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Comparative Physiology of Fasting, Starvation, and Food Limitation
Abstract
All animals face the possibility of food limitation and ultimately starvation-induced mortality. This book summarizes state of the art of starvation biology from the ecological causes of food limitation to the physiological and evolutionary consequences of prolonged fasting. It is written for an audience with an understanding of general principles in animal physiology, yet offers a level of analysis and interpretation that will engage seasoned scientists. Each chapter is written by active researchers in the field of comparative physiology and draws on the primary literature of starvation both in nature and the laboratory. The chapters are organized among broad taxonomic categories, such as protists, arthropods, fishes, reptiles, birds, and flying, aquatic, and terrestrial mammals including humans; particularly well-studied animal models, e.g. endotherms are further organized by experimental approaches, such as analyses of blood metabolites, stable isotopes, thermobiology, and modeling of body composition. © 2012 Springer-Verlag Berlin Heidelberg. All rights are reserved.
Chapters (24)
Thomas Malthus (An Essay on The Principle of Population, 1798) famously summarized the grim hysteresis
between food limitation and the growth of human populations two decades before the word ‘Biology’ was
ever used in the English language (Marston Bates’ The Forest and the Sea: a Look at the Economy of Nature
and the Nature of Man , 1960). Over the subsequent two centuries biologists have documented the prevalence
of food limitation in all types of animals confirming that humans are not particularly unique in this regard.
Food limitation and its most dramatic outcome—death from starvation—are not new phenomena and date
back to the dawn of heterotrophy. In fact a growing body of evidence suggests that deaths from starvation
contributed to some of the greatest mass extinctions in Earth’s history. Despite both the antiquity and ubiquity
of food limitation certain lineages of animals were apparently able to persist. Comparative physiologists are
now charged with exploring the various adaptations that enable different types of animals to survive and often
flourish in the face of food limitation.
Fasting and starvation (prolonged fasting), are the most severe forms of malnutrition, and are experienced by aquatic and terrestrial species due to physiological, nutritional, or behavioral constraints. Migration, metamorphosis, reproduction, and molting are among the main endogenous factors, while food paucity, unpredictable feeding times, remote feeding grounds, and environmental and climatic changes are other external but similarly decisive cues. When the critical starving period is over, it can necessitate gradual refeeding, induce nutritional shifts, and also induce permanent damage. It has, therefore, always been a goal in physiology to understand the different adjustments during food deprivation and refeeding phases. In this field, most of the studies focusing on the physiological consequences of the imbalance between energy intake and energy expenditure have considered time to be the main function. However, since the late 1970s/early 1980s and the "rediscovery" of earlier studies, some researchers have considered starvation to be a continuous series of different metabolic phases composed of a short initial period of adaptation followed by a second phase characterized by fat oxidation. At this point, body lipid stores are not fully exhausted and a third nonpathological and reversible phase follows during which energy requirements are mostly derived from increased protein utilization. If prolonged, this phase can lead to a critical lethal endpoint, even if food becomes available. More recent studies have investigated the alarm signal that triggers behavioral changes such as nest abandonment and refeeding, and have also examined complex hormonal and metabolic regulations in response to food deprivation, such as the marked reduction of apolipoprotein A-IV levels observed in rodents during long-term fasting. The new challenges in this field concern the severely disrupted populations faced with increasing food restrictions due to anthropization.
Planktonic rotifers live in a world where food abundance can change rapidly and where food limitation is common and sometimes extreme. The goal of this review is to synthesize the ecological importance of food limitation in nature with the physiological responses of rotifers to starvation in the laboratory. Different rotifer species have very different responses to starvation. Some species respond to food deprivation by decreasing their metabolic rate and curtailing reproduction, while other species maintain a constant metabolic rate and continue to produce eggs, essentially reproducing themselves to death. This tradeoff between survival and reproduction explains much of the several-fold range in starvation times of different rotifer species. Future research is needed on the chemical composition of energy reserves in rotifers, the patterns of allocation of those reserves during starvation, and the frequency of starvation episodes in nature.
Fruit flies of the genus Drosophila have become an important model for energy storage and metabolism at multiple levels of organization. Drosophila species differ substantially in their abilities to survive without food, and many species exhibit latitudinal clines in energy storage and starvation resistance. Variation in starvation resistance can also be generated using experimental evolution, by subjecting populations to starvation selection. Physiological analyses of starvation-selected flies reveal that the entire life history of the animal is affected, particularly larval traits associated with growth and energy storage. As adults, these animals contain large lipid stores, but at the cost of reduced fecundity. The genetic toolkit available for Drosophila melanogaster has also allowed researchers to identify the molecular basis for how energy is stored and distributed to tissues that need it. Insulin signaling and other pathways can be manipulated in tissue- and temporal-specific ways that are revealing fundamental energy regulatory mechanisms common to all animals.
Spiders are a diverse group of invertebrates that successfully inhabit most terrestrial ecosystems. Part of their success can be ascribed to a remarkable feeding ecology that allows spiders to tolerate prolonged periods of starvation and provide the capacity to feed on very large prey. In this chapter, we review the existing knowledge on the physiological transitions in spiders during prolonged fasting and during consumption of (large) meals. We focus on the metabolic transitions between feast and famine as well as the use and uptake of macronutrients and water. Spiders reduce energy consumption during fasting and food deprivation is primarily associated with utilization of lipid stores. Also, despite the continuous catabolism of energy stores spiders defend body mass through a relative increase in body water. Feeding causes huge stimulation of energy consumption, where metabolic rate can increase more than 20-fold. The elevated metabolism persists for hours to days during the postprandial period and digestion is likely to constitute the largest sustained increase in metabolism of spiders. Because spiders use extraoral digestion, it is easy to investigate the energy balance of prey and predator during feeding. We argue, therefore, that spiders represent a promising animal model to study energy flux during feeding and fasting and hope this review will inspire further studies on the feeding physiology and ecology of this interesting animal group.
