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Journal articles on the topic 'Estivation'

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Published: 4 June 2021

Last updated: 5 February 2022

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1

REES, BERNARD B., and STEVEN C. HAND. "Heat Dissipation, Gas Exchange and Acid-Base Status in the Land Snail Oreohelix During Short-Term Estivation." Journal of Experimental Biology 152, no. 1 (September 1, 1990): 77–92. http://dx.doi.org/10.1242/jeb.152.1.77.

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Within 4 days following entry into estivation, heat dissipation and oxygen consumption by the land snail Oreohelix spp. decreased by 83% compared to standard non-estivating rates. During both non-estivating and estivating conditions, the quantity of heat dissipated per mole of O2 consumed was indicative of a completely aerobic metabolism. This calorimetric-respirometric (C/R) ratio was −461±12 kJ mol−1O2 (S.E.M., N=5) under standard non-estivating conditions and −464±26 kJ mol−1O2 (N=4) during estivation. Respiratory exchange ratios reflected a primary dependence upon carbohydrate as a metabolic substrate during both states. Carbon dioxide retention occurred during the first 36h of estivation, resulting in an increase in hemolymph PCOCO2 and a decrease in pH. The respiratory acidosis during short-term estivation was not compensated by elevation of hemolymph [HCO3−] above levels predicted from the in vitro nonbicarbonate buffer value of hemolymph. A brief period of rapid CO2 release, which caused hemolymph PCOCO2 and pH to return to pre-estivation values, preceded the increase in O2 consumption during arousal. Exposure of nonestivating snails to 4.67 kPa PCOCO2 (1 kPa=7.5 mmHg) caused a rapid and fully reversible 50% suppression of respiration rate. The temporal nature of CO2 retention and release during entry into and arousal from estivation, and the suppression of O2 consumption by artificial hypercapnia, support the hypothesis that elevated PCOCO2. or the resultant acidosis may contribute to metabolic suppression during estivation by land snails.

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2

Reilly, Beau D., David I. Schlipalius, Rebecca L. Cramp, Paul R. Ebert, and Craig E. Franklin. "Frogs and estivation: transcriptional insights into metabolism and cell survival in a natural model of extended muscle disuse." Physiological Genomics 45, no. 10 (May 15, 2013): 377–88. http://dx.doi.org/10.1152/physiolgenomics.00163.2012.

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Green-striped burrowing frogs ( Cyclorana alboguttata ) survive in arid environments by burrowing underground and entering into a deep, prolonged metabolic depression known as estivation. Throughout estivation, C. alboguttata is immobilized within a cast-like cocoon of shed skin and ceases feeding and moving. Remarkably, these frogs exhibit very little muscle atrophy despite extended disuse and fasting. Little is known about the transcriptional regulation of estivation or associated mechanisms that may minimize degradative pathways of atrophy. To investigate transcriptional pathways associated with metabolic depression and maintenance of muscle function in estivating burrowing frogs, we assembled a skeletal muscle transcriptome using next-generation short read sequencing and compared gene expression patterns between active and 4 mo estivating C. alboguttata . This identified a complex suite of gene expression changes that occur in muscle during estivation and provides evidence that estivation in burrowing frogs involves transcriptional regulation of genes associated with cytoskeletal remodeling, avoidance of oxidative stress, energy metabolism, the cell stress response, and apoptotic signaling. In particular, the expression levels of genes encoding cell cycle and prosurvival proteins, such as serine/threonine-protein kinase Chk1, cell division protein kinase 2, survivin, and vesicular overexpressed in cancer prosurvival protein 1, were upregulated during estivation. These data suggest that estivating C. alboguttata are able to regulate the expression of genes in several major cellular pathways critical to the survival and viability of cells, thus preserving muscle function while avoiding the deleterious consequences often seen in laboratory models of muscle disuse.

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3

Bell, Ryan A. V., Neal J. Dawson, and Kenneth B. Storey. "Insights into the In Vivo Regulation of Glutamate Dehydrogenase from the Foot Muscle of an Estivating Land Snail." Enzyme Research 2012 (March 26, 2012): 1–10. http://dx.doi.org/10.1155/2012/317314.

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Land snails, Otala lactea, survive in seasonally hot and dry environments by entering a state of aerobic torpor called estivation. During estivation, snails must prevent excessive dehydration and reorganize metabolic fuel use so as to endure prolonged periods without food. Glutamate dehydrogenase (GDH) was hypothesized to play a key role during estivation as it shuttles amino acid carbon skeletons into the Krebs cycle for energy production and is very important to urea biosynthesis (a key molecule used for water retention). Analysis of purified foot muscle GDH from control and estivating conditions revealed that estivated GDH was approximately 3-fold more active in catalyzing glutamate deamination as compared to control. This kinetic difference appears to be regulated by reversible protein phosphorylation, as indicated by ProQ Diamond phosphoprotein staining and incubations that stimulate endogenous protein kinases and phosphatases. The increased activity of the high-phosphate form of GDH seen in the estivating land snail foot muscle correlates well with the increased use of amino acids for energy and increased synthesis of urea for water retention during prolonged estivation.

