Gordon R. Ultsch

Physiological regulation and conformation: a BASIC program for the determination of critical points

A BASIC program is given that fits two-segmented straight lines. It is applicable for analysis of data concerning the physiological response of an organism to varying environmental conditions where the response of the organism is to regulate some physiological parameter over a range of a relevant environmental variable (zone of regulation) and to fail to regulate that parameter over some more stressful range (zone of conformation). The program identifies as an example a critical point where the shift from metabolic regulation of O2 consumption to metabolic O2 conformation occurs (Pc, critical O2 tension). A discussion is presented of the relative merits of our method and that of Nickerson, Facey, and Grossman (in this issue), which addresses the same problem.

ECOLOGY AND PHYSIOLOGY OF HIBERNATION AND OVERWINTERING AMONG FRESHWATER FISHES, TURTLES, AND SNAKES

1. Freshwater fishes are the most northerly of freshwater ectotherms, followed by frogs. North American freshwater snakes, turtles, and salamanders do not range farther north than southernmost Canada.

The ecology of overwintering among turtles: where turtles overwinter and its consequences

Turtles are a small taxon that has nevertheless attracted much attention from biologists for centuries. However, a major portion of their life cycle has received relatively little attention until recently ‐ namely what turtles are doing, and how they are doing it, during the winter. In the northern parts of their ranges in North America, turtles may spend more than half of their lives in an overwintering state. In this review, I emphasise the ecological aspects of overwintering among turtles, and consider how overwintering stresses affect the physiology, behaviour, distributions, and life histories of various species.

Molecular systematics, phylogeography, and the effects of pleistocene glaciation in the painted turtle (Chrysemys picta) complex

Abstract.— The painted turtle, Chrysemys picta, is currently recognized as a continentally distributed polytypic species, ranging across North America from southern Canada to extreme northern Mexico. We analyzed variation in the rapidly evolving mitochondrial control region (CR) in 241 turtles from 117 localities across this range to examine whether the painted turtle represents a continentally distributed species based on molecular analysis. We found strong support for the novel hypothesis that C. p. dorsalis is the sister group to all remaining Chrysemys, with the remaining Chrysemys falling into a single, extremely wide‐ranging and genetically undifferentiated species. Given our goal of an evolu‐tionarily accurate taxonomy, we propose that two evolutionary lineages be recognized as species within Chrysemys: C. dorsalis (Agassiz 1857) in the southern Mississippi drainage region, and C. picta (Schneider 1783) from the rest of the range of the genus. Neither molecular nor recent morphological analyses argue for the hybrid origin of C. p. marginata as previously proposed. Within C. picta, we find evidence of at least two independent range expansions into previously glaciated regions of North America, one into New England and the other into the upper Midwest. We further find evidence of a massive extinction/recolonization event across the Great Plains/Rocky Mountain region encompassing over half the continental United States. The timing and extent of this colonization is consistent with a recently proposed regional aridification as the Laurentide ice sheets receded approximately 14,000 years ago, and we tentatively propose this paleoclimatological event as a major factor shaping genetic variation in Chrysemys.

Physiological ecology of aquatic overwintering in ranid frogs.

In cold‐temperate climates, overwintering aquatic ranid frogs must survive prolonged periods of low temperature, often accompanied by low levels of dissolved oxygen. They must do so with the energy stores acquired prior to the onset of winter. Overwintering mortality is a significant factor in their life history, occasionally reaching 100% due to freezing and/or anoxia. Many species of northern ranid frogs overwinter in the tadpole stage, which increases survival during hypoxic episodes relative to adults, as well as allowing for larger sizes at metamorphosis. At temperatures below 5 °C, submerged ranid frogs are capable of acquiring adequate oxygen via cutaneous gas exchange over a wide range of ambient oxygen partial pressures (PO2), and possess numerous physiological and behavioural mechanisms that allow them to maintain normal rates of oxygen uptake across the skin at a relatively low PO2. At levels of oxygen near and below the critical PO2 that allows for aerobic metabolism, frogs must adopt biochemical mechanisms that act to minimise oxygen utilisation and assist in maintaining an aerobic state to survive overwintering. These mechanisms include alterations in mitochondrial metabolism and affinity, changes in membrane permeability, alterations in water balance, and reduction in cellular electrochemical gradients, all of which lead to an overall reduction in whole‐animal metabolism. Winter energetic requirements are fueled by the energy stores in liver, muscle, and fat depots, which are likely to be sufficient when the water is cold and well oxygenated. However, under hypoxic conditions fat stores cannot be utilised efficiently and glycogen stores are used up rapidly due to recruitment of anaerobiosis. Since ranid frogs have minimal tolerance to anoxia, it is untenable to suggest that they spend a significant portion of the winter buried in anoxic mud, but instead utilise a suite of behavioural and physiological mechanisms geared to optimal survival in cold, hypoxic conditions.

The viability of nearctic freshwater turtles submerged in anoxia and normoxia at 3 and 10°C

1. 1. Survival times of temperature-acclimated freshwater turtles submerged in normoxic and anoxic water were determined. 2. 2. Juvenile Chrysemys scripta from Alabama and adult Chrysemys picta bellii from Wisconsin exhibited the maximal survival times of the 10 species and subspecies investigated, both being able to survive at least a half-year of submergence at 3°C in normoxic water. 3. 3. Minimal viability was exhibited by Sternotherus odoratus and Trionyx spiniferus submerged in anoxia at 10°C (5.2 and 2.6 days, respectively). 4. 4. All species lived longer in normoxic water than in anoxic water, attesting to the importance of extrapulmonary gas exchange during submergence at low temperature. 5. 5. While freshwater turtles are often reputed to overwinter buried in mud, which is an anoxic microenvironment, this behaviour seems unlikely for southern Trionyx and Sternotherus, although it may be possible for northern Chrysemys.