Most of the theory about starvation physiology in fish is based on observations of birds and mammals. Such observations have given rise to the idea that starving animals undergo three distinct physiological and/or morphological phases. These phases are typically defined by the type of physiological fuel (e.g. carbohydrates, lipids, or proteins) that is being utilized. Transitions from one phase to another may be indirectly identified by changes in hormone levels, enzyme activities, blood metabolites, or body mass. Similar to birds and mammals, we notice three distinctive transitions in the sequential compositional changes during long-term starvation of fish. The first phase is a short transient one where both protein tissues and fat reserves are mobilized, and where the concentration of several hormones (such as ghrelin and growth hormone levels) deviates significantly from the normal steady-state levels. The second phase appears to be a (usually long) steady state, with mobilization of fat as the main source of energy. During this phase the change in concentration of endocrine factors is minimal and protein breakdown is nearly constant. When the primary lipid source which was utilized as energy during the second phase reaches a critical value, a transition to the third stage occurs, in which proteins are being mobilized as the primary energy source. It appears that various fish species use different lipid sources (e.g. liver, viscera, muscle) and exhibit transition to Phase III at different critical values. Hormonal levels also change significantly at this final stage and they may facilitate the transition to alternative energy source (e.g. muscle protein). We also notice changes in composition and structure of the gut system of fish during these stages. A loss of vacuolization of the mucosa cells and the transformation to finely granular cytoplasm is already noticed after 2 days and is prominent after 7 days of starvation (Phases I and II, respectively). Changes in the mucosa folds can be observed after a short fasting period, at Phase II. Generally, the cells kept their regular cylindrical form and the number of goblet cells increased during the second stage of starvation. To conclude, data on starvation in fish suggest three distinctive phases during prolonged starvation periods, with transitions that are triggered by hormonal changes and are strongly effected by temperature.
Subterranean habitats are characterized by constant abiotic factors usually, including darkness, humidity, and temperature; yet these habitats also exhibit high temporal and spatial patchiness of food availability. Therefore, hypogean organisms often cope with periods of starvation that can last a few weeks to a few months. Subterranean species generally exhibit specific adaptations to long-term food deprivation and show a higher resistance to starvation than their epigean counterparts. The effects of long-term fasting and subsequent refeeding on behavior, locomotory and ventilatory activities, oxygen consumption, digestive physiology, and energy stores were investigated in subterranean aquatic crustaceans, fishes, and amphibians and then compared with responses observed among closely related or morphologically similar surface-dwelling species. When possible epigean and hypogean populations of the same species were compared. The remarkable resistance to long-term fasting showed by subterranean organisms may be partly explained by (1) lower metabolic demands and larger body stores in their nourished state, (2) the ability to undergo starvation-induced hypometabolism, and (3) a prolonged state of glycogen- and protein-sparing, permitted by extensive lipid catabolism. In addition, these groundwater species display high recovery abilities during refeeding, showing an optimal utilization of available food and a rapid restoration of their body reserves. Such responses are adaptive for life in harsh and unpredictable subterranean environments. The first part of this review focuses on the food status of subterranean ecosystems (especially caves and groundwaters'). The second part examines the sensitivity and responses of hypogean organisms to prolonged starvation. © 2012 Springer-Verlag Berlin Heidelberg. All rights are reserved.
Many types of snakes are capable of surviving over a year of complete starvation. The physiological effects of food limitation on snakes can be appreciated both by controlled studies of individuals and wild populations of snakes. Here we summarize morphological, physiological, and biochemical responses to food limitation among several distantly related snake species. Controlled studies revealed that the three traditional phases of fasting (i.e., stress, transition, adaptation), observed among endotherms, may not be clearly differentiated among fasting snakes. Nevertheless, starving snakes exhibited various potentially adaptive strategies for tolerating food limitation including the ability to: (1) reduce resting energy expenditure by entering a hypometabolic state, (2) regulate levels of circulating metabolites, (3) remodel tissues and increase body length, and (4) prioritize mass loss among different organs. Not surprisingly, the magnitude to which different species relied upon these different strategies varied, and was in part correlated with their ecological background and phylogenetic history. Starvation is a part of the natural history of many wild snake populations. Snakes inhabiting islands often experience boom and bust cycles where food is only available seasonally, usually corresponding to unpredictable allochthonous resources from birds that use islands for migratory stopovers and rookeries. Insular snakes have apparently adjusted to limited food supplies by morphological and behavioral modifications and shifting reproductive windows to minimize risk of starvation to mothers and offspring. The overall success of these strategies is evidenced in the comparatively dense population of snakes on many islands. Food available to snakes inhabiting forested areas can be influenced by land management practices (e.g., logging and fire supression) which indirectly affect the health of snake populations. Long-term mark-recapture and radiotelemetry studies reveal dramatic interannual shifts in mean body condition and extended periods of starvation driven by variation in mast crop in a degraded upland oak ecosystem. © 2012 Springer-Verlag Berlin Heidelberg. All rights are reserved.
Turtles, squamates, and crocodiles show remarkable morphological and physiological plasticity of their gastrointestinal tract in response to feeding. They also show a remarkably complicated and diverse morphology of their cardiovascular circuitry and cardiovascular functioning. In particular, many species have the option to bypass the pulmonary (or the systemic) circulation by redirecting blood into the systemic (or pulmonary) circulation, respectively. In this chapter we review the evidence that supports a functional integration of the gastrointestinal system with the cardiovascular system. In particular the morphology of the cardiovascular circuits suggests that both systems are tightly integrated. The main hypotheses about a functional integration are: (1) increased blood flow to the gastrointestinal system may provision more blood for transport, and also possibly drives inflation of the gastrointestinal tract after feeding. (2) Central redirection of blood may play a role for digestion by balancing the blood pH during the alkaline tide. (3) The anatomy of the vascular circuits suggests that CO2-rich blood is directed to the gastrointestinal tract to facilitate gastric acid production. We critically review the evidence and support for each of these ideas and outline avenues for future research that may ultimately help to clarify many of the contrasting ideas discussed in the literature. We conclude that the timing of shunting during digestion has not been fully explored; many important quantitative data (e.g., ventricle and blood volume, shunting volume) are completely missing; experimental studies are dominated by highly invasive studies with unclear effects on normal physiology; capillary filtration rate and the role of the lymphatic system have been neglected; and finally, volume compensation and compensatory shunts have largely been neglected. © 2012 Springer-Verlag Berlin Heidelberg. All rights are reserved.