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4

WHITWAM, ROSS E., and KENNETH B. STOREY. "Pyruvate Kinase from the Land Snail Otala Lactea: Regulation by Reversible Phosphorylation During Estivation and Anoxia." Journal of Experimental Biology 154, no. 1 (November 1, 1990): 321–37. http://dx.doi.org/10.1242/jeb.154.1.321.

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Pyruvate kinase (PK) from tissues of the desert snail Otala lactea (Müller) undergoes a stable modification of its kinetic properties during estivation or in response to anoxia stress. In foot muscle and mantle, the kinetic changes induced by either state were virtually identical and were consistent with a less active enzyme form in estivation or anoxia: S0.5 PEP increased, and I50 values for Mg-ATP and L-alanine decreased, compared to the enzyme in control (aroused) snails. Estivation and anoxia also changed the properties of PK from hepatopancreas; some changes were consistent with a more active enzyme form (So.5 PEP decreased, I50 values for Mg-ATP and L-alanine increased) but the enzyme lost all sensitivity to the potent activator fructose-l,6-bisphosphate. A time course of changes in I50 Mg-ATP for foot PK and S0.5 PEP for hepatopancreas PK revealed that estivation-induced changes in enzyme properties occurred between 12 and 48 h after snails were deprived of access to food and water, whereas the reversal of these changes occurred within as little as lOmin in foot muscle after arousal was initiated. The molecular basis of the stable modification of PK kinetics appears to be reversible protein phoshorylation. The action of added cyclic-AMP-dependent protein kinase on foot or hepatopancreas PK from control (aroused) snails changed PK kinetic parameters to those characteristic of the enzyme form in estivating animals; the addition of stimulators of endogenous cyclic-GMPdependent protein kinase or protein kinase C had the same effect. Conversely, treatment with added phosphatases reconverted the properties of foot muscle PK from estivating snails to those characteristic of the control enzyme. The data suggest that reversible phosphorylation control over the activity state of regulatory enzymes of glycolysis is one mechanism contributing to the overall metabolic rate depression of the estivating state.

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5

Bishop, Tammie, Julie St-Pierre, and Martin D. Brand. "Primary causes of decreased mitochondrial oxygen consumption during metabolic depression in snail cells." American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 282, no. 2 (February 1, 2002): R372—R382. http://dx.doi.org/10.1152/ajpregu.00401.2001.

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Cells isolated from the hepatopancreas of estivating snails ( Helix aspersa) have strongly depressed mitochondrial respiration compared with controls. Mitochondrial respiration was divided into substrate oxidation (which produces the mitochondrial membrane potential) and ATP turnover and proton leak (which consume it). The activity of substrate oxidation (and probably ATP turnover) decreased, whereas the activity of proton leak remained constant in estivation. These primary changes resulted in a lower mitochondrial membrane potential in hepatopancreas cells from estivating compared with active snails, leading to secondary decreases in respiration to drive ATP turnover and proton leak. The respiration to drive ATP turnover and proton leak decreased in proportion to the overall decrease in mitochondrial respiration, so that the amount of ATP turned over per O2 consumed remained relatively constant and aerobic efficiency was maintained in this hypometabolic state. At least 75% of the total response of mitochondrial respiration to estivation was caused by primary changes in the kinetics of substrate oxidation, with only 25% or less of the response occurring through primary effects on ATP turnover.

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6

Ferreira, Marcus V. R., Antonieta C. R. Alencastro, and Marcelo Hermes-Lima. "Role of antioxidant defenses during estivation and anoxia exposure in the freshwater snail Biomphalaria tenagophila (Orbigny, 1835)." Canadian Journal of Zoology 81, no. 7 (July 1, 2003): 1239–48. http://dx.doi.org/10.1139/z03-104.

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The effects of 24 h of exposure to underwater anoxia and 15 days of estivation (at 2627°C) on the enzymatic antioxidant system of the hepatopancreas of the freshwater snail Biomphalaria tenagophila (Planorbidae) are described. The effect of 24 h of recovery was also investigated. Catalase activity dropped by 31% during 24 h of anoxia, and superoxide dismutase (SOD) activity was reduced by 43% during the 15 days of estivation. This is consistent with the overall decrease in metabolic rate during estivation or anoxia. Indeed, the heartbeat diminished by 2836% during estivation (determination was possible for only 4 days) and by 66% after 24 h of anoxia. On the other hand, selenium-dependent glutathione peroxidase (Se-GPX) activity increased during anoxia (from 10 to 14 mU/mg protein) and estivation (by 14%). Glutathione S-transferase (GST) and glutathione reductase activities remained unchanged during estivation and anoxia. Glucose 6-phosphate dehydrogenase activity was unchanged during estivation and recovery. Recovery restored SOD activity. Catalase, Se-GPX, and GST activities during recovery were significantly lower than those of the respective controls. Lipid peroxidation, determined as the level of thiobarbituric acid-reactive substances, was unchanged in the hepatopancreas after 15 days of estivation and 26 h of recovery from estivation. It is possible that the increase in Se-GPX activity during anoxia and estivation, and the maintenance of GST activity, are relevant in minimizing the effects of reactive oxygen species that can be formed upon resumption of aerobic metabolism. Thus, B. tenagophila may have a biochemical strategy of preparation for oxidative stress such as that observed in several other species of anoxia/hypoxia-tolerant animals.

