Introduction

The ways in which animals obtain and handle food resources depend on the physiological processes that follow ingestion. Preconsumptive and post-consumptive processes make up an integrated, whole-organism operation (Bautista et al. 1998; Karasov and Diamond 1988; Karasov and Hume 1997; Levey and Martinez del Rio 2001; Penry and Jumars 1986; Whelan et al. 2000). However, while foraging ecologists have made tremendous progress in understanding the ecological factors influencing patch use and prey choice, and while studies of the physiology of digestion have increased our understanding of food processing, theoreticians have made few connections between these two fields. This is unfortunate, because each depends on the other.

Food acquisition and processing are not independent processes. We view foraging as a suite of ecological tools for selecting habitats and diets, which in turn direct foods to the gut that facilitate the gut's processing tools. Foraging and digestion constitute a coordinated and coadapted division of labor. Efforts to secure a resource, or to prepare it for consumption, facilitate efforts to process and assimilate it (Courtney and Sallabanks 1992; Levey 1987). The actions of any one component of the digestive system, right down to the electrophysiological coordination of the two-membrane domains of the absorptive cells ofthe intestine, the enterocytes (Reuss 2000), facilitate the operation of other components (Caton et al. 2000).

Following Rosenzweig (1981), we recognize a continuum from foraging specialists to foraging generalists. Coadaptation ofbehavioral, morphological, and physiological traits pertinent to food acquisition and processing shapes the level of a particular animal's specialization. A specialist may need a specialized gut, while a generalist may require a more generalist (jack-of-all-trades) gut (Bjorndal and Bolten 1993; Murphy and Linhart 1999; Sorenson et al. 2004). These scenarios may represent alternative evolutionary strategies of coadaptation offood acquisition and food processing.

Students offeeding will continue to investigate pre- and postconsumptive processes independently, and these separate tracks will often yield important results. Yet, to answer many important questions, we must combine the two fields. Digestive physiologists and foraging ecologists should both "give a hoot" (C. Martinez del Rio, personal communication) about the other field. Foraging ecology matters—omitting or misidentifying the ecological constraints on foraging can render physiological experiments uninterpretable, if not downright meaningless. Likewise, digestive processing matters. Digestive enzymes influence diet choice (Martinez del Rio and Stevens 1989; Martinez del Rio et al. 1992). Internal handling of food in the gut matters—foods compete for processing in the gut, and past consumption influences future consumption (Forbes 2001; Whelan and Brown 2005; and see below).

While this chapter focuses on the interplay between foraging ecology and digestive physiology, we first consider the role of ecology, particularly that ofsearch strategies, in determining diet choice. Without variation in the diet, there is no need for variability in digestive physiology. Next, we briefly review digestive structure and function. Variability in digestive systems reflects variability in foraging ecology. We then describe a variety ofapproaches to forging tighter links between the two disciplines. We conclude with thoughts on current gaps in our understanding of pre- and postconsumptive processes and their integration, and we offer suggestions for future avenues ofresearch and pertinent readings.

5.3 Physiological Processes

In an Introductory Biology course at the University of Wisconsin, Professor John Neese remarked that we often think of the interior (lumen) of an animal's gut as being inside the animal. In fact, it is actually exterior space that exists as a cavity (as in cnidarians such as jellyfishes) or a tube (as in humans), created by invagination during very early development. When an organism ingests food for processing, what perhaps seems the end ofthe process to a foraging ecolo-gist is only the beginning of the process to a digestive physiologist: the important work of getting the food inside the forager (absorption) has only begun.

The digestive system breaks down macromolecules ofcarbohydrates, fats, and proteins into sugars, alcohols and fatty acids, and peptides and amino acids. The intestinal wall absorbs these products, transporting them into the circulatory system. But just how this is accomplished, as we will see below, differs considerably among animals with different diets. The last few decades have seen increasing investigations of wild (as opposed to domesticated) animals, revealing an astonishing array of digestive strategies (Hume 1989). Modeling frameworks adopted from optimality and chemical reactor theory have provided new analytic tools.

