Energy Storage and Expenditure

Anders Brodin and Colin W. Clark

7.1 Prologue

The snow creaks under our winter boots as we walk along the snow scooter track to our study site. The cold is overwhelming, and though we have been walking for an hour, we do not feel warm. The air is perfectly still, and the heavy snow on the branches of the surrounding conifers absorbs all sounds. When we arrive at the bait station, we spill some seeds onto the feeding tray and retire to the nearby trees. The seeds soon attract the attention of some willow tits. It is astonishing that these 10 g animals with their high-speed metabolism can survive in an environment where the temperature can remain below freezing for months. We know they need to eat three or four food items per minute throughout the short winter day to survive the long night. Surprisingly, the willow tits do not consume the seeds. Instead, they begin ferrying seeds from the tray to hiding places nearby. They conceal them carefully under flakes of bark, in broken branches, and in tufts of lichen. Evidently, willow tits can exploit the temporary abundance ofseeds most effectively by hoarding them, deferring their consumption until later. sophisticated energy management makes their survival in these extreme conditions possible. Their daily regimen combines use and maintenance of external (thousands of individually stored items) and internal (several lllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllll

222 Anders Brodin and Colin W. Clark grams of fat) energy supplies, augmented when necessary with tactics such as hypothermia.

7.2 Introduction

Organisms need energy to sustain their growth and metabolism. Most animals do not forage continuously and must store energy for periods when foraging is not possible. They also need to perform other activities that may not be compatible with foraging. Periods when energy expenditure exceeds energy intake may be short; for example, between two meals or overnight. They may also be long, lasting through the winter or throughout extended periods of drought. Energy can be stored in the body as fat, carbohydrates, or sometimes as proteins, or in the environment as hoarded supplies.

Many forms of energy storage are well known. Bears become very fat in autumn before they go into hibernation. Honeybees store large supplies of honey in the hive to be used as food during the winter. Many avian and mammalian species hoard thousands ofseeds and nuts in autumn and depend on these foods during the winter. Energy storage is also common in organisms such as plants and fungi. Many of our most common root vegetables, such as potatoes, rutabagas, and carrots, are good examples ofplants that store energy for future growth and reproduction.

Animals must actively regulate their energy expenditure. During hibernation, most animals reduce expenditure by lowering their body temperature and thereby their metabolism. Many humans try to decrease their body fat energy stores and get slimmer; for example, by reducing food intake. Others instead try to increase their energy stores. Before a race, cross-country and marathon runners may actively deplete the glycogen reserves in the liver and muscles. The evening before the race, they gorge on carbohydrates, attempting to enlarge those reserves and so increase their endurance (e.g., Astrand and Rodahl 1970). For animals that live in seasonally fluctuating environments, finely tuned management of the energy supply may be crucial for survival and reproduction. Indeed, without such adaptations, these organisms could not inhabit these environments.

We begin this chapter by presenting examples of how animals store and regulate energy. Next, we adopt an economic perspective that focuses on the costs and benefits of energy storage. This leads to a brief overview ofhowbe-havioral ecologists have modeled energy storage. We devote the second halfof the chapter to dynamic state variable modeling (Houston and McNamara 1999; Clark and Mangel 2000). From the simplest possible model, we proceed through models of increasing complexity to illustrate the key factors

Energy Storage and Expenditure 223

controlling energy storage. The text considers the problems of small passerine birds in a cold winter climate as a convenient model for problems of energy storage and regulation. We focus on evolutionary aspects of energy regulation. Box 7.1 introduces neural and endocrine mechanisms of energy regulation.

BOX 7.1 Neuroendocrine Mechanisms of Energy Regulation in

Mammals

Stephen C. Woods and Thomas W. Castonguay

Myriad approaches have been applied to the study of how animals meet their energy requirements. A century ago, the predominant view was that events such as gastric distension and contractions determine food intake, with signals from the stomach relayed to the brain over sensory circuits such as the vagus nerve. One of the most influential theories of energy balance, the "glucostatic hypothesis" posited over 50 years ago by Jean Mayer (1955), proposed that individuals eat so as to maintain a privileged level of immediately available and usable glucose. When this commodity decreased, either due to enhanced energy expenditure or to depleted energy stores, hunger occurred and eating was initiated; as a meal progressed, newly available glucose was able to reduce the hunger signal. While theories such as this were highly influential, subsequent research has found them to be simplistic and limited, and it is now recognized that an intricate and highly complex control system integrates signals related to metabolism, energy expenditure, body fat, and environmental factors to control food intake.

Most contemporary research has concentrated on the question "How much do we eat in a given meal, or in a given period of time?" Over 50 years ago, Adolph (1947) pointed out that when we eat energetically diluted foods, a greater bulk of food is consumed. Conversely, we eat smaller meals when food is energetically rich. This simple observation implies that we eat to obtain a predetermined number of calories of food energy. In fact, we humans adjust our caloric intake with remarkable precision, with our intake under free feeding conditions matching our energy expenditure with an error of less than 1% over long intervals (Woods et al. 2000).

