Scott A. Reese

The physiology of hibernation in common map turtles (Graptemys geographica)

Map turtles from Wisconsin were submerged at 3 degrees C in normoxic and anoxic water to simulate extremes of potential respiratory microenvironments while hibernating under ice. In predive turtles, and in turtles submerged for up to 150 days, plasma PO2, PCO2) pH, [Cl-], [Na+], [K+], total Mg, total Ca, lactate, glucose, and osmolality were measured; hematocrit and body mass were determined, and plasma [HCO3-] was calculated. Turtles in anoxic water developed a severe metabolic acidosis, accumulating lactate from a predive value of 1.7 to 116 mmol/l at 50 days, associated with a fall in pH from 8.010 to 7.128. To buffer lactate increase, total calcium and magnesium rose from 3.5 and 2.0 to 25.7 and 7.6 mmol/l, respectively. Plasma [HCO3-] was titrated from 44.7 to 4.3 mmol/l in turtles in anoxic water. Turtles in normoxic water had only minor disturbances of their acid-base status and ionic statuses; there was a marked increase in hematocrit from 31.1 to 51.9%. This study and field studies suggest that map turtles have an obligatory requirement for a hibernaculum that provides well-oxygenated water (e.g. rivers and large lakes rather than small ponds and swamps) and that this requirement is a major factor in determining their microdistribution.

The Physiology of Overwintering in a Turtle That Occupies Multiple Habitats, the Common Snapping Turtle (Chelydra serpentina)

Common snapping turtles, Chelydra serpentina (Linnaeus), were submerged in anoxic and normoxic water at 3°C. Periodic blood samples were taken, and PO2, PCO2, pH, [Na+], [K+], [Cl−], total Ca, total Mg, [lactate], [glucose], hematocrit, and osmolality were measured; weight gain was determined; and plasma [HCO3−] was calculated. Submergence in normoxic water caused a decrease in PCO2 from 10.8 to 6.9 mmHg after 125 d, partially compensating a slight increase in lactate and allowing the turtles to maintain a constant pH. Submergence in anoxic water caused a rapid increase in lactate from 1.8 to 168.1 mmol/L after 100 d. Associated with the increased lactate were decreases in pH from 8.057 to 7.132 and in [HCO3−] from 51.5 to 4.9 mmol/L and increases in total Ca from 2.0 to 36.6 mmol/L, in total Mg from 1.8 to 12.1 mmol/L, and in [K+] from 3.08 to 8.45 mmol/L. We suggest that C. serpentina is tolerant of anoxic submergence and therefore is able to exploit habitats unavailable to some other species in northern latitudes.

Tissue Glycogen and Extracellular Buffering Limit the Survival of Red‐Eared Slider Turtles during Anoxic Submergence at 3°C

The goal of this study was to identify the factors that limit the survival of the red‐eared slider turtle Trachemys scripta during long‐term anoxic submergence at 3°C. We measured blood acid‐base status and tissue lactate and glycogen contents after 13, 29, and 44 d of submergence from ventricle, liver, carapace (lactate only), and four skeletal muscles. We also measured plasma Ca2+, Mg2+, Na+, K+, Cl−, inorganic phosphate (Pi), lactate, and glucose. After 44 d, one of the six remaining turtles died, while the other turtles were in poor condition and suffered from a severe acidemia (blood pH = 7.09 from 7.77) caused by lactic acidosis (plasma lactate 91.5 mmol L−1). An initial respiratory acidosis attenuated after 28 d. Lactate rose to similar concentrations in ventricle and skeletal muscle (39.3–46.1 μmol g−1). Liver accumulated the least lactate (21.8 μmol g−1), and carapace accumulated the most lactate (68.9 μmol g−1). Plasma Ca2+ and Mg2+ increased significantly throughout submergence to levels comparable to painted turtles at a similar estimated lactate load. Glycogen depletion was extensive in all tissues tested: by 83% in liver, by 90% in ventricle, and by 62%–88% in muscle. We estimate that the shell buffered 69.1% of the total lactate load, which is comparable to painted turtles. Compared with painted turtles, predive tissue glycogen contents and plasma \documentclass{aastex} \usepackage{amsbsy} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{bm} \usepackage{mathrsfs} \usepackage{pifont} \usepackage{stmaryrd} \usepackage{textcomp} \usepackage{portland,xspace} \usepackage{amsmath,amsxtra} \usepackage[OT2,OT1]{fontenc} \newcommand\cyr{ \renewcommand\rmdefault{wncyr} \renewcommand\sfdefault{wncyss} \renewcommand\encodingdefault{OT2} \normalfont \selectfont} \DeclareTextFontCommand{\textcyr}{\cyr} \pagestyle{empty} \DeclareMathSizes{10}{9}{7}{6} \begin{document} \landscape