Birds have body temperatures that are typically higher than those of mammals, and thus spend a large proportion of their total energy budget maintaining these temperatures-particularly in cold environments. Birds also have high surface to volume ratios and comparatively small energy reserves causing additional energetic challenges during periods of food limitation or complete starvation. During starvation, energy can be saved if the need for active thermogenesis can be reduced. Such a hypometabolic state can be achieved by reducing body temperature in a regulated manner or by increasing thermal insulation, or by employing both of these mechanisms. Adaptive changes in heat loss (thermal conductance) is well known among birds, but a growing number of studies are documenting how birds are able to conserve limited energy by reducing body temperature in a regulated manner. Rest-phase hypothermia and shallow torpor involve decreases in body temperature ranging from 1 to 10°C, with the birds retaining responsiveness to the environment, whereas deep torpor is characterized by a larger decrease, with body temperatures often approaching ambient temperature and resulting in true torpidity. Starvation is well known to induce deep torpor in some avian groups, notably hummingbirds and swifts; however, recent studies show that basically all avian groups can save energy during starvation by entering shallow torpor during the rest-phase of their daily cycle. So far, such responses have been found in at least 29 avian families. This chapter reviews our current understanding of how birds alter their thermoregulatory patterns in the face of starvation and underscores the need to: (1) investigate the neurohumoral responses underlying hypothermia and (2) better quantify the energy savings ensuing from small decreases in body temperature. © 2012 Springer-Verlag Berlin Heidelberg. All rights are reserved.
Birds undergo among the most extraordinary fasting events which may last up to several months as in breeding or moulting penguins during the subantarctic winter or more than 100 h during the migratory flight of bar-tailed godwits (Limosa lapponica) from Alaska to New Zealand across the Pacific ocean. In this review we demonstrate that it is the extraordinary ability of birds to extensively store and use lipids as the main energy source which allows them to fast for long periods during breeding, moulting, and migratory flight despite their high metabolic rates. Long-term fasting birds derive the largest part of the required energy (up to about 95%) from fat and only a minimum amount from protein. In contrast to mammalian running, birds maintain such a high proportion of energy derived from fat also during endurance flight. This is achieved by physiological adaptations during preparation, as well as for the catabolism of fatty acids during flight, such as extensive lipid storage and a specific upgrading of the transport system of fatty acids to the flight muscles and their oxidative capacity. Only little is known about the hormonal regulation of the metabolism during endurance flight, most of it related to the possible actions of the glucocorticoid hormone corticosterone. There are a number of trade-offs between competing physiological processes (e.g. between maximum fat catabolism and upgrading of the metabolic system or between oxygen transport and fuel transport) which likely are linked to the migration strategy of a bird.
Phenotypic flexibility in organ size is common in animals during fasting and is especially remarkable in birds during their migrations. This phenotypic flexibility is often explained in relation to changes in functional demands in response to environmental change. A new hypothesis suggests that the rate of tissue-specific degradation during fasting is related to the tissue-specific rate of protein turnover. This hypothesis predicts allometric scaling of tissue-specific protein turnover rate across species and so provides estimates of the rate of tissue degradation for a specific tissue in relation to other tissues within a given animal. We used carbon isotopic incorporation rate as a proxy for protein turnover and then predicted that organ size changes during fasting in migratory birds would occur in the following rank order from most to least reduced: small intestine, liver, kidney, gizzard, heart, flight, and leg muscles. Furthermore, the hypothesis that protein turnover determines the degree of tissue-specific mass loss during fasting predicts that rate of change is independent of activity levels of tissues. In the following contribution we discuss the proposed hypothesis in the context of other competing hypotheses and review its support given the existing data on tissue turnover and mass change.
Limitation of food availability caused by seasonal reduction in vegetation or other food resources is a commonly encountered environmental threat for seasonal small mammals in the wild. In response to this adversity, small mammals inhabiting temperate regions and higher latitudes exhibit seasonal fluctuations in physiology, behavior, and morphology, which may ensure survival in these challenging environments. Small mammals living in Qinghai–Tibet Plateau (average elevation above 4,500 m), routinely face harsh conditions that include extremely low temperatures (occasionally reaching-37°C) and severe altitudinal hypoxia. Surviving these conditions would be a challenge to most mammals, especially nonhibernating species that do not store food for winter. Small mammals living in the Inner Mongolian grassland must also cope with reduced food availability amidst increased energy requirements. Its climate is characterized by warm summers (mean temperatures of 17.8°C) but cold winters (mean temperature of-18°C) (Wang et al. 2003). 13.2 Seasonal Changes in Body Mass and Thermogenesis Brandt's voles (Lasiopodomys brandtii) and Mongolian gerbils (Meriones unguiculatus) are sympatric rodents and primarily distributed in the Inner Mongolian grasslands of China. Brandt's voles are strictly herbivorous and feed mainly on grass leaves,
During episodes of food deprivation, animals enhance survival by minimising energy costs incurred by the metabolically demanding maintenance and activity of their digestive system. The response occurs at physiological, biochemical and molecular levels and mainly concerns the intestinal wall. After a feeding episode, this response leads to a rapid decrease in gut length and mass, as well as enzyme activities, protein synthesis and the expression of many proteolytic-related genes. Intestinal atrophy affects the mucosa, and induces a general decrease in its surface area through the diminishing of the mucosal area (shortening of the intestinal folds), changes in the microvilli surface area and by reducing both the size (hypotrophy) and number of cells along the intestinal barrier (hypoplasia). In most of the species studied, these morphological responses are time dependent and do not alter nutrient transport capacity, at least at the beginning of the fasting period. Fasting is usually anticipated in hibernating mammals, migratory vertebrates and infrequent feeders such as pythons. When preparing itself for fasting, the digestive system mainly uses tools such as hyperphagia, intracellular recycling and the production of new cells that are downregulated at the end of the postprandial period. As food deprivation continues starving animals may respond differently. This has been illustrated in rats that had reached a proteolytic phase during which energy requirements were mostly derived from increased protein utilisation. In these animals, cell proliferation and cell migration were seen to increase while apoptosis at the tip of the intestinal villi ceased. This has been considered as an optimising process that may also exist in other species.