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7

Fishman, Alfred P., Allan I. Pack, Richard G. Delaney, and Raymond J. Galante. "Estivation inProtopterus." Journal of Morphology 190, S1 (1986): 237–48. http://dx.doi.org/10.1002/jmor.1051900416.

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8

Hermes-Lima, M., and K. B. Storey. "Antioxidant defenses and metabolic depression in a pulmonate land snail." American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 268, no. 6 (June 1, 1995): R1386—R1393. http://dx.doi.org/10.1152/ajpregu.1995.268.6.r1386.

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During arousal from estivation oxygen consumption by land snails (Otala lactea) increases severalfold. To determine whether snails prepared for an accompanying rise in the rates of oxyradical generation by altering their antioxidant defense mechanisms, changes in the activities of antioxidant enzymes and lipid peroxidation products were quantified in foot and hepatopancreas of control, 30-day estivating, and aroused snails. Compared with controls, estivating O. lactea showed significant increases in the activities of foot muscle superoxide dismutase (SOD) (increasing by 56-67%), catalase (51-72%), and glutathione S-transferase (79-108%), whereas, in hepatopancreas, SOD (57-78%) and glutathione peroxidase (93-144%) increased. Within 40 min after arousal began, hepatopancreas glutathione peroxidase activity had returned to control values, but SOD showed a further 70% increase in activity but then returned to control levels by 80 min. Estivation had no effect on total glutathione (GSH + 2 GSSG) concentrations in tissues, but GSSG content had increased about twofold in both organs of 30-day dormant snails. Lipid peoxidation (quantified as thiobarbituric acid reactive substances) was significantly enhanced at the onset of arousal from dormancy, indicating that oxidative stress and tissue damage occurred at this time. The data suggest that antioxidant defenses in snail organs are increased while snails are in the hypometabolic state as a preparation for oxidative stress during arousal.

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9

BROOKS, STEPHEN P., and KENNETH B. STOREY. "Glycolytic Enzyme Binding and Metabolic Control in Estivation and Anoxia in the Land Snail Otala Lactea." Journal of Experimental Biology 151, no. 1 (July 1, 1990): 193–204. http://dx.doi.org/10.1242/jeb.151.1.193.

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The mechanisms controlling glycolytic rate were examined in foot muscle of the terrestrial snail Otala lactea (Miiller) (Pulmonata, Helicidae), during short and long periods of estivation and anoxia. Binding associations between glycolytic enzymes and the particulate fraction of the cell were assessed in both states. The percentage of enzyme activity bound to particulate matter decreased significantly over the short term (4 days estivation and 14.5 h anoxia); significant changes were seen for hexokinase (HK), phosphofructokinase (PFK), aldolase and lactate dehydrogenase (LDH) in estivation and, for these enzymes plus triosephosphate isomerase and pyruvate kinase (PK), in anoxia. Over the longer term in estivation (22 days) and anoxia (45 h), enzyme binding returned to control values. Tissue content of fructose-2,6-bisphosphate, a potent phosphofructokinase activator, decreased under all experimental conditions. Total glycogen phosphorylase activity decreased during short-term anoxia (14.5 h) and during long-term estivation (22 days), but the percentage of the active a form decreased significantly during anoxia only. Significant changes in the maximal activities of several enzymes were observed during both estivation and anoxia. Decreases inthe maximal activity of HK, PFK, glyceraldehyde-3-phosphate dehydrogenase, phosphoglycerate kinase (PGK) and LDH were observed during long-term estivation. Increases in PGK and PK maximal activity in short-term anoxia and aldolase and PGK in long-term anoxia were also observed. These results suggest that changes in glycolytic enzyme binding may be part of an immediate mechanism used to cause a rapid decrease in glycolytic flux and initiate glycolytic rate depression, which also includes a reduction of fructose-2,6-bisphosphate content and decreased glycogen phosphorylase activity. In the long term, however, control of snail glycolytic rate is reorganized, so that enzyme binding associations revert to the control values. In the long term, then, control is mediated by lower fructose- 2,6-bisphosphate concentrations and, during estivation, also by a decrease in maximal enzyme activities.

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10

Hermes-Lima, Marcelo, and Kenneth B. Storey. "Xanthine Oxidase and Xanthine Dehydrogenase from an Estivating Land Snail." Zeitschrift für Naturforschung C 50, no. 9-10 (October 1, 1995): 685–94. http://dx.doi.org/10.1515/znc-1995-9-1015.