Preconsumptive Food Handling

The relationship between mouthparts and diet in virtually all taxa clearly reveals the importance of preconsumptive food handling (Labandeira 1997; Lentle et al. 2004; Magnhagen and Heibo 2001; Owen 1980; Schmidt-Nielson 1997; Smith and Skulason 1996). For instance, bill size and shape in birds clearly relate to diet (Benkman 1988; Denbow 2000; Grant 1986; Welty

1975). In their classic investigations of Darwin's finches, Grant and colleagues (e.g., Schluter and Grant 1984; Schluter et al. 1985) elegantly demonstrated the fit of bill size and shape to the prevailing supply of seeds and the remarkably rapid evolution of bill morphology in response to the changing availability of seeds differing in size and hardness. Many other taxa exhibit similar adaptations (Ehlinger 1990; Mittelbach et al. 1999; Smith and Skulason 1996).

Preconsumptive food handling may serve several functions, including preventing escape of the prey organism, preventing injury to the forager by the prey, and preparing the food for ingestion and more efficient postconsumptive processing. Herbivores consume diets of highly fibrous or woody plant parts, and many herbivore species possess grinding mouthparts that fragment cellulose and release cell contents (Owen 1980 and Schmidt-Nielson 1997 provide many examples). This grinding, or mastication, increases the surface area available to digestive enzymes, allowing more efficient chemical breakdown in the intestines. Many birds swallow their food whole and rely on a muscular gizzard (and sometimes, ingested small rocks or pebbles) to physically break down food before it passes into the intestines for digestive processing.

Prinz and Lucas (1997) provide another explanation for mastication in mammals, which combines the physical breaking down of food into small particles with lubrication from saliva. Previous work suggested that initiation of swallowing depended on separate thresholds for food particle size and for particle lubrication. It now appears instead that swallowing is initiated after "it is sensed that a batch of food particles is binding together under viscous forces so as to form a bolus" (Prinz and Lucas 1997, 1715). Bolus formation ensures that swallowed food will successfully pass the pharyngeal region with minimal risk of inhalation of small particles into the respiratory tract, an accident with potentially fatal consequences.

Some spider species chew their prey with their maxillae and then suck out the nutritious body fluids. Other spiders inject hydrolytic enzymes into their immobilized prey and then use their piercing mouthparts to suck out the resulting fluid. Cohen (1995) estimates that 79% of predaceous land-dwelling arthropods use extraoral digestion (EOD). Via extraoral digestion, these small-bodied predators increase their efficiency of nutrient extraction by abbreviating handling time and concentrating nutrients from the consumed foods (Cohen 1995). Venomous snakes inject toxins that not only immobilize prey, but also begin digestion prior to ingestion, when the prey is swallowed whole.

Gut Structure and Function

One can think of the digestive system (gut) as a tubular reactor that extends from the oral opening to the anus. A typical invertebrate's gut has three parts:

the headgut, corresponding to the oral cavity and pharynx; the foregut, corresponding to the esophagus and crop or stomach; and the intestine (Gardiner 1972). The foregut mainly transports food from the oral cavity to the intestine, but in some taxa with an enlarged crop and/or diverticula (blind sacs), the foregut may store food. In some invertebrates (e.g., insects), the intestine consists of the midgut, or ventriculus, and the hindgut, which includes the anterior intestine and the rectum. Most digestion and absorption take place in the midgut. The main role of the hindgut is to transport undigested material away from the midgut for expulsion, but it also is responsible for water, salt, and amino acid absorption, thus playing a role in water and salt balance (Romoser 1973; Stevens and Hume 1995).