Animals often rely heavily on stored lipids as a fuel source during extended periods of fasting/starvation; this results in notable decreases in lipid content during the fast. Additionally, the composition of stored lipids often changes during periods of fasting, although the reasons for these compositional changes have not been fully explored. We examine the changes in fatty acid composition that occur during starvation through the lens of two important processes: (1) changes in the triacylglycerol to phospholipid ratio and (2) selective mobilization and oxidation of particular fatty acids. As triacylglycerols are oxidized, the ratio of triacylglycerols to phospholipids should decrease, resulting in higher overall proportions of polyunsaturated fatty acids, which are more abundant in phospholipids. Selective mobilization of fatty acids results in the preferential oxidation of short-chained and highly unsaturated fatty acids, the proportions of which should therefore decrease during starvation. In general, decreases in the triacylglycerol to phospholipid ratio appear to explain observed changes in fatty acid composition of whole animals and some tissues. On the other hand, selective mobilization of fatty acids can explain many of the compositional changes observed in adipose tissue. Together, these two processes should be considered when seeking to identify exceptional species or examples of unique lipid regulation. One notable exception is hibernating mammals, which do not exhibit standard selective mobilization patterns, possibly in order to conserve certain essential polyunsaturated fatty acids during their hibernation fast.
- Miriam Ben Hamo
- Agustí Muñoz-Garcia
- Berry Pinshow
The evolution of powered flight afforded bats the opportunity to fill ecological niches void of non-volant mammals, a circumstance that might explain their remarkable diversity in terms of number of species, diet, and habitat types that they occupy. However, besides its clear ecological advantages, the evolution of powered flight brought about high energetic costs for bats. To compensate for these costs, bats have evolved a variety of energy-saving thermoregulatory traits. The mechanisms underlying these attributes make bats a fascinating model for exploring physiological responses to fasting. In this chapter, we document the diversity of physiological traits behind the ability of bats to undergo long periods of fasting, and we associate it with their respective diets. At one extreme are hematophagous species that are unable to fast longer than 72 h due to its apparent inability to store and mobilize endogenous fuels; at the other are insectivorous vespertilionid and rhinolophid species that can fast for months at a stretch. Despite their ecological importance, far less is known about adaptations to fasting in bats than non-volant mammals or birds. Many questions remain open regarding the physiology, endocrinology, biochemistry, and energetics of fasting in bats and we hope that this review will encourage further investigation on this topic.
While maintaining the body temperature at only 5°C below normal, black bears in the winter undergo 5 months when they do not eat, drink, urinate, or defecate. They have a high hypothalamic set point regulating fall hyperphagia and a large fat reserve followed by complete anorexia with a 50% reduction in energy demands while in their den. Cardiac and skeletal muscle is preserved, perhaps at the expense of smooth muscle and labile protein reserves. Winter protein demands are reduced by (1) no arousal bouts, (2) delayed implantation by pregnant females, and (3) urea hydrolysis to avoid urinary nitrogen and water loss. Bears recycle almost 100% of their urea due to urea transporters (UTB) in the bladder and intestines which salvage urea for microbial hydrolysis in the intestine with hepatic reammination of ammonia nitrogen into new amino acids and muscle protein. Bears exhibit subtle EMG patterns and respiratory sinus arrhythmia throughout the denning period. As a result of protein conservation and muscle contraction patterns, bears during 150 days of inactivity and complete food deprivation show no cardiac left ventricular atrophy. In addition, skeletal muscle exhibits no or only marginal loss of: protein, fiber number, size, or conversion of slow oxidative (MHC1) to fast glycolytic (MHC2x) fiber composition with a concomitant retention of strength. Bears are truly adapted to long periods of food deprivation and immobility that can afford a model for the study of humans in space flight and hospital confinement.
White-tailed deer (Odocoileus virginianus) living in northern regions of the U.S. and southern Canada are subject to large seasonal variations in food supply. White-tails are browsing ruminants that consume leaves of forbs, shrubs, and low-hanging trees when available. When autumn frosts deprive them of that food supply, deer are commonly relegated to less nutritious twigs and evergreen fronds. Deep snows can restrict travel and foraging opportunities and increase energy demand, thus compounding winter’s nutritional challenges. Our studies of digestible energy (DE) and metabolizable energy (ME) requirements of white-tailed deer and the DE and ME supplied by typical winter browse show that maintenance energy requirements are rarely met, leading to increased winter mortality. Behaviors to minimize energy requirements include lying down on a sunny, wind-sheltered hillside, or seeking shelter on cloudy days or at night in protected locations such as cedar swamps. Here, deer curl up under overhanging branches to restrict radiant heat loss. Avoidance of death requires that sufficient accessible energy be stored in body fat depots during the previous summer and fall to sustain life until spring green-up. We have measured seasonal changes in food intake and lipogenic activity in subcutaneous and perirenal adipose tissue. These measures are markedly affected by photoperiod, presumably via the pineal gland and its response to day-length, and perhaps by other mechanisms. We also have reviewed and examined the effects of season, sex, and age on food intake and the corresponding morphological and physiological changes in white-tailed deer, along with other environmental factors that influence their welfare and that of other wild ruminants.
