We explore how the thermal sensitivity of organismic performance emerges from the thermal sensitivity of the underlying component processes involved, using growth and feeding of Manduca sexta caterpillars as a model system. We measured thermal performance curves for the short-term rates of growth, consumption, protein (casein) digestion, amino acid (methionine) uptake, and respiration in fifth-instar caterpillars over a biologically realistic temperature range from 14 degrees to 42 degrees C. Growth and consumption rates increased between 14 degrees and 26 degrees C, reached a maximum value near 34 degrees C, and declined rapidly above 38 degrees C. In contrast, protein digestion rate and respiration rate increased monotonically over the entire temperature range, and amino acid uptake rate increased with temperatures up to 38 degrees C and then leveled off between 38 degrees and 42 degrees C. These results suggest that the shape and position of the thermal performance curve for growth rate--in particular the maximum at 34 degrees C and rapid decline above 38 degrees C--was most closely correlated with the thermal sensitivity of consumption rate; the declining growth performance above 38 degrees C was not associated with declines in digestion or uptake rates or with accelerated respiration rates at these temperatures.
Carbonic anhydrase activity in the extracellular fluid of lower vertebrates is considered to be minimal, either because of the absence of carbonic anhydrase or because of the presence of naturally occurring inhibitors. The presence of carbonic anhydrase activity and circulating inhibitors was measured in plasma and subcellular fractions of gill tissue in elasmobranchs and teleosts. Plasma carbonic anhydrase activity was confirmed in the former but in extremely low amounts, especially compared with activity in red cells. The activity was correlated with plasma iron concentration and red cell hemolysis, which suggests that it is a byproduct of endogenous hemolysis during red cell turnover. A subcellular fraction of dogfish gills rich in microsomes contained significantly higher carbonic anhydrase activity than previously found in teleosts, making elasmobranchs the only aquatic lower vertebrates to possess putative basolateral membrane-associated carbonic anhydrase in the gill vasculature. It is suggested that branchial membrane-associated carbonic anhydrase is correlated more with a pH and/or CO2-sensitive ventilatory drive than with the maintenance of resting CO2 excretion. The occurrence and effectiveness of plasma carbonic anhydrase inhibitors were highly species-specific, with the salmonids having the most potent inhibitor. Cross-reactivity of inhibitor to red cell carbonic anhydrase appeared to be related to phylogenetic proximity. Selection for the presence of carbonic anhydrase inhibitors in fish plasma appears to be the result of multiple physiological pressures, including preservation of red cell intracellular pH, ventilatory control, and red cell fragility.
We studied tolerance for cold in hatchling painted turtles (Chrysemys picta) from Lake Metigoshe, Bottineau County, North Dakota, to determine whether neonates in populations near the northern limit of distribution rely on a tolerance for freezing or on a capacity for supercooling to survive their first winter of life. We placed hatchlings individually into artificial hibernacula constructed in jars of damp, loamy sand and then cooled the jars to approximately -0.45 degrees C, which was below the equilibrium freezing point for water held by the sand but above that for body fluids of the neonatal turtles. A piece of ice next was placed on the surface of the sand in each jar to induce freezing of the soil water. After the soil water had frozen to an equilibrium, the temperature in the jars was lowered by 1 degrees C/d to minima averaging -2.5 degrees C, -4.5 degrees C, -6.5 degrees C, and -10.5 degrees C in different treatments. These temperatures were maintained for varying periods, so that animals in each treatment were exposed to temperatures below the equilibrium freezing point for their body fluids for a total of 11 d. Thirty of 32 hatchlings survived exposure to -2.5 degrees C; 24 of 32 survived at -4.5 degrees C; 14 of 32 withstood -6.5 degrees C; and 7 of 32 tolerated -10.5 degrees C. Freezing exotherms were detected in temperature profiles for turtles that succumbed but not in those for hatchlings that survived. Thus, the ability of hatchlings to withstand subzero temperatures for extended periods apparently requires that they avoid freezing. Although other workers contend that tolerance for freezing is the key to survival over winter by hatchling painted turtles from the region of Lake Metigoshe, our findings indicate that neonates rely primarily on their ability to remain unfrozen and supercooled.
The barrier to gas flux across the eggs of American alligators (Alligator mississippiensis) consists of a calcareous shell and an underlying shell membrane of two layers, a limiting membrane facing the embryo and a fibrous membrane facing the shell. The limiting membrane is penetrated by an immense population (averaging 341,188 cm-2) of tiny pores (averaging 0.51 micron in diameter) and a small population (averaging 190 cm-2) of large pores (averaging 34.6 microns in diameter). An estimated 6% of these pores are open at the onset of incubation, and 22%-24% are open near hatch. The shell membrane is 2.6-10 times less permeable to O2 than the shell. Its permeability nearly quadruples during incubation, is higher at the equator than elsewhere, increases more rapidly when eggs are incubated at 33 degrees C as opposed to 30 degrees C, and appears to depend primarily on its water content. In contrast, the shell's permeability to O2, as well as its water vapor conductance and the number of open pores in it, does not change significantly during incubation.
Sodium is considered the mineral most limiting to growth and reproduction of mammalian herbivores worldwide. Notwithstanding the large database on physiological adaptations to low sodium intake, information on maintenance sodium requirements and sodium dynamics of mammals is depauperate. We measured sodium intake and output in adult, nonreproductive white-tailed deer (n = 15) over four seasons to estimate daily requirements for sodium on a seasonal and an annual basis. Dietary sodium content was based on best available predictions of sodium requirements. With regression techniques, we estimated metabolic fecal excretion and endogenous urinary losses of sodium. Average daily sodium requirement, defined as the minimum sodium intake at which intake equaled excretion, was estimated to be 3.27 mg kg-1 body mass d-1. Seasonal estimates did not vary. We propose that sodium requirements for maintenance in mammalian herbivores scale to body mass at an exponent that is similar to that for metabolic rate and forage intake (0.71-0.75). Development of an allometric relationship between sodium need and body mass would permit stronger inference regarding the role of sodium in population regulation, foraging decisions, or distribution and movements of mammalian herbivores.