Most of the components found in invertebrate digestive systems are also found in vertebrate systems (Stevens and Hume 1995). We divide the vertebrate digestive system into four parts: the headgut (including the oral cavity and pharynx, as well as the gill cavity in fishes and larval amphibians); the foregut (esophagus and stomach); the midgut (often referred to as the small intestine), including the duodenum, jejunum, and ileum as well as the pancreas and biliary system (which secrete enzymes and bile, respectively); and the hindgut (often referred to as the large intestine).

As stated above, food digestion typically begins with the process of mechanical breakdown and lubrication within the oral cavity. Saliva not only lubricates the bolus for transport through the esophagus to the stomach, but in some species, it may also contain the hydrolytic enzyme amylase, which digests carbohydrates (Stevens and Hume 1995). The stomach stores food and secretes HCl and pepsinogen, the precursor ofthe hydrolytic enzyme pepsin, to physically break down food and initiate protein digestion. After the food has been broken down sufficiently and transformed into a slurry (Karasov and Hume 1997), it moves to the small intestine, the principal site of both digestion and absorption.

The midgut is the primary location ofdigestion and absorption ofdigestive products into the circulatory system. The mechanism ofabsorption (active or passive; more on this below) has been a subject of considerable controversy and interest (Diamond 1991; Lane et al. 1999; Pappenheimer 1993; Pappenheimer et al. 1994; Pappenheimer and Reiss 1987). Within the midgut, mucosal folds and villi increase the surface area available for absorption tremendously (perhaps fractally; Pennycuick 1992). Villi are composed of absorptive cells known as enterocytes, whose own surface area is increased by the microvilli or brush border (Stevens and Hume 1995). The pancreas secretes enzymes that degrade carbohydrates, fats, and proteins. Biliary secretions, which include salts, phospholipids, cholesterol, and hydrophobic apolipoprotein fractions (Karasov and Hume 1997), are emulsifying agents important in fat digestion.

The gastric mucosa secretes pepsin, which digests proteins into polypeptides. A number of additional enzymes (e.g., trypsin, chymotrypsin) break polypeptides into amino acids. Carbohydrases, including amylase (secreted by the pancreas and by the salivary gland in some species), and glycosidases (e.g., sucrase, maltase, lactase) digest carbohydrates. Fats, which are insoluble in water, undergo a two-stage process ofemulsification and dispersion, followed by formation of small aggregates of mixed lipids and bile salts suspended within the ingesta, called micelles. Lipase, secreted by the pancreas, attacks the micelles and releases fatty acids, glycerol, and mono- and diglycerides. Other enzymes in the midgut include chitinase (which attacks chitin, a major structural carbohydrate in animals, fungi, and bacteria), found in many vertebrate taxa (Stevens and Hume 1995), and cellulase (which attacks cellulose), found only in microorganisms, some ofwhich are symbionts in some invertebrate and vertebrate guts.

The gut absorbs the products ofdigestive degradation via passive or carrier-mediated mechanisms. Passive mechanisms include transcellular diffusion, in which particles move through the cells (mainly lipophilic compounds), and paracellular diffusion, in which particles move between the cells (mainly wa-tersoluble compounds, including sugars, amino acids, and some vitamins). Carrier-mediated transport across the (apical) brush border and basolateral membranes of the enterocytes involves carrier proteins. Carrier-mediated transport is either active (involving investment ofenergy to transport the substance against an electrochemical concentration gradient) or facilitated (in which the substance is transported down an electrochemical gradient). In both cases, saturation of the carrier proteins places an upper bound on transport, following Michaelis-Menten kinetics. Carrier proteins appear to be the primary transport mechanisms for sugars, amino acids, some vitamins, and calcium.

Pappenheimer (Pappenheimer 1993, 2001; Pappenheimer et al. 1994;Pap-penheimer and Reiss 1987) proposed an alternative involving passive diffusion of sugars, amino acids, and other small molecules via a mechanism called para-cellular solvent drag. Briefly, concentrative sodium-dependent transcellular transport provides an osmotic force that triggers contraction ofthe cytoskele-tal proteins (tight junctions) regulating paracellular permeability, permitting solvent drag between absorptive cells. Pappenheimer (1993) estimated that the paracellular pathway may account for most (60%—80%) absorption of sugars and amino acids.

