Marshall D. McCue

Starvation physiology: Reviewing the different strategies animals use to survive a common challenge

All animals face the possibility of limitations in food resources that could ultimately lead to starvation-induced mortality. The primary goal of this review is to characterize the various physiological strategies that allow different animals to survive starvation. The ancillary goals of this work are to identify areas in which investigations of starvation can be improved and to discuss recent advances and emerging directions in starvation research. The ubiquity of food limitation among animals, inconsistent terminology associated with starvation and fasting, and rationale for scientific investigations into starvation are discussed. Similarities and differences with regard to carbohydrate, lipid, and protein metabolism during starvation are also examined in a comparative context. Examples from the literature are used to underscore areas in which reporting and statistical practices, particularly those involved with starvation-induced changes in body composition and starvation-induced hypometabolism can be improved. The review concludes by highlighting several recent advances and promising research directions in starvation physiology. Because the hundreds of studies reviewed here vary so widely in their experimental designs and treatments, formal comparisons of starvation responses among studies and taxa are generally precluded; nevertheless, it is my aim to provide a starting point from which we may develop novel approaches, tools, and hypotheses to facilitate meaningful investigations into the physiology of starvation in animals.

The Effect of Meal Composition on Specific Dynamic Action in Burmese Pythons (Python molurus)

We quantified the specific dynamic action (SDA) resulting from the ingestion of various meal types in Burmese pythons (Python molurus) at 30°C. Each snake was fed a series of experimental meals consisting of amino acid mixtures, simple proteins, simple or complex carbohydrates, or lipids as well as meals of whole animal tissue (chicken breast, beef suet, and mouse). Rates of oxygen consumption were measured for approximately 4 d after feeding, and the increment above standard metabolic rate was determined and compared to energy content of the meals. While food type (protein, carbohydrate, and lipid) had a general influence, SDA was highly dependent on meal composition (i.e., amino acid composition and carbohydrate structure). For chicken breast and simple carbohydrates, the SDA coefficient was approximately one‐third the energetic content of the meal. Lard, suet, cellulose, and starch were not digested and did not produce measurable SDA. We conclude that the cost of de novo protein synthesis is an important component of SDA after ingestion of protein meals because (1) simple proteins, such as gelatin and collagen, did not stimulate levels of SDA attained after consumption of complete protein, (2) incomplete mixtures of amino acids failed to elicit the SDA of a complete mixture, and (3) the inhibition of de novo protein synthesis with the drug cycloheximide caused a more than 70% decrease in SDA. Stomach distension and mechanical digestion of intact prey did not cause measurable SDA.

Unique and shared responses of the gut microbiota to prolonged fasting: a comparative study across five classes of vertebrate hosts

Many animals face unpredictable food sources and periods of prolonged fasting, which likely present significant challenges to gut microorganisms. While several studies have demonstrated that fasting impacts the gut microbiota, experiments have not been carried out in a comparative context. We used 16S rRNA gene sequencing to document changes in colonic and cecal microbiomes of animals representing five classes of vertebrates at four time points through prolonged fasting: tilapia, toads, geckos, quail, and mice. We found differences in the starvation-induced changes in the microbiome across host species and across gut regions. Microbial phylogenetic diversity increased as a result of fasting in the colons of fish, toads, and mice, while quail exhibited a decrease in diversity; geckos exhibited no change. Microbial diversity in the cecum decreased in fish and exhibited no change in mice. Alterations in relative abundances of microbial taxa varied across hosts. Fish exhibited the most significant changes due to fasting, while geckos maintained a stable community over 28 days of fasting. We uncovered several shared responses of the microbiota across hosts. For example, all tetrapods exhibited decreases in the abundances of Coprobacillus and Ruminococcus in response to fasting. We also discuss host-mediated physiological mechanisms that may underlie these community changes.

Flight Modes in Migrating European Bee-Eaters: Heart Rate May Indicate Low Metabolic Rate during Soaring and Gliding

Background Many avian species soar and glide over land. Evidence from large birds (m b>0.9 kg) suggests that soaring-gliding is considerably cheaper in terms of energy than flapping flight, and costs about two to three times the basal metabolic rate (BMR). Yet, soaring-gliding is considered unfavorable for small birds because migration speed in small birds during soaring-gliding is believed to be lower than that of flapping flight. Nevertheless, several small bird species routinely soar and glide. Methodology/Principal Findings To estimate the energetic cost of soaring-gliding flight in small birds, we measured heart beat frequencies of free-ranging migrating European bee-eaters (Merops apiaster, m b∼55 g) using radio telemetry, and established the relationship between heart beat frequency and metabolic rate (by indirect calorimetry) in the laboratory. Heart beat frequency during sustained soaring-gliding was 2.2 to 2.5 times lower than during flapping flight, but similar to, and not significantly different from, that measured in resting birds. We estimated that soaring-gliding metabolic rate of European bee-eaters is about twice their basal metabolic rate (BMR), which is similar to the value estimated in the black-browed albatross Thalassarche (previously Diomedea) melanophrys, m b∼4 kg). We found that soaring-gliding migration speed is not significantly different from flapping migration speed. Conclusions/Significance We found no evidence that soaring-gliding speed is slower than flapping flight in bee-eaters, contradicting earlier estimates that implied a migration speed penalty for using soaring-gliding rather than flapping flight. Moreover, we suggest that small birds soar and glide during migration, breeding, dispersal, and other stages in their annual cycle because it may entail a low energy cost of transport. We propose that the energy cost of soaring-gliding may be proportional to BMR regardless of bird size, as theoretically deduced by earlier studies.