![Fig. 19.2 The contribution of protein to field metabolic rate (FMR) decreases with initial adiposity in various bird and mammal species. Figure reproduced, with permission, from Verrier et al. (2009); see original for references. Species abbreviations: Wg, William grous; Pt L , lean ptarmigan; Am, American marten; R L , lean rat; Rb, rabbit; Gp, gentoo penguin; H L , lean human; Pt F , fat ptarmigan; Kp A , adult king penguin; Afs, Antarctic fur seal pup; Ep, emperor penguin; Kp C , king penguin chick; Ne, Northern elephant seal pup [Ne1 (d); mass balance method; Ne2 and Ne3 (s), urinary urea turnover method]; Se, Southern elephant seal pup (mass balance method); Pb, polar bear; W, woodchuck; Gs, grey seal pup; R O , obese rat; H O , obese human; SFS, subantarctic fur seal pup](https://www.researchgate.net/profile/Daniel-Crocker-3/publication/281733426/figure/fig2/AS:390759179145237@1470175656897/The-contribution-of-protein-to-field-metabolic-rate-FMR-decreases-with-initial_Q320.jpg)
Most animal species experience periods of food deprivation and many periodically forgo foraging in favor of other activities such as migration and reproduction. Pinnipeds-seals, sea lions, fur seals, and walrus-forage on marine resources but remain tied to land for reproduction. This separates energy acquisition from energy allocation for maternal investment, competition for mates, and for tissue maintenance and repair during pelage synthesis. Thus, pinnipeds regularly undertake energetically costly activities simultaneous with extended fasting at multiple life stages. This life history characteristic should favor physiological mechanisms for efficient fasting metabolism while supporting the energetic and substrate requirements of energy-demanding activities (e.g. lactation). Studies on a variety of pinnipeds have revealed highly efficient protein sparing despite high rates of energy expenditure and nutrient mobilization for lactation. Carbohydrate oxidation is low and high rates of lipolysis support nutrient delivery. Despite prolonged fasting and high rates of β-oxidation there is little accumulation of ketoacids. In contrast to numerous investigations on nonfasting adapted species, studies on phocid seals have revealed high rates of glucose production during fasting that exceed the needs for glucose dependent tissues and suggest high rates of carbohydrate recycling. Investigations into the hormonal regulation of fuel use and intracellular signaling pathways indicate adjustments to the typical mammalian regulation of gluconeogenesis. Together, these findings suggest alterations in the metabolic strategies for fasting exist in the pinnipeds compared to domestic and wild terrestrial mammals. © 2012 Springer-Verlag Berlin Heidelberg. All rights are reserved.
Maintaining adequate energy and mass balance is necessary to the survival and reproduction of any organism. However, nearly all organisms experience periods of catabolism, when insufficient food is being consumed and endogenous stores must be metabolized to provide the difference. The ubiquity of this phenomenon, perhaps an intuitive understanding of the threat that starvation poses to an individual’s survival, and the fact that many organisms seem to "voluntarily" enter long periods of catabolism (fasting) has caused great interest among physiologists to discover and understand the mechanisms organisms have evolved to survive such periods. In wild animals, merely detecting the existence and duration of periods of fasting or starvation can be difficult and much effort has been devoted toward establishing stable isotope analysis (SIA) as a tool for detecting and understanding the duration of catabolic states in wild animals. However, the results of these studies have been mixed. Increasingly, SIA is also being used to investigate the mechanisms organisms use to cope with periods of catabolism: how nutrients are routed, which are recycled, which are used for energy, and how that differs between different organs and organ systems. This chapter reviews the past and current applications of SIA for understanding fasting and starvation in animals and identifies areas where SIA may yet be applied to increase our understanding of fasting and starvation.
In the late nineteenth century, nutritional scientists and physicians recognized the clinical symptoms of human starvation, which they regarded primarily as a protein deficiency. In the absence of large studies of advanced starvation, they could not, however, determine how long a normal person could live without food. British physicians and famine relief officers feared the illusive danger point at which a starving person could presumably suffer a deadly collapse. Scientists made dramatic advances in their understanding of human nutrition in the first half of the twentieth century. They learned that the most critical factors in starvation were deficiencies in amino acids, vitamins, and, above all, carbohydrates. Yet these advances were slow to influence the treatment of starvation by British physicians. Prison medical officers, in particular, continued to focus on protein in their diagnosis and forcible feeding of the growing number of hunger strikers in British, Irish, and Indian prisons. Long after nutritional scientists had abandoned the Victorian maxim that protein was the only true nutrient, prison medical officers continued to forcibly feed hunger strikers a liquid mixture of milk, eggs, beef, and brandy. © 2012 Springer-Verlag Berlin Heidelberg. All rights are reserved.
Complex metabolic adaptations occur during human starvation. Metabolic rate decreases, energy stores are mobilized, fuel utilization shifts from carbohydrate toward fat and ketone oxidation, and body fat and lean tissue mass are lost. A mechanistic computational model of human metabolism and body composition change has recently been developed to simulate the dynamic coordination of these physiological adaptations. This chapter describes the integrative physiology of human starvation using illustrative computer simulations along with real data from prolonged fasting experiments. © 2012 Springer-Verlag Berlin Heidelberg. All rights are reserved.
Dietary restriction regimens are commonly employed to facilitate weight loss in overweight and obese individuals. The dietary restriction regimen most frequently implemented is daily calorie restriction (CR), which involves decreasing energy intake by a certain percentage daily. Another dietary restriction regimen employed, although far less commonly, is alternate day fasting (ADF). ADF regimens include a "feed day" where food is consumed ad libitum, alternated with a "fast day," where food intake is fully or partially reduced. The present review examines the ability of ADF regimens to facilitate weight loss in human and animal models. I also discuss the ability of this fasting regimen to reduce the risk of certain chronic diseases, such as cardiovascular disease and type 2 diabetes. © 2012 Springer-Verlag Berlin Heidelberg. All rights are reserved.