This controversial proposal has stimulated much research (Afik et al. 1997; Chang et al. 2004; Chediack et al. 2003; Ferraris and Diamond 1997; Karasov and Cork 1994; Lane et al. 1999: Lee et al. 1998; Levey and Cipollini 1996; Weiss et al. 1998). One attractive aspect of this mechanism is an almost instantaneous fine-tuning of the match of absorption to digestive loads because transport is proportional to solute concentration at cell junctions, which is proportional to the rate of hydrolysis (Pappenheimer 1993). A drawback of this mechanism is its nonspecificity, which could lead to the inadvertent uptake of toxins or secondary metabolites (Chediack et al. 2001). Lane et al. (1999) tested paracellular transport ofglucose in dogs and concluded that it plays, at most, a minor role (4%—7%) compared with carrier-mediated transport. Some low estimates of the extent of absorption by paracellular transport may be arti-factual, however, attributable to inhibition ofnormal villus microvascular responses to epithelial transport in anaesthetized animals (Pappenheimer and Michel 2003).

In contrast to amino acids, sugars, and vitamins, most products oflipid digestion (free fatty acids and monoglycerides) cross the brush border membrane by simple diffusion. Passive systems transport fatty acids and monoglycerides to the endoplasmic reticulum, where they are transformed into particles called chylomicrons, small milky globules of fat and protein. Chylomicrons enter the lymphatic vessel that penetrates into each villus, and the lymphatic system transports them to the blood.

Digesta are discharged from the midgut into the hindgut. In birds and mammals, a cecum (or paired ceca in birds) at thejunction of the midgut and hindgut often serves as a fermentation chamber. The hindgut serves for final storage of digesta, absorption of water (osmoregulation), bacterial fermentation, and feces formation (Laverty and Skadhauge 1999). The extent of these functions differs considerably among taxa in relation to diet. A carnivore's hindgut is a relatively passive structure, while herbivores have greatly enlarged hindguts that are critical fermentation chambers. The hindgut empties into the cloaca (in reptiles, birds, fetal mammals, some adult mammals) or the anus (in most mammals) (Stevens and Hume 1995).

This description ofdigestive system structure and function is very general, and great variety exists among taxa, as illustrated by the following examples. Ruminants possess a greatly enlarged and compartmentalized stomach (the rumen) and the ability to regurgitate, re-chew, and re-swallow their food. The rumen acts as a fermentation chamber, providing anaerobic conditions, constant temperature and pH, and good mixing (Church 1988). The only known avian foregut fermenter is the hoatzin (Opisthocomus hoazin). It has an enlarged muscular crop, containing mixed microflora and protozoans that do the work of fermentation throughout the crop and in the lower esophagus (Grajal 1995; Grajal et al. 1989). In lagomorphs (rabbits, hares, pika), the stomach is simple but elongated. Part of the small intestine has a dilated structure called the sacculus rotundus, and the cecum has a capacity roughly ten times that of stomach (Stevens and Hume 1995).

Figure 5.1. Sibly's optimality model relating retention time of food in the gut to net energy gain. Sibly reasoned that following ingestion, energy would at first have to be expended to break the chemical and/or physical defenses of foods against digestion (phase A in the figure). Once the defenses are breached, energy is quickly gained (phase B). As food digestion continues, net energy gain eventually diminishes until all potential energy has been acquired (phase C). T' indicates the length of food retention that maximizes the rate of net energy assimilation. T" indicates the length of food retention that is associated with complete assimilation of energy. (AfterSibly 1981.)