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Abstract During arousal from estivation in land snails. Otala lactea, active metabolic functions are restored within minutes and oxygen consumption increases dramatically. During the transition from the hypoxic conditions of estivation to normoxia it is possible that xanthine oxidase (XO ) in hepatopancreas contributes to the observed lipid peroxidation. Using a fluorometric assay that is based on the oxidation of pterin, the activities and some properties of XO and XO+XDH (sum of XO and xanthine dehydrogenase activities) were measured in hepatopancreas extracts. Km values for pterin for XO and X O +XDH were 9 and 6 μm, respectively, and the Km of XDH for methylene blue was 5 μm . Both XO +XDH and XO activities were inhibited by allopurinol (I50 = 2 μm ) , pre-incubation at 40 °C, and by 5 min H2O2 pre-exposure. Inclusion of azide in the reaction promoted a rise of approximately 70-fold in the inactivation power of H2O2 due to inhibition of high endogenous catalase activity. The /so for H2O2 of XO +XDH and XO activities in the presence of azide was 0.04 and 0.11 mM , respectively. Unlike the situation for mammalian XO. a previous reduction of O. lactea XO (by pterin) was not necessary to make the enzyme susceptible to H2O2 effects. Interestingly, methylene blue partially prevented both heat- and H20 2-induced inactivation of XO +XDH activity. These data indicate that the formation of an enzyme-methylene blue complex induces protection against heat and oxidative damage at the FAD-active site. Both XO and XO +XDH activities were significantly higher in snails after 35 days of estivation compared with active snails 24 h after arousal from dormancy. The ratio of XO /(XO +XDH) activities was also slightly increased in estivating O. lactea (from 0.07 to 0.09; P < 0.025). XO activity was 0.03 nmol · min-1 · mg protein-1 in estivating snails. Compared with hepatopancreas catalase, XO activity is probably too low to contribute significantly to the net generation of oxyradicals, and hence to peroxidative damage. Rather, the low potential of XO to induce oxidative stress may constitute an adaptive advantage for O. lactea during arousal periods

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11

Hoyeck, Myriam P., Hanane Hadj-Moussa, and Kenneth B. Storey. "Estivation-responsive microRNAs in a hypometabolic terrestrial snail." PeerJ 7 (February 20, 2019): e6515. http://dx.doi.org/10.7717/peerj.6515.

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When faced with extreme environmental conditions, the milk snail (Otala lactea) enters a state of dormancy known as estivation. This is characterized by a strong reduction in metabolic rate to <30% of normal resting rate that is facilitated by various behavioural, physiological, and molecular mechanisms. Herein, we investigated the regulation of microRNA in the induction of estivation. Changes in the expression levels of 75 highly conserved microRNAs were analysed in snail foot muscle, of which 26 were significantly upregulated during estivation compared with controls. These estivation-responsive microRNAs were linked to cell functions that are crucial for long-term survival in a hypometabolic state including anti-apoptosis, cell-cycle arrest, and maintenance of muscle functionality. Several of the microRNA responses by snail foot muscle also characterize hypometabolism in other species and support the existence of a conserved suite of miRNA responses that regulate environmental stress responsive metabolic rate depression across phylogeny.

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12

Pakay, Julian L., Philip C. Withers, Andrew A. Hobbs, and Michael Guppy. "In vivo downregulation of protein synthesis in the snailHelix apersaduring estivation." American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 283, no. 1 (July 1, 2002): R197—R204. http://dx.doi.org/10.1152/ajpregu.00636.2001.

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Protein synthesis is downregulated during metabolic depression in a number of systems where the metabolic depression is effected by obvious extrinsic cues. The metabolic depression of the estivating land snail Helix apersa occurs in the absence of any obvious physiological stress and has an intrinsic component independent of temperature, pH, O2status, or osmolality. We show that this metabolic depression is accompanied by a downregulation of protein synthesis in vivo. The rate of protein synthesis decreases in two major tissues during estivation: to 23% and 53% of the awake rate in hepatopancreas and foot muscle, respectively. We show from calculations of the theoretical contribution of protein synthesis to total O2consumption that the depression of protein synthesis must be a significant, obligate, in vivo component of metabolic depression in H. aspersa.

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13

Frick, N. T., J. S. Bystriansky, Y. K. Ip, S. F. Chew, and J. S. Ballantyne. "Cytochrome c oxidase is regulated by modulations in protein expression and mitochondrial membrane phospholipid composition in estivating African lungfish." American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 298, no. 3 (March 2010): R608—R616. http://dx.doi.org/10.1152/ajpregu.90815.2008.

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We examined some of the potential mechanisms lungfish ( Protopterus dolloi ) use to regulate cytochrome c oxidase (CCO), during metabolic depression. CCO activity was reduced by 67% in isolated liver mitochondria of estivating fish. This was likely accomplished, in part, by the 46% reduction in CCO subunit I protein expression in the liver. No change in the mRNA expression levels of CCO subunits I, II, III, and IV were found in the liver, suggesting CCO is under translational regulation; however, in the kidney, messenger limitation may be a factor as the expression of subunits I and II were depressed (∼10-fold) during estivation, suggesting tissue-specific mechanisms of regulation. CCO is influenced by mitochondrial membrane phospholipids, particularly cardiolipin (CL). In P. dolloi , the phospholipid composition of the liver mitochondrial membrane changed during estivation, with a ∼2.3-fold reduction in the amount of CL. Significant positive correlations were found between CCO activity and the amount of CL and phosphatidylethanolamine within the mitochondrial membrane. It appears CCO activity is regulated through multiple mechanisms in P. dolloi , and individual subunits of CCO are regulated independently, and in a tissue-specific manner. It is proposed that altering the amount of CL within the mitochondrial membrane may be a means of regulating CCO activity during metabolical depression in the African lungfish, P. dolloi .