In this study, we asked whether within-species variation in chick resting metabolic rate was related to variation in growth and whether this relationship changed during development in three galliform species (turkey, Meleagris gallopavo, guinea fowl, Numida meleagris, and Japanese quail, Coturnix coturnix japonica). Resting metabolic rate increased by a bi- or triphasic pattern with body mass. For each phase, the relationship between metabolic rate and growth was studied by residual analysis, with two measures of growth: growth rate and body mass. Chick mass reflects the net result of accumulated growth, while hatchling mass reflects embryonic growth. In hatchlings, high metabolic rates coincided with low growth rates in turkeys and guinea fowl. These species delay initial food intake, and under these circumstances high metabolic expenditure may preclude conversion of yolk energy into body mass. No relationship was present between residual hatching metabolic rate and residual body mass. In older chicks, residual metabolic rate was positively linearly related with residual growth rate (turkeys and young quail) or residual body mass (guinea fowl and older quail). The similarity of the slopes suggests that growth rate and accumulated growth affected maintenance metabolism to the same extent throughout development. These findings suggest that growth models must take ontogenetic adjustments of metabolic rate into account in addition to costs of maintenance.
Flight muscles of the cricket Gryllus firmus are polymorphic, existing as pink or white phenotypes. White muscles are smaller in size, have reduced number and size of muscle fibers, and have reduced in vitro enzyme activities and respiration rates relative to pink muscles of newly molted, fully winged adults. G. firmus is also polymorphic for wing length. All newly molted long-winged adults exhibited the pink-muscle phenotype, while most newly molted short-winged adults exhibited the white-muscle phenotype, which resulted from arrested muscle growth. As long-winged adults aged, fully grown pink muscle was transformed into white muscle via histolysis. The substantially higher respiration rate of pink muscle likely contributes to the elevated whole-organism respiration rate of long-winged females, which has been documented previously and which is thought to divert nutrients from egg production. Histolyzed white flight muscle from long-winged crickets also exhibited significantly elevated respiration rate and enzyme activities compared with underdeveloped white muscle from short-winged adults, although these differences were not as great as those between pink and white muscles. Fecundity was much more elevated in females with white verus pink flight muscles than it was in females with short versus long wings. The fitness gain resulting from flightlessness has typically been estimated in previous studies by comparing enhanced egg production of short-winged and long-winged females, without considering the influence of flight-muscle variation. Our results suggest that the magnitude of this fitness gain has been substantially underestimated.
To investigate the energetic costs of lactation in a female mammal in relation to previous reproductive history, we compared the performance of adult female Long-Evans rats that had previously bred (multiparous) with young females that had not previously given birth (primiparous). All litters were standardized to 10 +/- 1 young. We compared maternal production (growth of pups), body mass, and energy intake (food consumption) of mothers, as well as their energy expenditure (resting oxygen consumption). The mass of litters at birth and the growth of pups during lactation did not differ according to reproductive history of the mothers. The body mass of primiparous mothers was less than that of multiparous mothers, and primiparous mothers showed an increase in mass during early lactation. To accomplish the essentially identical production of offspring under these circumstances, the primiparous mothers consumed and expended more energy than the multiparous mothers. This remarkable performance of first-time mothers results in an overall efficiency of energy allocation to reproduction amounting to only 25%, compared with 38% in multiparous mothers. The energetic inefficiency of primiparous female lactation results largely from the excessive expenditures associated with physiological and behavioral performances of first-time reproduction, together with a small component of additional expenditure due to further growth by the primiparous mothers. We suggest that this inefficiency probably contributes to the observed low reproductive success of novice breeders; furthermore, active restraint of fecundity may be an evolutionary response to the constraints of the energetic inefficiency of primiparous breeding by female mammals.
The effects of arousal from hibernation and presence of plasma androgen on the expression of mating behavior in male big brown bats (Eptesicus fuscus) were tested in a captive population exposed to seminatural conditions in central Alabama. In the mild winter of 1994-1995, flight cage temperatures never fell below 10 degrees C. Bats were never observed to enter sustained (over 2 d) torpor. They were also never observed to mate. Unmanipulated, sham-operated, and gonadectomized males and unmanipulated females were exposed to 6 d of 4 degrees C. All individuals appeared torpid, and body temperatures of monitored bats fell at least 15 degrees-20 degrees C. Plasma androgen levels of torpid unmanipulated, sham-operated, and gonadectomized males averaged 25.4 +/- 9.2, 19.7 +/- 9.1, and 1.5 +/- 0.25 ng/mL, respectively, and did not differ significantly from levels for the same groups 1 mo previous to induced torpor. When animals were returned to 23 degrees C, 57% of unmanipulated, 40% of the sham-operated, and 33% of gonadectomized males displayed mating behavior upon arousal. Almost all matings occurred within 48 h of arousal, the majority in the first 3 h. Males not exposed to low temperatures were not observed to mate. Although individuals from all three treatments mated, gonadectomized males averaged fewer mounts and copulations per individual. Androgen levels declined significantly from torpor levels in all groups 48 h after arousal. Thus, an extended period of low body temperature and arousal appeared to be a short-term activator of sexual behavior in the big brown bat; unmanipulated males were more strongly affected by this stimulus than gonadectomized males.