Retention Timerr

Figure 5.1. Sibly's optimality model relating retention time of food in the gut to net energy gain. Sibly reasoned that following ingestion, energy would at first have to be expended to break the chemical and/or physical defenses of foods against digestion (phase A in the figure). Once the defenses are breached, energy is quickly gained (phase B). As food digestion continues, net energy gain eventually diminishes until all potential energy has been acquired (phase C). T' indicates the length of food retention that maximizes the rate of net energy assimilation. T" indicates the length of food retention that is associated with complete assimilation of energy. (AfterSibly 1981.)

Optimality and Chemical Reactor Models

Sibly (1981) made the first optimality model of the digestive system. He assumed that digestive processes maximized the "rate at which energy is obtained by digestion" (109). He reasoned that, following ingestion, the rate of energy gain at first declines, because energy must be expended on breaking down food defenses before any nutrient absorption can take place. After the digestive system breaches the food's chemical defenses, the rate of energy acquisition rises rapidly at first, then declines as digestion proceeds (fig. 5.1). This scenario is reminiscent of the patch model (Charnov 1976b) because of the strong role of diminishing returns.

Sibly's model identified important relationships between two characteristics of digestive systems, gut volume and retention time. In addition, the model related these gut properties to food characteristics (see also Karasov 1990; Karasov and Diamond 1985). For a given gut volume, higher-quality food should be retained for shorter periods of time than lower-quality food. Letting E = the concentration of enzyme (or equivalent), C = the concentration of substrate, r = reation rate, T = retention time of food in the gut, k = gut volume, and Vo the flow rate of food through the gut, the model can be summarized by the following relationships (Karasov and Hume 1997):

n Vo

The extent (or efficiency) of the reaction (hydrolysis, absorption, etc.) is thus positively related to the concentration of enzyme and/or substrate and retention time of food in the gut; retention time is itself positively related to gut volume and inversely related to flow of food through the gut.

Chemical reactor theory allows a rigorous examination ofthe relationships in equation (5.1). Penry and Jumars (1986, 1987) introduced chemical reactor theory to the study of optimal gut design. They recognized the analogy between animal guts and reaction chambers used in industrial applications, and they applied the large body of theory on the physical chemistry of idealized reaction chambers to a variety of gut designs. Penry and Jumars (1986, 1987) analyzed three idealized reactor types: batch reactors, continuousflow, stirred-tank reactors (CSTR), and plug-flow reactors (PFR). These models describe mass transfer between phases (e.g., food reactants and enzyme reagents to products and untransformed reactants) using mass balance equations. Batch reactors are analogues for the gastrovascular cavities found in some invertebrates, including hydras and coelenterates; plug-flow reactors are analogues for the tubular guts found in most multicellular invertebrates and vertebrates; and continuous-flow, stirred-tank reactors are analogues for the large chambers found in foregut and hindgut fermenters. Models of actual animal guts often allow different idealized reaction chambers to be connected serially. For instance, a ruminant may be modeled as a large continuous-flow, stirred-tank reactor serially followed by a plug-flow reactor and then a small continuous-flow, stirred-tank reactor (Alexander 1994).

Chemical reactor models of guts have been heuristically useful by helping investigators diagnose the configurations ofdigestive systems and digesta flow within them; by specifying how the interplay of processing costs, reac-tant volumes, and reaction kinetics affects digestive system performance; and by spawning empirical tests of the predictions of specific models (Alexander 1991, 1993; Dade et al. 1990; Hume 1989; Jumars 2000a, 2000b; Jumars and Martinez del Rio 1999; Levey and Martinez del Rio 1999; Martinez del Rio and Karasov 1990; Martinez del Rio et al. 1994). Early models were general and permitted broad comparisons among widely different digestive systems. These early models indicated, for instance, that plug-flow reactors outperform both batch and continuous-flow, stirred-tank reactors for a given reactor volume and when reactions are catalytic, but continuous-flow, stirred-tank reactors outperform plug-flow reactors when reactions are autocatalytic. They also showed that a digestive system consisting of a continuous-flow, stirred-tank reactor/plug-flow reactor series was superior in performance on the low-quality foods eaten by foregut fermenters (Alexander 1991; Penry and Jumars 1987).