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14

Wu, Cheng-Wei, Shannon N. Tessier, and Kenneth B. Storey. "Regulation of the insulin–Akt signaling pathway and glycolysis during dehydration stress in the African clawed frog Xenopus laevis." Biochemistry and Cell Biology 95, no. 6 (December 2017): 663–71. http://dx.doi.org/10.1139/bcb-2017-0117.

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Estivation is an adaptive stress response utilized by some amphibians during periods of drought in the summer season. In this study, we examine the regulation of the insulin signaling cascade and glycolysis pathway in the African clawed frog Xenopus laevis during the dehydration stress induced state of estivation. We show that in the brain and heart of X. laevis, dehydration reduces the phosphorylation of the insulin growth factor-1 receptor (IGF-1R), and this is followed by similar reductions in the phosphorylation of the Akt and mechanistic target of rapamycin (mTOR) kinase. Interestingly, phosphorylation levels of IGF-1R and mTOR were not affected in the kidney, and phosphorylation levels of P70S6K and the ribosomal S6 protein were elevated during dehydration stress. Animals under estivation are also susceptible to periods of hypoxia, suggesting that glycolysis may also be affected. We observed that protein levels of many glycolytic enzymes remained unchanged during dehydration; however, the hypoxia response factor-1 alpha (HIF-1α) protein was elevated by greater than twofold in the heart during dehydration. Overall, we provide evidence that shows that the insulin signaling pathway in X. laevis is regulated in a tissue-specific manner during dehydration stress and suggests an important role for this signaling cascade in mediating the estivation response.

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15

Konno, Norifumi, Susumu Hyodo, Yoko Yamaguchi, Kouhei Matsuda, and Minoru Uchiyama. "Vasotocin/V2-Type Receptor/Aquaporin Axis Exists in African Lungfish Kidney but Is Functional Only in Terrestrial Condition." Endocrinology 151, no. 3 (February 10, 2010): 1089–96. http://dx.doi.org/10.1210/en.2009-1070.

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The vasopressin/vasotocin (VT)-V2-type receptor (V2R)-aquaporin (AQP)-2 axis plays a pivotal role in renal water reabsorption in tetrapods. It is widely thought that this axis evolved with the emergence of the tetrapods, reflecting a requirement of water retention in terrestrial environment. Here we report that lungfish, the closest living relatives of tetrapods, already possess a system similar to the VT-V2R-AQP2 axis in the kidney, but the system is functional only in the terrestrial estivating condition. We cloned a novel AQP paralogous to AQP0. The water permeability of Xenopus oocytes was increased by injection with the AQP cRNA and was further facilitated by preincubation with cAMP. In the kidney of estivating lungfish, the AQP protein was localized on the apical plasma membrane of the late distal tubule and was colocalized with basolateral V2R. By contrast, we found only little expression of the AQP mRNA and protein in the kidney of lungfish in aquatic condition. The expression levels of mRNA and protein were dramatically increased during estivation and decreased again by reacclimation of estivating lungfish to water. The AQP mRNA levels positively correlated with the VT mRNA levels in the hypothalamus, suggesting that the AQP exerts tubular antidiuretic action under control of VT. Because the tetrapod AQP2/AQP5 lineage is considered to be evolved from duplication of an AQP0 gene, the paralogous AQP0 in the lungfish probably represents ancestral molecule for tetrapod AQP2.

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16

Wilcox, R. Stimson, and Hilmar A. Maier. "Facultative estivation in the water strider Gerris remigis." Canadian Journal of Zoology 69, no. 5 (May 1, 1991): 1412–13. http://dx.doi.org/10.1139/z91-200.

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17

Storey, Kenneth B. "Life in the slow lane: molecular mechanisms of estivation." Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 133, no. 3 (November 2002): 733–54. http://dx.doi.org/10.1016/s1095-6433(02)00206-4.

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18

Secor, S. M. "Physiological responses to feeding, fasting and estivation for anurans." Journal of Experimental Biology 208, no. 13 (July 1, 2005): 2595–609. http://dx.doi.org/10.1242/jeb.01659.

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19

Young, John Ding-E., and Eugene Taylor. "Meditation as a Voluntary Hypometabolic State of Biological Estivation." Physiology 13, no. 3 (June 1998): 149–53. http://dx.doi.org/10.1152/physiologyonline.1998.13.3.149.

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Meditation, a wakeful hypometabolic state of parasympathetic dominance, is compared with other hypometabolic conditions, such as sleep, hypnosis, and the torpor of hibernation. We conclude that there are many analogies between the physiology of long-term meditators and hibernators across the phylogenetic scale. These analogies further reinforce the idea that plasticity of consciousness remains a key factor in successful biological adaptation.

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20

Christian, Keith, Brian Green, and Rod Kennett. "Some Physiological Consequences of Estivation by Freshwater Crocodiles, Crocodylus johnstoni." Journal of Herpetology 30, no. 1 (March 1996): 1. http://dx.doi.org/10.2307/1564699.

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21

Ligon, Day B., and Paul A. Stone. "Radiotelemetry Reveals Terrestrial Estivation in Sonoran Mud Turtles (Kinosternon sonoriense)." Journal of Herpetology 37, no. 4 (December 2003): 750–54. http://dx.doi.org/10.1670/244-01n.