All the chapters in this volume draw attention to the remarkable recent progress that has been made in
documenting how different animals respond to voluntary or involuntary starvation. Here, I outline how this
progress has led to a new horizon of research prospects and provide some examples of promising new areas
of investigation. We generally acknowledge that starvation has shaped the evolutionary history of animals,
but we know much less about how variation in starvation tolerance may have favored some lineages over
others and to what different extent modern animals are suited to tolerate natural environment-induced
anthropogenic changes in food resources. Moreover, it is clear that our progress in identifying the behavioral
and physiological adaptations that animals have evolved to tolerate prolonged starvation has not kept pace
with our understanding of the potential tradeoffs associated with such adaptations. We take it for granted that
food limitation is an important circumstance in regulating the populations of many wild animals, yet we need
more studies that quantitatively document this factor in the wild. Such studies will lend themselves to
opportunities to improve and expand the techniques we use to monitor nutritional stress among wild animals.
For most animals, lipids are the most important fuel source during prolonged fasting and starvation; however,
we have only begun to consider how starvation influences the composition of fatty acids in the body, and
how this fatty acid composition affects starvation tolerance. A growing number of recent studies have
documented starvation-induced hypometabolic responses in a variety of species. Unfortunately, to date, we
have little insight into the specific regulatory mechanisms that enable these adaptive responses. Many types
of animals host enormous populations of intestinal symbionts that rival the number of cells in their own bodies;
however, we know little about how starvation alters the communities of gut microflora, and more importantly
the repercussions that these microecological disturbances may have on the host organism. Overall, I believe
that the future of starvation research is promising as long as we recognize that significant progress requires
an integrative approach and the expertise of researchers in many subfields of biology.
... Starvation in zebrafish over 21 days lead to increased diversity and altered microbial composition that showed relative increases in Vibrio (phylum Proteobacteria/Pseudomonadota) [71]. In other aquaculture species, including Nile tilapia (Oreochromis niloticus) and Asian seabass (Lates calcarifer), the relative abundance of Proteobacteria also increased in prolonged fasting individuals compared to well-nourished individuals [36,72]. In human gut microbiota studies, members of Proteobacteria are believed to indicate dysbiosis. ...
... Results from human studies are similar to our findings of large increases in the relative abundance of Aeromonas in the GI tract communities of TR larvae. These changes may occur because during the fasting, the supply of nutrients to GI tract symbionts were significantly reduced, causing an "energy crisis" [36,75], where some microbial species may not be able to survive. Further, other studies show that starved fish show evidence of intracellular degradation and reduced endothelium that subsequently reduced the tissue mass of the host digestive system, and in turn could have affected the taxonomic composition of microbiota [36,72]. ...
... These changes may occur because during the fasting, the supply of nutrients to GI tract symbionts were significantly reduced, causing an "energy crisis" [36,75], where some microbial species may not be able to survive. Further, other studies show that starved fish show evidence of intracellular degradation and reduced endothelium that subsequently reduced the tissue mass of the host digestive system, and in turn could have affected the taxonomic composition of microbiota [36,72]. ...
Compromised nutritional conditions associated with dietary transitions and feeding cessation in the wild and during fish aquaculture operations are common and can impact growth and survival. These effects are especially prevalent during early ontogenetic stages. We quantified phenotypic and GI tract microbial community responses with an emphasis on protease-producing bacteria of lake sturgeon (Acipenser fulvescens) larvae, a species of aquacultural and conservational importance. To quantify responses associated with experimental food transition and feeding cessation, we performed a 36-day feeding experiment using two treatments: control and diet transition. However, larvae in the diet transition treatment failed to undergo transition and ceased feeding. Larvae in the diet transition treatment exhibited lower growth (total length and body weight) and survival than control larvae. Treatment had a greater effect than ontogenetic changes on taxonomic composition and diversity of the GI tract microbial community. Proteobacteria dominated the GI tract microbial community of the diet transition larvae whereas Firmicutes dominated the GI tracts of control larvae. Most of the 98 identified protease-producing isolates in both treatments were from genera Pseudomonas and Aeromonas: taxonomic groups that include known fish pathogens. Overall, failing to transition diets affected responses in growth and GI tract microbiome composition and diversity, with the later dysbiosis being an indicator of morbidity and mortality in larval lake sturgeon. Thus, microbiological interrogations can characterize responses to dietary regimes. The results can inform fish culturalists and microbiologists of the importance of dietary practices consistent with the establishment and maintenance of healthy GI tract microbiota and optimal growth during early ontogeny.
... Accordingly, humans have developed numerous behavioral and physiological adaptations that allow them to survive in a food-deprived/fasted state. Contemporary scientific investigation of human starvation began in the late nineteenth and early twentieth centuries [9,[11][12][13][14]. We focus our analysis on the coordinated metabolic responses of adults to short-term fasting (i.e., 0-72 h), as it is applicable to all IF regimens. ...
... Blood ketones concentration is similar to FFA (~1.5 mmol/L) after 72 h of fasting and the brain begins to use significant amounts of ketones as a fuel source, reducing the need for glucose production [14,15]. In addition, there is a further decrease in metabolic rate beyond the absence of TEF, which is partially underlined by decreased circulating leptin and thyroid hormones [11,15,25]. ...
This review summarizes the effects of different types of intermittent fasting (IF) on human cardiometabolic health, with a focus on energy metabolism. First, we discuss the coordinated metabolic adaptations (energy expenditure, hormonal changes and macronutrient oxidation) occurring during a 72 h fast. We then discuss studies investigating the effects of IF on cardiometabolic health, energy expenditure and substrate oxidation. Finally, we discuss how IF may be optimized by combining it with exercise. In general, IF regimens improve body composition, ectopic fat, and classic cardiometabolic risk factors, as compared to unrestricted eating, especially in metabolically unhealthy participants. However, it is still unclear whether IF provides additional cardiometabolic benefits as compared to continuous daily caloric restriction (CR). Most studies found no additional benefits, yet some preliminary data suggest that IF regimens may provide cardiometabolic benefits in the absence of weight loss. Finally, although IF and continuous daily CR appear to induce similar changes in energy expenditure, IF regimens may differentially affect substrate oxidation, increasing protein and fat oxidation. Future tightly controlled studies are needed to unravel the underlying mechanisms of IF and its role in cardiometabolic health and energy metabolism.