Later models, aimed at capturing the digestive systems of particular animals, incorporated specific physiological and/or ecological traits of the foragers under investigation (herbivorous fishes—Horn and Messer 1992; frugivorous and nectarivorous birds—Karasov and Cork 1996; Levey and Martinez del Rio 1999; Martinez del Rio and Karasov 1990; herbivorous insects—Yang andJoern 1994b; Woods and Kingsolver 1999). Some of these more specific models did not produce predictions that were upheld by empirical tests. For instance, Karasov and Cork (1996) and Lopez-Calleja et al. (1997) tested a model proposed by Martinez del Rio and Karasov (1990). In their work with the rainbow lorikeet (Trichoglossus haematodus), a species that absorbs sugars passively, Karasov and Cork expected that increased sugar concentrations in the diet would result in decreased retention times and extraction efficiencies. Neither prediction was upheld. Karasov and Cork (1996) suggested that the response ofthe lorikeet in their experiments was better interpreted as being consistent with the goal oftime minimization and extraction efficiency.

Lopez-Calleja et al. (1997) found that captive green-backed firecrowns (Sephanoides sephanoides), which absorb glucose actively (by carrier-mediated transport), exhibited close to complete assimilation of sugars and increased both food retention and inter-meal interval times with increasing sugar concentrations, as predicted by Martinez del Rio and Karasov's (1990) model. In contrast, they did not observe the predicted correlation between sugar concentration and daily energy intake. Lopez-Calleja et al. (1997) concluded that one objective function of the original model, energy maximization, was inappropriate for birds that were not growing, storing fat, or reproducing, and that a more appropriate objective under these conditions might be "sat-isficing" (Ward 1992).

The chemical reactor paradigm has proved useful as an organizing framework for constructing models and tests of gut structure and function. Jumars and Martinez del Rio (1999) and Levey and Martinez del Rio (2001) provide excellent discussions of chemical reactor models, including several explanations for why they sometimes fail: inaccurate estimation of the physiological parameters (processing [foraging] costs, gut volumes, reaction kinetics) or incorrect specification of the objective function (optimization criterion) itself. Section 5.4 (below) considers the challenges of measuring foraging costs. In addition, some important assumptions ofthe approach may not hold; for example, real guts may seldom be at a steady state (Penry and Jumars 1986, 1987).

Diet Composition and Modulation of Gut Structure and Function

Foraging ecologists often consider gut morphology, digestion and absorption biochemistry, and the flow rate of food through the gut as constraints on foraging behavior (Stephens and Krebs 1986). But digestive physiologists have long known that diet composition influences gut structure and gut function in a flexible way (Afik et al. 1995; Karasov 1996; Karasov and Hume 1997; Starck 2003). The interplay between gut function and diet composition gives the forager some leeway, allowing it to bend the rules (Foley and Cork 1992). In the following discussion, we use the term "modulation" to include acclimatization and regulation of gut structure and function in response to changes in diet composition.

The most dramatic example of gut modulation yet investigated involves foragers that undergo extreme bouts of feast and famine: sit-and-wait-for-aging snakes that feed at infrequent intervals, but consume 25%—160% of their body mass when they do. Examples include the boa constrictor (Boa constrictor), the Burmese python (Python molurus), and the sidewinder rattlesnake (Crotalus cerastes) (Secor and Diamond 1995, 2000; Secor 2003; but see Starck and Beese 2002; Starck 2003; Starck et al. 2004). In these snakes, the gut responds to extreme variation in contents: it is empty most ofthe time and only occasionally full. Changes in the structure and function of the gut at meal ingestion are among the highest recorded (Secor and Diamond 2000; Secor 2003; see also Hopkins et al. 2004). Less extreme variation in diet composition, such as seasonal switches between fruits and insects in passerine bird species (Levey and Karasov 1989, 1992), leads to more modest, but nonetheless significant, changes in gut function (Karasov 1996; Whelan et al. 2000).

