al. ectothermic animals use two anti-freezing strategies: 2005). Seasonal changes in the haemolymph concen- (i) freeze-tolerance – using low-molecular-weight or- tration of cryoprotectants, such as glycerol and glu- ganic solutions as cryoprotectants and (ii) freeze- cose, in H. pomatia Linnaeus, 1758 do not depend on -avoidance – enhancing the ability of body fluids to organ dehydration (NOWAKOWSKA et al. 2006). There 156 Anna Nowakowska, Micha³ Caputa, Justyna Rogalska is a modest increase in glucose concentration in win- because glucose and glycerol synthesis is based on ter. On the other hand, glycerol concentration is catabolism of liver glycogen (STOREY et al. 1981, slightly elevated in spring-active snails, which are well STEINER et al. 2000, LI et al. 2002). Another purpose hydrated but frequently exposed to freezing during of our study was to determine whether seasonal episodes of night ground frosts. changes in the cryoprotectant concentration in H. The cellular mechanisms responsible for regula- pomatia resulted from internal clock or were a re- tion of freeze tolerance in land snails are still far from sponse to environmental changes. We applied accli- being clear. Therefore, the objective of this study was mation to various combinations of ambient tempera- to verify the exogenous/endogenous control of cryo- ture and photoperiod to analyse various aspects of in- protectants synthesis in H. pomatia. The first aim of termediate metabolism, including synthesis of glu- the present study was to record changes in the haemo- cose and glycerol. Accordingly, we checked separately lymph concentrations of glucose and glycerol in snails the effect of temperature and photoperiod on the acclimated to different thermal and photoperiod con- biochemical changes, which could occur over time ditions during spring and autumn. We also decided to preceding or following torpor in nature. determine glycogen concentration in selected organs MATERIAL AND METHODS ANIMALS ambient conditions (25°C, 16L:8D), (ii) summer tem- perature (25°C) combined with short-day photo- A total of 38 adult H. pomatia, weighing approxi- period (8L:16D) and (iii) autumn temperature (5°C) mately 24 g, were collected from their natural habitat combined with long-day (16L:8D) photoperiod. (permission of the Polish Ministry of Environmental Autumn control data were taken from our previous Protection No.WsiR.II.KLD-6631-209/05) in the vi- ° ° paper (NOWAKOWSKA et al. 2006). When the control cinity of Toruñ (central Poland, 53 02’N, 18 35'E), snails were collected, the ambient temperature was twice over a period of their natural activity (i) in 9°C and the photoperiod was 10L:14D. spring (April), just after their arousal from winter tor- During acclimation the snails were housed in large por and (ii) in autumn (October), prior to natural acrylic boxes of 0.4 × 0.3 × 0.2 m, covered with wire onset of winter torpor. All the snails were weighted mesh, with leaf litter from their natural habitat. They and the height of their shells was measured. Only were fed ad libitum with fresh lettuce and vegetables. adult individuals with developed lip were used. Fragmented shells were provided as a calcium source. In both series of experiments biochemical analyses EXPERIMENTS were carried out after acclimation. The snails were used post mortem to examine haemolymph concen- The first set of experiments was performed in the trations of glycerol and glucose as well as organ con- spring. Immediately after bringing the snails to the centration of glycogen. They were decapitated, and laboratory, they were exposed to (i) summer-specific ° haemolymph samples were taken by puncturing the ambient temperature of 25 C combined with short-day heart with a syringe needle. The foot, kidney and photoperiod (8L:16D) and (ii) summer temperature ° hepatopancreas were removed and used to determine (25 C) combined with long-day photoperiod organ glycogen concentration. (16L:8D), for three weeks preceding biochemical analyses. Spring-active control snails were taken from the field at the end of the acclimation period in order LABORATORY ANALYSES to reduce the effect of season on cryoprotectants con- Chemicals: Anthrone reagent, potassium hydro- centration, which had been shown previously (NOWA- xide (KOH), trichloroacetic acid (TCA), were pur- KOWSKA et al. 2006). When the snails were collected, ° chased from Polskie Odczynniki Chemiczne (Gliwice, the ambient temperature was 8 C and the photo- Poland) and o-toluidine was purchased from period was 15L:9D. Data concerning summer-specific ° Sigma-Aldrich GmbH (Steinheim, Germany). All ambient conditions (temperature of 24 Cand other reagents were of analytic grade. All solutions long-day photoperiod of 16L:8D) were taken from were prepared with deionized water. our previous investigation (NOWAKOWSKA et al. 2006). Determination of glycerol concentration: The vol- The second set of experiments was performed in ume of haemolymph samples used to examine gly- the autumn. The freshly collected snails were divided cerol content was 0.1 ml. Haemolymph concentration into three groups which, during three weeks, were of glycerol was tested enzymatically using commercial subject to acclimation to the following photoperiod kits (Boehringer Mannheim Corp, Germany). Briefly, and temperature combinations: (i) summer-specific the hemolymph samples were diluted in 0.4 ml of Glucose, glycerol and glycogen in Helix pomatia 157 double-distilled water. The samples were incubated at to determine their fresh mass and then they were put 100°C for 5 min, then quickly cooled, and centrifuged into flasks, and immediately dissolved in 3 ml of KOH at 8,000 g × for 5 min. Finally, 0.1 ml of the super- per1goffresh mass. The samples were heated in a natant was used for the enzymatic reaction. The sam- boiling water bath for 20 min. The contents of the ples were subject to spectrophotometer (SEMCO flasks were diluted in 50 ml of water. The water sol- S91E, Warsaw, Poland) analysis at 365 nm. Glycerol ution of each sample (1 ml) was poured into tubes concentration was expressed in mmol/l. and 5 ml of anthrone was carefully added. The tubes Determination of glucose concentration: The were then incubated at 100°C for 10 min. Following haemolymph glucose concentration was assessed from cooling, the samples were subject to spectro- reaction of o-toluidine with glucose, which is the main photometer analysis at 620 nm. Glycogen concentra- haemolymph monosaccharide in molluscs (BORGES et tions were assessed using 5.5 mmol/l glucose stan- al. 2004). Glucose and o-toluidine give a colour com- dard (Carmay, Lublin, Poland) and expressed in plex. Briefly, 0.1 ml of the hemolymph was added to 1 mg/g tissue. ml of 3% TCA, and the samples were centrifuged at 10,000 g × for 5 min. Then, 0.2 ml of the supernatant DATA ANALYSIS was added to 1.8 ml of o-toluidine reagent and the samples were incubated in boiling water for 8 min. The The results were presented as mean values ±SE. absorbance of the colour complex was determined at Mean concentrations of cryoprotectant substances in 630 nm.
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