... Lipids in fish play a crucial role as a source of energy and for the provision of essential fatty acids, necessary for fish growth and development (Kim et al., 2012). However, fish prefer to consume energy from protein, more specifically from the amino acids (Walton and Cowey, 1982;Wu et al., 2020), while lipids are known to be stored in liver and muscle by fish and to spare the role of protein (Kim et al., 2012;Zhang et al., 2019) when protein are sourced inadequately or fish needs to adapt physiologically through energetic cost (McCue, 2013). Silica NP undoubtedly increased digestibility and absorption of nutrients including protein and lipids. ...
With the aim of investigating the effects of silica nanoparticle (NP) on nutrition and physiology of Nile tilapia, Oreochromis niloticus, an eight-week experiment was designed. Highly pure, activated silica NP at different levels (0, 100, 200, 300 mg/Kg diet) were incorporated into 30% proteinous diet. Healthy fish of 6.52 (±0.20) g were assigned randomly in triplicate tanks maintaining for each treatment in a recirculatory aquaculture system and fed with their respective diets from July 02 to August 26, 2019. Throughout the study period, effects of silica NP on length gain, survival, dry matter digestibility, blood cells count, hemoglobin level, condition factor and final product composition (moisture, ash and crude protein) except lipid content were found insignificant (p>0.05). Results showed that growth parameters (WG, PWG, SGR, DGC) and feed efficiency increased significantly with the increasing level of silica NP up to 200 mg/Kg and then decreased. This favor was gained because of the highest apparent protein digestibility with strong significance (p<0.001) took place while fish were fed with silica NP at 200 mg/Kg diet. However, fish at early stage showed better performance in all dietary groups than later. Blood glucose content and histology of kidney revealed that fish got stressed when silica NP at 300 mg/Kg diet was used and adapted energetically through excessive excretion via elongated glomerulus. Though no significant (p>0.05) effect on villi length was observed however, silica NP widened the villi of midgut (p<0.001) and increased goblet cells in the intestine significantly (p<0.05) in T2. Bioaccumulation study of silica interprets that incorporation of silica NP in fish feed might not be able to compromise human health safety upon consumption. Conclusively, incorporation of silica at 100 and 300 mg/Kg diet though exposed some improvement in growth and final product quality, 200 mg/Kg silica NP is obviously the best performer in regards of all indicators.
... But hungry and thirsty people are evidently more sensitive to food-related cues (Aarts et al., 2001;Parmentier et al., 2018;Radel & Clément-Guillotin, 2012;Skrynka & Vincent, 2019) and report mental preoccupation with food (Keys, 1950). Our results suggest that just as the body's reaction to hunger changes over time (McCue, 2012), so too might the mind's reaction to fasting. In the early hours of fasting, even though fasters are likely not hungry because they prepared for the fast, subtle probes around food seem to capture their attention, distracting them from related tasks. ...
During Ramadan, people of Muslim faith fast by not eating or drinking between sunrise and sunset. This is likely to have physiological and psychological consequences for fasters, and societal and economic impacts on the wider population. We investigate whether, during this voluntary and temporally limited fast, reminders of food can impair the fasters’ reaction time and accuracy on a non-food-related test of cognitive control. Using a repeated measures design in a sample of Ramadan fasters ( N = 190), we find that when food is made salient, fasters are slower and less accurate during Ramadan compared with after Ramadan. Control participants perform similarly across time. Furthermore, during Ramadan performances vary by how recently people had their last meal. Potential mechanisms are suggested, grounded in research on resource scarcity, commitment, and thought suppression, as well as the psychology of rituals and self-regulation, and implications for people who fast for religious or health reasons are discussed.
... Migration, however it is shaped and controlled (chapter 1), allows birds to capitalize 1519 seasonal availability of punctuated resources, for example following upcoming resources on 1520 migration as seen in Common cuckoos (Cuculus canorus) and Red-backed shrikes (Lanius before the winter season (Biebach, 1996). However, those fat reserves are not used for 1537 insulation like in other animals (Scholander, Walters, Hock, & Irving, 1950), because in birds 1538 bodyweight sharply limits flight performance (McCue, 2013). Instead, fat is used as a reserve 1539 to overcome short periods of harsh weather which limits energy intake due to the inaccessibility 1540 of food resources (Biebach, 1977b). ...
... Specific dynamic action is the amount of energy expenditure above the basal metabolic rate (RMR) due to the ingestion and digestion of food for use as energy or conversion to a storage form (Secor, 2009). One major metabolic variable is the temporary rise in metabolic rate following feeding status or swallowing food (Karasov & del Rio, 2007;McCue, 2012). This feeding status-associated rise in metabolic rate is a result of food breakdown and processing in the gut of the organism (Karasov & del Rio, 2007). ...
Temperature is a crucial driver of insect activity and physiological processes throughout their life-history, and heat stress may impact life stages (larvae, pupae and adult) in different ways. Using thermolimit respirometry, we assessed the critical thermal maxima (CT max -temperature at which an organism loses neuromuscular control), CO 2 emission rate (V́CO 2 ) and Q10 (a measure of V́CO 2 temperature sensitivity) of three different life stages of Helicoverpa punctigera (Wallengren) by increasing their temperature exposure from 25 °C to 55 °C at a rate of 0.25 °C min ⁻¹ . We found that the CT max of larvae (49.1 °C ± 0.3 °C) was higher than pupae (47.4 °C ± 0.2 °C) and adults (46.9 °C ± 0.2 °C). The mean mass-specific CO 2 emission rate (ml V́CO 2 h ⁻¹ ) of larvae (0.26 ± 0.03 ml V́CO 2 h ⁻¹ ) was also higher than adults (0.24 ± 0.04 ml V́CO 2 h ⁻¹ ) and pupae (0.06 ± 0.02 ml V́CO 2 h ⁻¹ ). The Q 10 : 25–35 °C for adults (2.01 ± 0.22) was significantly higher compared to larvae (1.40 ± 0.06) and Q 10 : 35–45 °C for adults (3.42 ± 0.24) was significantly higher compared to larvae (1.95 ± 0.08) and pupae (1.42 ± 0.98) respectively. We have established the upper thermal tolerance of H. punctigera , which will lead to a better understanding of the thermal physiology of this species both in its native range, and as a pest species in agricultural systems.