Why do animals modulate their guts so dramatically? Why aren't they geared up for efficient food processing whenever the chance presents itself? Intuitively, it seems that active guts must be costly to maintain (Karasov and Diamond 1983; Karasov 1992, 1996), as the dramatic "up-regulation" in gut morphology and function after feeding in snakes suggests. Stevens and Hume (1995) summarize a number of studies showing that the contribution of the digestive system to total (whole-animal) oxygen consumption ranges from 12% in rats to 25% in pigs. They also document that protein synthesis is particularly high in actively proliferating or secreting tissues. In ruminants, for example, the gut wall constitutes a mere 6% of body protein, but accounts for a whopping 28%—46% of whole-animal protein synthesis.

When they fed fasting snakes, Secor and Diamond (2000) found a "10-to 17-fold increase in aerobic metabolism, 90%—180% increase in small intestinal mass, 37%—98% increases in masses of other organs active in nutrient processing, three- to 16-fold increases in intestinal nutrient transport rates, and five- to 30-fold increases in intestinal uptake capacities [integrated over the entire intestine]" within a single day. Following digestion, the digestive organs quickly atrophied to preconsumptive levels. Starck and Beese (2001, 2002) found that the mass of the snake's small intestine increases without cell proliferation because the mucosal epithelium, a transitional epithelium, can reversibly undergo enormous size changes. The cost of gut modulation in snakes may therefore owe more to changes in gut function (specific dynamic action, gastric processes involving digestion, protein synthesis, action ofasso-ciated organs) than to changes in gut structure (Overgaard et al. 2002; Secor 2003; Starck 2003).

American robins (Turdus migratorius) change their diets seasonally. Robins consume arthropods during the breeding season, but eat mostly fruit during the rest of the year (Levey and Karasov 1989, 1992; Martin et al. 1951; Wheelwright 1986, 1988; Whelan et al. 2000). In contrast to the dramatic short-term changes in snake guts, American robins do not increase absorption rates of sugars and amino acids when they switch to their fruit diet, nor do they compensate via changes in gut length, surface area, or volume. Instead, fruit-eating robins pass food more quickly than insect-eating robins. Short retention time is the key adaptation to frugivory in this (and other bird) species (Karasov 1996; Levey and Karasov 1989, 1992).

In the face of infrequent feedings, it is not surprising that the gut should atrophy (Piersma and Lindstrom 1997; Karasov et al. 2004). What is perhaps more surprising (and impressive) is how quickly the gut structure and function can be reconstituted. The robin-snake comparison tells us that the degree of modulation reflects the degree of diet change: from feast to famine in the python; from one food type (insect) to a second (fruit) in the robin. Digestive physiologists have observed gut modulation in many taxa (Starck 2003). This modulation can include changes in digestive enzymes, nutrient absorbers, gut structure, or gut retention time. Digestive modulation increases digestive efficiency (Karasov 1996; Whelan et al. 2000) and helps foragers meet their metabolic demands in the face of a shifting and sometimes unpredictable resource base.

5.4 Integrating Ecological and Physiological Processes

This section examines a number ofways to integrate digestive physiology and foraging ecology. To begin, we compare the disparate cost accounting practices of foraging ecologists and digestive physiologists. We argue that better integration of these costs will increase our understanding of both ecological and physiological processes.

Costs of Foraging

Foraging ecologists and digestive physiologists focus on different aspects of the costs of foraging. These differences reflect distinct perspectives on the intrinsic and extrinsic factors that influence foraging. To a foraging ecologist, intrinsic factors include the forager's search and attack strategies, habitat preferences, and susceptibilities to predation. Extrinsic factors are properties of the environment, such as the abundance and distribution of resources and predators, together with properties of the resource, such as ease of detection and capture. In contrast, to a digestive physiologist, intrinsic factors include the structure and function of the gut, including gut capacity, the suite of digestive enzymes, and transport mechanisms (active and passive) for moving nutrients from the gut lumen into the forager's bloodstream. Extrinsic factors include properties of the resource, such as the proportion of digestible versus refractory components, nitrogen content, and energetic value (see Karasov 1990 for extensive review and discussion).