Acid-base regulation in response to environmental hypercapnia in two aquatic salamanders, Siren lacertina and Amphiuma means.

The partial pressure of CO2 (PCO2) in certain areas of the aquatic habitat of the salamanders Siren lacertina and Amphiuma means frequently rises to values of up to 60 mm Hg. This ambient hypercapnia occurs due to hindrance of gas exchange between water and air caused by dense water-surface vegetation. In order to investigate the acid-base regulation in response to the respiratory acidosis, which wound be expected to result from the high CO2 conductance of the amphibian skin, specimens of both species were subjected to water PCO2 of 47 mm Hg while having free access to normocapnic air in a closed water recirculation system. Arterial PCO2 rose considerably from 12 to 35 mm Hg in Siren and from 17 to 36 mm Hg in Amphiuma. The resultant fall in plasma pH remained uncompensated, whereas intracellular pH of white muscle and heart muscle of Siren were little affected owing to elevated intracellular bicarbonate concentrations. The bicarbonate accumulated in the intracellular compartments was in part produced by intracellular and extracellular nonbicarbonate buffering, and in part gained from the environment in exchange for Cl- ions. Elevated water bicarbonate concentration or bicarbonate infusion into Siren had no effect on the acid-base regulation. These data suggest that the availability of bicarbonate is not a limiting factor for extracellular compensation of increased PCO2, but that the threshold of the bicarbonate-regulating structures is simply not readjusted in hypercapnia. This type of regulation may have evolved as a result of the specific environmental conditions of these animals and may be considered as an energetically efficient way of maintaining a constant milieu for the pH-sensitive intracellular structures.

A theoretical and experimental investigation of the relationships between metabolic rate, body size, and oxygen exchange capacity.

Abstract The influence of body size upon the decrease in weight-specific metabolic rate of organisms with increasing size is discussed. It is suggested that metabolic rate is closely correlated with, and perhaps dependent upon, the ability of an organism to obtain oxygen from the external environment. A model is presented that illustrates the advantage of having a decreasing weight-specific metabolic rate with increasing body size, rather than a linear relationship between the two. Support for the model is presented in the form of a literature review and with experimentation conducted with the aquatic salamander Siren lacertina .

Gas exchange, hypercarbia and acid-base balance, paleoecology, and the evolutionary transition from water-breathing to air-breathing among vertebrates

The evolutionary transition from water-breathing to air-breathing among vertebrates was accompanied by a shift in acid-base status from a low-PCO2, low [HCO3−] acid-base status to a high-PCO2, high-[HCO3−] acid-base status. It has been hypothesized that this change occurred concomitant with the reduced ventilation rate associated with breathing O2-rich (relative to water) air, and that the integument was used in the initial stages of the transition as a primary site for CO2 elimination. Decoupling of O2 and CO2 exchange thereby avoided a respiratory acidosis that would be associated with the relative hypoventilation expected of protoamphibians while they were air-breathing. However, at least some primitive amphibians appear to have had integuments and body sizes that would make it unlikely that the skin could be a primary site for either O2 uptake or CO2 elimination, which casts doubt on any general theory that requires the skin to play a major role in acid-base balance in early amphibians. In this review, I survey the responses of lower vertebrates to hypercarbia and the role of their integument in gas exchange, and suggest that protoamphibians may have inhabited aquatic environments that were hypercarbic, and conclude that they therefore already may have had an acid-base status similar to terrestrial forms (i.e., high-PCO2, high [HCO3−]) before they emerged onto land, which would obviate the need for a gas-permeable integument.

The Comparative Physiology of Diving in North American Freshwater Turtles. I. Submergence Tolerance, Gas Exchange, and Acid-Base Balance

The responses to prolonged diving in a representative of each of the four families of North American freshwater turtles (Chelydridae, Emydidae, Kinosternidae, Trionychidae) were investigated. For turtles submerged at 10 C in anoxic (N₂-equilibrated) and normoxic (aerated) water, we found: (1) Survival times in anoxia (days) were 2.6 (Trionyx), 5.2 (Sternotherus), 8.5 (Chelydra), and 17.0 (Chrysemys); the corresponding survival times in normoxia were >100, >100, 14.2, and 29.3. The differences between survival in anoxic and normoxic water were significant in all species except Chelydra. (2) The acid-base responses of Trionyx and Sternotherus were similar, apparently as a result of the efficient use of extrapulmonary gas exchange in these species. The lack of such efficient aquatic respiration was evident in both Chelydra and Chrysemys, whose acid-base responses were similar to each other but very different from those of the other species. (3) Buffer capacities ([HCO₃⁻]/pH) of the blood were -8.81 (Chelydra), -12.6 (Chrysemys), -14.0 (Trionyx), and -17.0 (Sternotherus). These values are well below those of diving mammals and birds. (4) Hematocrit increased in all noncatheterized turtles. After 100 days of normoxic submergence, the increase in Trionyx was from 26.0% to 34.9%; (5) Turtles of all four species died when the blood pH fell by about 1.0 pH unit, regardless of whether the acidosis was metabolic or combined respiratory and metabolic. Ecological considerations of these findings are discussed, particularly with regard to the assumed long-term submergence associated with hibernation in the northern portions of the ranges of these species. We suggest that the superior anaerobic capabilities of freshwater turtles may be the result of selection for long-term wintertime submergence rather than for warm-weather diving.