Oxygen Consumption and the Energetics of Island‐Dwelling Florida Cottonmouth Snakes

We measured oxygen consumption (V̇o2) to estimate standard metabolic rates (SMR) in cottonmouth snakes (Agkistrodon piscivorus conanti) from Seahorse Key and the adjacent peninsula of northern Florida. The island population is unusual because adult snakes feed on fish that are dropped by colonial nesting birds, and food resources are temporally limited relative to that of mainland populations. We found no differences in SMR between island and mainland snakes at any of four experimental temperatures (15°–30°C), suggesting that any adjustments to energy limitations involve other aspects of physiology or behavior. As with other viperid species, the SMR of cottonmouths is about one‐half of that expected from interspecific allometric regressions previously reported for snakes generally. Allometric mass exponents of SMR averaged 0.76 and were not affected by temperature. We found that V̇o2 increased with temperature (Q10 = 2.4–2.8) and was elevated 29% during scotophase compared with photophase. Neonates exhibited elevated V̇o2 compared with older juveniles of similar size, apparently due to assimilation of yolk that is present in the neonatal gut. In adult snakes, specific dynamic action (SDA) following feeding resulted in four‐ to eightfold increases in V̇o2, with magnitude and duration related positively to relative meal size. The total energy devoted to SDA increased with meal size and averaged 32.8% ± 4.4% of total ingested energy. We estimate that a nonreproductive 500‐g adult cottonmouth at Seahorse Key uses 3,656 kJ of assimilated energy annually for maintenance and activity, which requires ingestion of approximately 1 kg of fish.

Tracking the oxidative kinetics of carbohydrates, amino acids and fatty acids in the house sparrow using exhaled 13CO2

SUMMARY Clinicians commonly measure the 13CO2 in exhaled breath samples following administration of a metabolic tracer (breath testing) to diagnose certain infections and metabolic disorders. We believe that breath testing can become a powerful tool to investigate novel questions about the influence of ecological and physiological factors on the oxidative fates of exogenous nutrients. Here we examined several predictions regarding the oxidative kinetics of specific carbohydrates, amino acids and fatty acids in a dietary generalist, the house sparrow (Passer domesticus). After administering postprandial birds with 20 mg of one of seven 13C-labeled tracers, we measured rates of 13CO2 production every 15 min over 2 h. We found that sparrows oxidized exogenous amino acids far more rapidly than carbohydrates or fatty acids, and that different tracers belonging to the same class of physiological fuels had unique oxidative kinetics. Glycine had a mean maximum rate of oxidation (2021 nmol min−1) that was significantly higher than that of leucine (351 nmol min−1), supporting our prediction that nonessential amino acids are oxidized more rapidly than essential amino acids. Exogenous glucose and fructose were oxidized to a similar extent (5.9% of dose), but the time required to reach maximum rates of oxidation was longer for fructose. The maximum rates of oxidation were significantly higher when exogenous glucose was administered as an aqueous solution (122 nmol min−1), rather than as an oil suspension (93 nmol min−1), supporting our prediction that exogenous lipids negatively influence rates of exogenous glucose oxidation. Dietary fatty acids had the lowest maximum rates of oxidation (2-6 nmol min−1), and differed significantly in the extent to which each was oxidized, with 0.73%, 0.63% and 0.21% of palmitic, oleic and stearic acid tracers oxidized, respectively.

Effect of dietary fatty acid composition on fatty acid profiles of polar and neutral lipid tissue fractions in zebra finches, Taeniopygia guttata

The growing awareness that the fatty acid (FA) composition of the diets of birds, and ultimately their tissues, influence physiological performance variables, such as aerobic capacity, thermosensitivity, digestive efficiency, etc., underscores the need to understand how differences in dietary fatty acid composition actually translate into differences in the fatty acid composition of specific tissues. We quantified the fatty acid profiles of polar and neutral lipid fractions of several tissues in zebra finches (Taeniopygia guttata) and compared these profiles among birds fed either a control diet of only hulled millet, or one of two experimental diets of hulled millet supplemented with either 8% (by mass) sunflower seed oil (omega6-enriched diet) or linseed oil (omega3-enriched diet). We found that different lipid fractions vary widely in their diversity and complexity of FA composition, with neutral lipids being much less structurally diverse than those of polar lipids, for example, and that the fatty acid compositions of different organs exhibited different propensities to be altered by the diet, with brain and cardiac tissues having lower levels of flexibility than skeletal muscle and liver. We also present evidence suggesting that adipose tissue may be used to sequester essential FAs when they occur in the diet at levels that exceed immediate requirements. We conclude that the fatty acid composition of adipose tissue may not be a particularly useful indicator of the dietary FA composition of birds, and suggest that future studies investigating the relationships between the FA profiles of bird tissues and bird diets and/or physiological performance variables examine multiple tissues and distinguish between neutral and polar lipid fractions.