Both perspectives offer valid insights, but they emphasize different costs. Improper accounting ofeither ecological or physiological costs can lead to errors in both ecological and physiological models, and thus to experimental manipulations that do not test the predictions of the models (see Jumars and Martinez del Rio 1999). Thoughtful integration of ecological and physiological approaches can help avoid errors.

From a physiological perspective, constraints on gut emptying impose frequent bouts ofinactivity as a hummingbird waits for its crop to clear before it can resume foraging. However, foraging hummingbirds may experience high predation risk (Lima 1991; Martinez del Rio 1992). From a foraging ecology perspective, we suggest that because hummingbirds are highly vulnerable while foraging, they have evolved a foraging strategy and an accompanying gut processing system that allows them to minimize their exposure to predation while maintaining a high rate ofenergy gain. Relyea and Auld (2004) present a related scenario involving tadpoles.

A difficulty arises because the physiological costs of foraging are quantifiable in joules expended, but not all ecological costs are. Physiological costs include the metabolic cost offoraging, the fixed cost ofmaintaining the digestive system, the variable cost of moving food through the digestive system, and the cost ofspecific dynamic action (also referred to as the thermogenic cost of foraging, which includes the enzymatic costs of food processing and the costs of chemosynthesis). Ecological costs not directly quantifiable in joules expended include the costs of predation risk and missed opportunities.

Foraging theory has solved the problem ofcosts measured in different currencies (see chap. 1). The fitness costs of predation danger or lost opportunities can be translated into a common currency by using experimental manipulations (Abrahams and Dill 1989; Nonacs and Dill 1990; Todd and Cowie 1990; Brown 1988) or the economic concept of marginal rates of substitution (Brown 1988; Brown, Kotler, and Valone 1994; Mitchell et al. 1990). The most powerful and flexible approach is that ofdynamic state variable models, described in chapters 1 and 7.

Linking Ecological and Physiological Processes

Ecological Consequences of Physiological Modulation

The harvest rate of a consumer in relation to resource abundance is known as the functional response. A widely used functional response model, Holling's disc equation [similar to equation (5.1.1)], includes variables representing conversion of food biomass to consumer biomass (e) and time needed to handle food (h). Whelan et al. (2000) developed models of gut function in which they assumed that these terms of the functional response implicitly incorporate physiological parameters, nutrient absorption, and gut handling of food (box 5.1). These models allow e and h to vary (independently or jointly) in response to changing diet composition in a manner that simulates physiological modulation. Through such modulation, two digestive modes emerge, each of which is more efficient at processing a particular diet. Modulation thus promotes diet switching and specialization. The models also indicate, as suggested by physiological investigations (Levey and Karasov 1992), that modulation incurs an initial cost, though it ultimately increases efficiency.

BOX 5.1 Modeling Digestive Modulation in an Ecological Framework

Christopher J. Whelan

Consider two perfectly substitutable resources denoted as 1 and 2 (Whelan et al. 2000). Let the forager's per capita growth rate be a monotonically increasing function of its feeding rate,f Let Holling's disc equation describe the feeding rate for an opportunistic forager seeking two co-occurring foods:

f = (e1a1R1 + e2a2R2) (5 1 1) (1 + a1hR1 + a2h2R2)'

where ei is net assimilated energy from consuming a food item i, ai is the encounter rate for a resource, hi is the handling time for a resource, and Ri represents the density of a resource (see Royama 1971 for a derivation).

We define a consumption isocline as all of the combinations of abundances, R1 and R2, such that a forager has the same feeding rate, k (Holt 1983; Brown and Mitchell 1989). To solve for the consumption isocline, we set equation (5.1.1) equal to a constant feeding rate k and solve for R2 in terms of R1:

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