The Physiology of Hibernation in Canadian Leopard Frogs (Rana pipiens) and Bullfrogs (Rana catesbeiana)

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Geographic Variation of the Physiological Response to Overwintering in the Painted Turtle (Chrysemys picta)

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Influences of temperature and oxygen upon habitat selection by bullfrog tadpoles and three species of freshwater fishes in two Alabama strip mine ponds

Midland painted turtles from Michigan were submerged at 3 degrees C in normoxic and anoxic water. In predive, and in turtles submerged for up to 150 days, plasma PO2, PCO2, pH, [Cl-], [Na+], [K+], total Mg, total Ca, lactate, glucose, and osmolality were measured; hematocrit and mass were determined, and plasma [HCO3-] was calculated. Anoxic turtles developed a severe metabolic acidosis, accumulating lactate from a predive value of 4.4 mmol/L to a 150-day value of 185 mmol/L, associated with a fall in pH from 7.983 to 7.189. To buffer lactate increase, total calcium and magnesium rose from 3.7 and 2.6 to 58.9 and 11.8 mmol/L, respectively. Plasma [HCO3-] was titrated from 39.2 to 4.8 mmol/L in anoxic turtles. Turtles in normoxic water had only minor disturbances of their acid-base and ionic statuses, associated with a much smaller increase of lactate to 23 mmol/L; there was a marked increase in hematocrit from 29.1% to 42.1%. We suggest that it is ecologic, rather than phylogenetic, relationships that determine the responses of painted turtles to prolonged submergence associated with hibernation.

Hibernation in freshwater turtles: softshell turtles (Apalone spinifera) are the most intolerant of anoxia among North American species

Canadian northern leopard frogs (Rana pipiens) and bullfrogs (Rana catesbeiana) were acclimated to 3°C and submerged in anoxic (0–5 mmHg) and normoxic (Po2 ∼158 mmHg) water. Periodic measurements of blood Po2, Pco2, and pH were made on samples taken anaerobically from subsets of each species. Blood plasma was analyzed for [Na+], [K+], [Cl−], [lactate], [glucose], total calcium, total magnesium, and osmolality. Blood hematocrit was determined, and plasma bicarbonate concentration was calculated. Both species died within 4 d of anoxic submergence. Anoxia intolerance would rule out hibernation in mud, which is anoxic. Both species survived long periods of normoxic submergence (R. pipiens, 125 d; R. catesbeiana, 150 d) with minimal changes in acid‐base and ionic status. We conclude that ranid frogs require a hibernaculum where the water has a high enough Po2 to drive cutaneous diffusion, allowing the frogs to extract enough O2 to maintain aerobic metabolism, but that an ability to tolerate anoxia for several days may still be ecologically meaningful.

Physiology of hibernation in Rana pipiens: Metabolic rate, critical oxygen tension, and the effects of hypoxia on several plasma variables

SUMMARY We submerged hatchling western painted turtles Chrysemys picta Schneider, snapping turtles Chelydra serpentina L. and map turtles Graptemys geographica Le Sueur in normoxic and anoxic water at 3°C. Periodically, turtles were removed and whole-body [lactate] and [glycogen] were measured along with relative shell mass, shell water, and shell ash. We analyzed the shell for [Na+], [K+], total calcium, total magnesium, Pi and total CO2. All three species were able to tolerate long-term submergence in normoxic water without accumulating any lactate, indicating sufficient extrapulmonary O2 extraction to remain aerobic even after 150 days. Survival in anoxic water was 15 days in map turtles, 30 days in snapping turtles, and 40 days in painted turtles. Survival of hatchlings was only about one third the life of their adult conspecifics in anoxic water. Much of the decrease in survival was attributable to a dramatically lower shell-bone content (44% ash in adult painted turtles vs. 3% ash in hatchlings of all three species) and a smaller buffer content of bone (1.3 mmol g–1 CO2 in adult painted turtles vs. 0.13–0.23 mmol g–1 CO2 in hatchlings of the three species). The reduced survivability of turtle hatchlings in anoxic water requires that hatchlings either avoid aquatic hibernacula that may become severely hypoxic or anoxic (snapping turtles), or overwinter terrestrially (painted turtles and map turtles).