The Control of Meals

Energy is derived from three macronutrients: proteins, fat, and carbohydrates. The carbohydrate glucose and various fatty acids provide energy to most tissues. The brain is unique, requiring a steady stream ofglucose from the blood in order to function. This reliance of the brain on glucose formed the basis of the glucostatic theory, and other theories over the years have focused on available fat or protein as being key to energy regulation. The premise underlying all of these hypotheses is that the level of some important commodity (glucose, fatty acids, total available energy to the brain or some other organ) waxes and wanes during the day. When the value gets low, indicating that some supply has become depleted, a signal is generated to eat; when the value is restored (repleted), a signal is generated to stop eating (Langhans 1996). While the logic of these "depletion-repletion" theories has considerable appeal, the bulk of evidence suggests that energy flux into the brain and other tissues is remarkably constant and that small fluctuations cannot account for the onset or offset of meals.

What, then, determines when a meal will begin, especially when an individual could, in theory, eat whenever it chooses? The best evidence, at least for omnivores such as humans and rats, suggests that eating occurs at times that are convenient given other constraints in the environment, or at times that have resulted in successful eating in the past. We eat at particular times because ofestablished patterns, or because someone has prepared food for us, or because we have a break in our busy schedules (Woods et al. 1998). If depletion of some critical supply of energy provided an impetus dictating that we put other behaviors on hold until the supply is replenished, daily activity patterns would be much different. Instead, animals enjoy the luxury of eating when it is convenient, and they regulate their energy needs via controls over how much is eaten once a meal is initiated.

Signals that Influence Intake

Armed with the tools of contemporary genetics, molecular biology, and neuroscience, scientists have discovered literally dozens of signals over the past 20 years that either stimulate or inhibit food intake (Schwartz et al. 2000; Woods et al. 1998). As depicted in figure 7.1.1, these signals fit into three broad categories. The first are signals generated during meals as the ingested food interacts with receptors in the mouth, the stomach, and the intestines. Most of these signals are relayed to the brain via peripheral nerves (especially the vagus nerve) and provide information as to the quality and quantity of what is being consumed. These are collectively called "satiety" signals because as their effect accumulates during a meal, they ultimately lead to the sensation of fullness or satiety in humans, and their administration reduces meal size in animals including humans. As an example, mechanoreceptors in the stomach respond to distension, and this information is integrated with chemical signals generated in response to the content of the meal. The best-known satiety signal is the intestinal peptide cholecystokinin (CCK). CCK is secreted in proportion to ingested fat and carbohydrates, and it elicits secretions from the pancreas and liver to facilitate digestion. CCK also stimulates receptors on vagus nerve fibers.

Agrp Satiety Center

Figure 7.1.1. Schematic diagram of the signals that control caloric homeostasis. Satiety signals arising in the periphery, such as gastric distension and CCK, are relayed to the nucleus of the solitary tract (NTS) in the hindbrain. Leptin and insulin, the two circulating adiposity signals, enterthe brain and interact with receptors in the arcuate nucleus (ARC) ofthe hypothalamus and other brain areas. These adiposity signals inhibit ARC neurons that synthesize NPY and AgRP (NPY cells in the diagram) and stimulate neurons that synthesize proopiomelanocortin (POMC), the precursor of a-MSH. These ARC neurons in turn project to other hypothalamic areas, including the paraventricular nuclei (PVN) and the lateral hypothalamic area (LHA). Catabolic signals from the PVN and anabolic signals from the LHA are thought to interactwith the satiety signals in the hindbrain to determine when meals will end. (From Schwartz et al. 2000.)

Figure 7.1.1. Schematic diagram of the signals that control caloric homeostasis. Satiety signals arising in the periphery, such as gastric distension and CCK, are relayed to the nucleus of the solitary tract (NTS) in the hindbrain. Leptin and insulin, the two circulating adiposity signals, enterthe brain and interact with receptors in the arcuate nucleus (ARC) ofthe hypothalamus and other brain areas. These adiposity signals inhibit ARC neurons that synthesize NPY and AgRP (NPY cells in the diagram) and stimulate neurons that synthesize proopiomelanocortin (POMC), the precursor of a-MSH. These ARC neurons in turn project to other hypothalamic areas, including the paraventricular nuclei (PVN) and the lateral hypothalamic area (LHA). Catabolic signals from the PVN and anabolic signals from the LHA are thought to interactwith the satiety signals in the hindbrain to determine when meals will end. (From Schwartz et al. 2000.)

If individuals are administered an antagonist to CCK receptors prior to eating, they eat a larger meal, implying that endogenous CCK normally helps to limit meal size. Analogously, if CCK is administered prior to a meal, less food is eaten (Smith and Gibbs 1998). CCK is but one example of peptides secreted by the stomach and intestine during meals that act as satiety signals (table 7.1.1).

(Box 7.1 continued)

Table 7.1.1 A partial list of signals known to influence food intake

Signals arising from peripheral

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