This narrative review aims to pinpoint mental and behavioral effects of starvation, which may be triggered by hypoleptinemia and as such may be amenable to treatment with leptin receptor agonists. The reduced leptin secretion results from the continuous loss of fat mass, thus initiating a graded triggering of diverse starvation related adaptive functions. In light of leptin receptors located in several peripheral tissues and many brain regions adaptations may extend beyond those of the hypothalamus-pituitary-end organ-axes. We focus on gastrointestinal tract and reward system as relevant examples of peripheral and central effects of leptin. Despite its association with extreme obesity, congenital leptin deficiency with its many parallels to a state of starvation allows the elucidation of mental symptoms amenable to treatment with exogenous leptin in both ob/ob mice and humans with this autosomal recessive disorder. For starvation induced behavioral changes with an intact leptin signaling we particularly focus on rodent models for which proof of concept has been provided for the causative role of hypoleptinemia. For humans, we highlight the major cognitive, emotional and behavioral findings of the Minnesota Starvation Experiment to contrast them with results obtained upon a lesser degree of caloric restriction. Evidence for hypoleptinemia induced mental changes also stems from findings obtained in lipodystrophies. In light of the recently reported beneficial cognitive, emotional and behavioral effects of metreleptin-administration in anorexia nervosa we discuss potential implications for the treatment of this eating disorder. We postulate that leptin has profound psychopharmacological effects in the state of starvation.
A clear understanding of past weaning practices can provide invaluable insights into social issues such as infant care, fertility rate, and demographic patterns in past societies. This study presents the first archeological research employing compound specific isotope analysis (CSIA) for the reconstruction of past weaning practices. Weaning practices of two Middle Neolithic communities in the Paris Basin region: Balloy (BLR) and Vignely (VPB), are evaluated by combining previously published bone collagen stable carbon, nitrogen, and sulfur (n = 66) isotope analysis with new compound specific carbon and nitrogen isotope compositions of bone collagen (n = 10). Our results demonstrate that the diets of individuals from BLR and VPB likely incorporated freshwater resources. The signals of freshwater resources consumption are even stronger among subadults, suggesting that freshwater resources were used as weaning food at these sites. The implications of our result are threefold. Currently many CSIA studies in archeology only involve either carbon or nitrogen. Our data shows that it is important to conduct CSIA on both carbon and nitrogen for a more integrated picture. Secondly, our data demonstrates that the use of a protein‐based weaning food—instead of a starch‐based weaning food (such as cereal gruel)—was likely more prevalent among the Middle Neolithic communities in the Paris Basin Region than previously thought. The finding thus prompts a rethinking of the role of protein‐based weaning food in other archeological contexts. Lastly, the common assumption that weaning foods and adult diets share similar isotopic compositions can be problematic, as the use of protein‐based, high trophic‐level weaning foods can skew the δ15N weaning curve and produce an erroneously late estimation for weaning ages.
A 56‐day feeding trial was conducted to investigate metabolic responses of hybrid grouper (Epinephelus fuscoguttatus × ♂ E. lanceolatus) induced by different feeding modes. The experimental groupers were divided into three feeding modes as follows: continuous feeding group (8 weeks, C group), prolonged starvation group (8 weeks, S group) and refeeding group (starving for 4 weeks + refeeding for 4 weeks, R group). The results show that prolonged starvation had negative effect on growth, yet refeeding caused compensatory growth (p < .05). Serum glucose, triglycerides, total cholesterol and glutamic oxalacetic transaminase activity decreased in S group; triglycerides and total cholesterol reduced in R group; insulin‐like growth factor‐1 and its gene expression both increased in S and R groups (p < .05). Both glycogen content and intestinal digestive enzymes activity decreased in S group (p < .05). Prolonged starvation caused decrease in hepatic enzymes activity of glycolysis and lipogenesis, while enhanced enzymes activity and genes expression of gluconeogenesis and lipolysis (p < .05). The glycolytic enzymes activity and genes expression improved in R group (p < .05), which may be a solution to compensatory growth. Thus, grouper performed more efficient and active glycolysis in the metabolism of hepatic glucose and lipid. Besides grouper obtained a certain ability to resist prolonged starvation.
Salamanders are unique among tetrapods in their ability to regenerate their limbs throughout life. Like other poikilothermic amphibians, salamanders also show a remarkable capacity to survive long periods of starvation. Whether the physiological reserves necessary for tissue regeneration are preserved or sacrificed in starved salamanders is unknown. In the current study, we maintained Iberian ribbed newts ( Pleurodeles waltl) under extreme physiological stress to assess the extent of regeneration and identify the molecular and cellular changes that may occur under such conditions. After 19 months of complete food deprivation, the animals exhibited extensive morphological and physiological adaptations but remained behaviorally active and vigilant. Autophagy was elevated in different tissues and the transformed gut microbiota indicated remodeling of the intestinal tract related to autophagy. Upon limb amputation in animals starved for 21 months, regeneration proceeded with progenitor cell proliferation and migration, leading to limb blastema formation. However, limb outgrowth and patterning were substantially attenuated. Blockage of autophagy inhibited cell proliferation and blastema formation in starved animals, but not in fed animals. Hence, tissue autophagy and the regenerative response were tightly coupled only when animals were under stress. Our results demonstrate that under adverse conditions, salamanders can exploit alternative strategies to secure blastema formation for limb regeneration.
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