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22

Bayley, Mark, Johannes Overgaard, Andrea Sødergaard Høj, Anders Malmendal, Niels C. Nielsen, Martin Holmstrup, and Tobias Wang. "Metabolic Changes during Estivation in the Common Earthworm Aporrectodea caliginosa." Physiological and Biochemical Zoology 83, no. 3 (May 2010): 541–50. http://dx.doi.org/10.1086/651459.

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23

Ligon, Day B., and Charles C. Peterson. "Physiological and Behavioral Variation in Estivation among Mud Turtles (Kinosternonspp.)." Physiological and Biochemical Zoology 75, no. 3 (May 2002): 283–93. http://dx.doi.org/10.1086/342000.

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24

Nowakowska, Anna, Grażyna Świderska-Kołacz, Justyna Rogalska, and Michał Caputa. "Antioxidants and oxidative stress in Helix pomatia snails during estivation." Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 150, no. 4 (November 2009): 481–86. http://dx.doi.org/10.1016/j.cbpc.2009.07.005.

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25

Hudson, Nicholas J., Sigrid A. Lehnert, Aaron B. Ingham, Beth Symonds, Craig E. Franklin, and Gregory S. Harper. "Lessons from an estivating frog: sparing muscle protein despite starvation and disuse." American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 290, no. 3 (March 2006): R836—R843. http://dx.doi.org/10.1152/ajpregu.00380.2005.

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Long (6- to 9-mo) bouts of estivation in green-striped burrowing frogs lead to 28% atrophy of cruralis oxidative fibers ( P < 0.05) and some impairment of in vitro gastrocnemius endurance ( P < 0.05) but no significant deficit in maximal twitch force production. These data suggest the preferential atrophy of oxidative fibers at a rate slower than, but comparable to, laboratory disuse models. We tested the hypothesis that the frog limits atrophy by modulating oxidative stress. We assayed various proteins at the transcript level and verified these results for antioxidant enzymes at the biochemical level. Transcript data for NADH ubiquinone oxidoreductase subunit 1 (71% downregulated, P < 0.05) and ATP synthase (67% downregulated, P < 0.05) are consistent with mitochondrial quiescence and reduced oxidant production. Meanwhile, uncoupling protein type 2 transcription ( P = 0.31), which is thought to reduce mitochondrial leakage of reactive oxygen species, was maintained. Total antioxidant defense of water-soluble (22.3 ± 1.7 and 23.8 ± 1.5 μM/μg total protein in control and estivator, respectively, P = 0.53) and membrane-bound proteins (31.5 ± 1.9 and 42.1 ± 7.3 μM/μg total protein in control and estivator, respectively, P = 0.18) was maintained, equivalent to a bolstering of defense relative to oxygen insult. This probably decelerates muscle atrophy by preventing accumulation of oxidative damage in static protein reserves. Transcripts of the mitochondrially encoded antioxidant superoxide dismutase type 2 (67% downregulated, P < 0.05) paralleled mitochondrial activity, whereas nuclear-encoded catalase and glutathione peroxidase were maintained at control values ( P = 0.42 and P = 0.231), suggesting a dissonance between mitochondrial and nuclear antioxidant expression. Pyruvate dehydrogenase kinase 4 transcription was fourfold lower in estivators ( P = 0.11), implying that, in contrast to mammalian hibernators, this enzyme does not drive the combustion of lipids that helps spare hypometabolic muscle.

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26

Rees, B. B., and S. C. Hand. "Biochemical Correlates of Estivation Tolerance in the Mountainsnail Oreohelix (Pulmonata: Oreohelicidae)." Biological Bulletin 184, no. 2 (April 1993): 230–42. http://dx.doi.org/10.2307/1542231.

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27

Peterson, Charles C., and Paul A. Stone. "Physiological Capacity for Estivation of the Sonoran Mud Turtle,Kinosternon sonoriense." Copeia 2000, no. 3 (August 2000): 684–700. http://dx.doi.org/10.1643/0045-8511(2000)000[0684:pcfeot]2.0.co;2.

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28

Withers, PC. "Metabolic Depression During Estivation in the Australian Frogs, Neobatrachus and Cyclorana." Australian Journal of Zoology 41, no. 5 (1993): 467. http://dx.doi.org/10.1071/zo9930467.

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The standard metabolic rate (SMR) of a number of species of Western Australian frogs is similar to that predicted for other anuran amphibians. The metabolic rate during activity is elevated 10-20 times above SMR, in close agreement with other studies of the energetics of amphibian activity. Species of two genera, Neobatrachus and Cyclorana, readily enter aestivation, which involves cessation of activity, formation of an epidermal cocoon, and depression of metabolic rate below SMR. The magnitude of metabolic depression varies between species from 70 to 80% (i.e. aestivation metabolic rate is 20-30% of SMR). The variation in magnitude of metabolic depression most likely reflects, in part, the difficulty of distinguishing the early stages of aestivation from the normal resting state. Both standard and aestivating metabolic rate are strongly mass-dependent, but the magnitude of metabolic depression is remarkably consistent in a number of different genera of frogs, salamanders and fish. The metabolic rate of aestivating amphibians is similar to that predicted for a unicellular organism of equivalent body mass, but is substantially lower than the metabolic rate of aestivating mammals.