Fatty acid analyses may provide insight into the progression of starvation among squamate reptiles

Fasting-induced changes in fatty acid composition have been reported to occur within the body lipids of several types of animals; however, little is known about the changes in fatty acid profiles exhibited by reptiles subjected to prolonged fasting. This study characterizes the fatty acid profiles of six reptile species subjected to sublethal periods of fasting lasting 0, 56, 112, and 168 days. Analyses of fatty acid methyl esters (FAMEs) conducted on the total body lipids of rattlesnakes (Crotalus atrox), ratsnakes (Elaphe obsoleta), pythons (Python regius), boas (Boa constrictor), true vipers (Bitis gabonica), and monitor lizards (Varanus exanthematicus) revealed that all of the species exhibited similar characteristic changes in their fatty acid profiles during starvation stress. According to ANOVAs, the four most effective indicators of the onset of starvation were significant increases in the [1] fatty acid unsaturation index as well as ratios of [2] linoleic to palmitoleic acid, [3] oleic to palmitic, and [4] arachidonic to total fatty acid concentrations. The results of this study suggest that FAME analyses might be useful for identifying nutritional stress and/or starvation among squamate reptiles; however, forthcoming studies will be required to validate the generality of these responses. I also review the potential limitations of this approach, and suggest experiments that will be important for future applications of FAME analyses. Ultimately, it is hoped that FAME analyses can be used in conjunction with current practices as an additional tool to characterize the prevalence of starvation experienced by free-living reptiles.

Dietary fatty acid composition influences tissue lipid profiles and regulation of body temperature in Japanese quail

Many avian species reduce their body temperature (Tb) to conserve energy during periods of inactivity, and we recently characterized how ambient temperature (Ta) and nutritional stress interact with one another to influence physiologically controlled hypothermic responses in Japanese quail (Coturnix japonica). In the present study, we examined how the fatty acid (FA) composition of the diet influences the FA composition of phospholipids in major organs and how these affect controlled hypothermic responses and metabolic rates in fasted birds. For 5xa0weeks prior to fasting, quail were fed a standard diet and gavaged each morning with 0.7xa0ml of water (control), or a vegetable oil comprising saturated fatty acids (SFA; coconut oil), or unsaturated fatty acids (UFA; canola oil). Birds were then fasted for 4xa0days at a Ta of 15°C. We found that, while fasting, both photophase and scotophase Tb decreased significantly more in the SFA treatment group than in the control group; apparently the former down-regulated their Tb set point. This deeper hypothermic response was correlated with changes in the phospholipid composition of the skeletal muscle and liver, which contained significantly more oleic acid (18:1) and less arachidonic acid (20:4), respectively. Our data imply that these two FAs may be associated with thermoregulation.

Endogenous and Environmental Factors Influence the Dietary Fractionation of 13C and 15N in Hissing Cockroaches Gromphadorhina portentosa

Since DeNiro and Epstein’s discovery that the 13C and 15N isotopic signatures of animals approximate those of their respective diets, the measurement of stable isotope signatures has become an important tool for ecologists studying the diets of wild animals. This study used Madagascar hissing cockroaches (Gromphadorhina portentosa) to examine several preexisting hypotheses about the relationship between the isotopic composition of an animal and its diet. Contrary to my predictions, the results revealed that the tissues of adult cockroaches raised for two generations on a diet of known isotopic composition did not demonstrate enrichment of heavy stable isotopes. Moreover, the 15N signatures of cockroaches were neither influenced by periods of rapid growth (i.e., 300‐fold increase in dry body mass over 120 d) nor by imposed periods of starvation lasting up to 80 d. The offspring born to mothers raised on known diets were enriched in 15N. Diet‐switching experiments showed that turnover times of 13C were highly correlated with age and ranged from 9 to 10 d to 60 to 75 d in subadults and adults, respectively. Adults subjected to diet switches differed from the subadults in that the adults achieved equilibrated isotopic signatures that were shifted approximately 1.0‰ toward their respective original diets. Lipid fractions of adult cockroaches averaged 2.9‰ more depleted in 13C than in lipid‐free fractions, but no changes in 13C were observed in aging adults. Exposure to reduced ambient temperature from 33°C to 23°C over 120 d did not influence isotopic signatures of tissues. Overall, the results of this study reveal that different endogenous and exogenous factors can influence the isotopic signatures of cockroaches. These findings reinforce the need to conduct controlled studies to further examine environmental factors that influence the relationships between the isotopic signatures of animals and their diets.