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29

Storey, Kenneth B., and Janet M. Storey. "Metabolic Rate Depression and Biochemical Adaptation in Anaerobiosis, Hibernation and Estivation." Quarterly Review of Biology 65, no. 2 (June 1990): 145–74. http://dx.doi.org/10.1086/416717.

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30

NAKAI, Tetsuro, and Makio TAKEDA. "Effect of Temperature on the Estivation of Elcysma westwoodii (Lepidoptera, Zygaenidae)." Applied Entomology and Zoology 30, no. 4 (1995): 594–96. http://dx.doi.org/10.1303/aez.30.594.

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31

Cowan, Kyra J., Justin A. MacDonald, Janet M. Storey, and Kenneth B. Storey. "Metabolic reorganization and signal transduction during estivation in the spadefoot toad." Experimental Biology Online 5, no. 1 (December 2000): 1–25. http://dx.doi.org/10.1007/s00898-000-0001-8.

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32

Dhillon, Mukesh K., Fazil Hasan, Aditya K. Tanwar, and Amarpal S. Bhadauriya. "Factors responsible for estivation in spotted stem borer, Chilo partellus (Swinhoe)." Journal of Experimental Zoology Part A: Ecological and Integrative Physiology 331, no. 6 (May 20, 2019): 326–40. http://dx.doi.org/10.1002/jez.2271.

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33

Ramnanan, Christopher J., and Kenneth B. Storey. "The regulation of thapsigargin-sensitive sarcoendoplasmic reticulum Ca2+-ATPase activity in estivation." Journal of Comparative Physiology B 178, no. 1 (August 10, 2007): 33–45. http://dx.doi.org/10.1007/s00360-007-0197-9.

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34

Storey, K. B. "Turning down the fires of life: metabolic regulation of hibernation and estivation." Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 126 (July 2000): S90. http://dx.doi.org/10.1016/s0305-0491(00)80178-9.

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35

Garnsey, RB. "Seasonal activity and estivation of lumbricid earthworms in the midlands of Tasmania." Soil Research 32, no. 6 (1994): 1355. http://dx.doi.org/10.1071/sr9941355.

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Earthworms have the ability to alleviate many soil degradational problems in Australia. An attempt to optimize this resource requires fundamental understanding of earthworm ecology. This study reports the seasonal changes in earthworm populations in the Midlands of Tasmania (<600 mm rainfall p.a.), and examines, for the first time in Australia, the behaviour and survival rates of aestivating earthworms. Earthworms were sampled from 14 permanent pastures in the Midlands from May 1992 to February 1994. Earthworm activity was significantly correlated with soil moisture; maximum earthworm activity in the surface soil was evident during the wetter months of winter and early spring, followed by aestivation in the surface and subsoils during the drier summer months. The two most abundant earthworm species found in the Midlands were Aporrectodea caliginosa (maximum of 174.8 m-2 or 55.06 g m-2) and A. trapezoides (86 m-2 or 52.03 g m-2), with low numbers of Octolasion cyaneum, Lumbricus rubellus and A. rosea. The phenology of A. caliginosa relating to rainfall contrasted with that of A. trapezoides in this study. A caliginosa was particularly dependent upon rainfall in the Midlands: population density, cocoon production and adult development of A. caliginosa were reduced as rainfall reduced from 600 to 425 mm p.a. In contrast, the density and biomass of A. trapezoides were unaffected by rainfall over the same range: cocoon production and adult development continued regardless of rainfall. The depth of earthworm aestivation during the summers of 1992-94 was similar in each year. Most individuals were in aestivation at a depth of 150-200 mm, regardless of species, soil moisture or texture. Smaller aestivating individuals were located nearer the soil surface, as was shown by an increase in mean mass of aestivating individuals with depth. There was a high mortality associated with summer aestivation of up to 60% for juvenile, and 63% for adult earthworms in 1993 in the Midlands. Cocoons did not survive during the summers of 1992 or 1994, but were recovered in 1993, possibly due to the influence of rainfall during late winter and early spring.

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36

Takada, Kaori, Kenji Kato, and Tokio Okino. "Environmental parameters and estivation of Rhyacodrilus (Tubificidae, Oligochaeta) in Lake Suwa, Japan." Ecography 15, no. 3 (July 1992): 328–33. http://dx.doi.org/10.1111/j.1600-0587.1992.tb00043.x.

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37

Giraud-Billoud, Maximiliano, María A. Abud, Juan A. Cueto, Israel A. Vega, and Alfredo Castro-Vazquez. "Uric acid deposits and estivation in the invasive apple-snail, Pomacea canaliculata." Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 158, no. 4 (April 2011): 506–12. http://dx.doi.org/10.1016/j.cbpa.2010.12.012.

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38

Cowan, Kyra J., and Kenneth B. Storey. "Urea and KCl have differential effects on enzyme activities in liver and muscle of estivating versus nonestivating species." Biochemistry and Cell Biology 80, no. 6 (December 1, 2002): 745–55. http://dx.doi.org/10.1139/o02-144.

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The effects of 300 mM urea or 300 mM KCl on the maximal activities of 25 enzymes of intermediary metabolism were assessed in extracts of liver and muscle from spadefoot toads (Scaphiopus couchii), leopard frogs (Rana pipiens), and rats to assess their sensitivity to these osmolytes. During estivation, toads can lose ~50% of total body water, and urea, which is known for its action as a protein denaturant, accumulates to 200300 mM. The data show that the maximal activities of toad liver enzymes were not affected when assayed in the presence of 300 mM urea in vitro whereas urea inhibited the activities of seven enzymes in frog and 11 enzymes in rat liver. High KCl affected 12 or 13 enzymes in liver of each species causing inhibition in eight or nine cases each, and for frog and rat enzymes, inhibition was frequently more pronounced than for urea. Both urea and KCl affected enzyme activities in muscle extracts of all three species, but whereas their effects were largely negative for frog and rat enzymes, the enzymes affected by urea or KCl in toad muscle were primarily activated by these osmolytes (six out of nine enzymes affected by urea and eight of 15 enzymes affected by KCl). Urea, KCl, and polyethylene glycol (a protein crowding agent) also had species-specific effects on the dissociation constant (Ka) for cAMP of protein kinase A. The data suggest that the accumulation of urea by water-stressed anurans not only contributes to minimizing cell volume reduction, but by doing so also limits the increase in intracellular ionic strength that occurs and thereby helps to minimize the potential inhibitory effects of high salts on metabolic enzymes.Key words: estivation, desiccation, urea, polyethylene glycol, spadefoot toad, leopard frog.

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39

Wilz, M., and G. Heldmaier. "Comparison of hibernation, estivation and daily torpor in the edible dormouse, Glis glis." Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 170, no. 7 (November 6, 2000): 511–21. http://dx.doi.org/10.1007/s003600000129.

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40

Smith, Matthew E., and Stephen M. Secor. "Physiological Responses to Fasting and Estivation for the Three-Toed Amphiuma (Amphiuma tridactylum)." Physiological and Biochemical Zoology 90, no. 2 (March 2017): 240–56. http://dx.doi.org/10.1086/689216.

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41

Whitwam, Ross E., and Kenneth B. Storey. "Regulation of Phosphofructokinase during Estivation and Anoxia in the Land Snail, Otala lactea." Physiological Zoology 64, no. 2 (March 1991): 595–610. http://dx.doi.org/10.1086/physzool.64.2.30158192.

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42

Groom, Derrick J. E., Louise Kuchel, and Jeffrey G. Richards. "Metabolic responses of the South American ornate horned frog (Ceratophrys ornata) to estivation." Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 164, no. 1 (January 2013): 2–9. http://dx.doi.org/10.1016/j.cbpb.2012.08.001.

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43

Schill, R. O., A. Reuner, and F. Brümmer. "Heat shock protein response during estivation in the Mediterranean Grunt Snail (Cantareus apertus)." Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 151, no. 1 (September 2008): S35. http://dx.doi.org/10.1016/j.cbpa.2008.05.126.

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44

Rees, Bernard B., and Steven C. Hand. "Regulation of glycolysis in the land snail Oreohelix during estivation and artificial hypercapnia." Journal of Comparative Physiology B 161, no. 3 (July 1991): 237–46. http://dx.doi.org/10.1007/bf00262304.

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45

Mueck, Kristy, Lewis E. Deaton, and Andrea Lee. "Estivation in the Apple Snail Pomacea maculata: Mobilization of Calcium Granules in the Lung." Journal of Shellfish Research 39, no. 1 (April 14, 2020): 133. http://dx.doi.org/10.2983/035.039.0113.

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46

Pakay, J. L. "The role of eukaryotic initiation factor 2 during the metabolic depression associated with estivation." Journal of Experimental Biology 206, no. 14 (July 15, 2003): 2363–71. http://dx.doi.org/10.1242/jeb.00422.

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47

Roe, John H., Arthur Georges, and Brian Green. "Energy and Water Flux during Terrestrial Estivation and Overland Movement in a Freshwater Turtle." Physiological and Biochemical Zoology 81, no. 5 (September 2008): 570–83. http://dx.doi.org/10.1086/589840.

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48

Ramnanan, C. J. "Suppression of Na+/K+-ATPase activity during estivation in the land snail Otala lactea." Journal of Experimental Biology 209, no. 4 (February 15, 2006): 677–88. http://dx.doi.org/10.1242/jeb.02052.

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49

Sun, Jin, Huawei Mu, Huoming Zhang, Kondethimmanahalli H. Chandramouli, Pei-Yuan Qian, Chris Kong Chu Wong, and Jian-Wen Qiu. "Understanding the Regulation of Estivation in a Freshwater Snail through iTRAQ-Based Comparative Proteomics." Journal of Proteome Research 12, no. 11 (October 2, 2013): 5271–80. http://dx.doi.org/10.1021/pr400570a.

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50

ŞEREFLİŞAN, Hülya. "The effect of different shell colors on helix lucorum (Gastropoda: Helicidae) in estivation period." Journal of Advances in VetBio Science and Techniques 6, no. 1 (April 30, 2021): 1–8. http://dx.doi.org/10.31797/vetbio.801902.

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