Herbivory

Jonathan Newman

6.1 Prologue

It is 4:00 a.m. on a cold, wet midsummer's day in Southwest England. The 500 kg dairy cows have been grazing for 30 minutes. A network of eighteen video cameras in weatherproof cases stands ready to record events across the study site. By 8.30 p.m. the cows have grazed for 9 hours and spent another 7 hours ruminating (regurgitating and chewing). A bite recorder (fig. 6.1) has logged every jaw movement (more than 72,000 of them). Each cow has ingested more than 6 kg of food while roaming across the 11-hectare field. Meanwhile, in a nearby greenhouse, an experimenter places individual peach aphids onto small melon plants growing in 12 cm pots. Each 2 x 10-6 kg aphid wanders across the plant for 10—15 minutes, occasionally stopping to probe the plant, then inserts its stylet into the leafphloem and remains motionless for the next 2 hours, sucking in sap and expelling honeydew. It repeats this process, continuously, day and night.

What could possibly be interesting about these two foraging situations? Who cares, and why? Milk production depends critically on crude protein ingestion. Are the cows selecting a diet that maximizes their protein intake? Can we manipulate their natural behaviors to increase milk production? How can we maintain the pasture species composition and density in the face of the cows' foraging behavior? The lllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllllll

recorder

Figure 6.1. Cow wearing the Penning bite recorder. The recorder works by recording the stretching of the elastic band under the jaw. Jaw movements of different types stretch the elastic in characteristic ways. A computer program then converts these data into jaw movements of different types based on their characteristic shapes. See www.ultrasoundadvice.co.uk for more information.

recorder

Figure 6.1. Cow wearing the Penning bite recorder. The recorder works by recording the stretching of the elastic band under the jaw. Jaw movements of different types stretch the elastic in characteristic ways. A computer program then converts these data into jaw movements of different types based on their characteristic shapes. See www.ultrasoundadvice.co.uk for more information.

aphids' population dynamics are intimately linked to their diet, mainly to amino acid concentrations. Aphids can go through a generation in about 10 days, doubling their population size every 3 days under ideal conditions. Even at low densities, aphids can significantly reduce crop yields, and aphids are the most important vectors of plant viruses. Virus acquisition and transmission depends on aphid feeding behavior and movement on and between plants. Winged aphids facilitate the long-distance dispersal ofviruses. Winged morph production increases with increasing aphid density or decreasing plant quality. Both of these problems have major financial implications, and a complete understanding of foraging behavior will inform our responses.

6.2 Introduction

A videorecording of herbivores feeding is not the sort of footage that leads to many Trials of Life-type, glossy documentaries, narrated by important natural historians with English accents. Predation, parasitism, and other animal-animal interactions dominate these documentaries. Yet, when it comes to foraging, herbivory is vastly more common. Insect herbivores make up 25% of the extant macroscopic organisms on earth, and every green plant (another 25%) has insect herbivores (Bernays and Chapman 1994, 1). Most nonaquatic vertebrate herbivores can be found in four orders of eutherian mammals: Lagomorpha (ca. 60 spp.), Proboscidea (2 spp.), Perissodactyla (ca. 18 spp.), and Artiodactyla (ca. 174 spp.); in addition, many of the Rodentia (ca. 1,700 spp.) are at least sometimes herbivorous. Herbivores are also by far the most common vertebrate animals housed by humans—from laboratory rodents (tens of millions) to farmed cattle, sheep, and goats (hundreds of millions each) to horses, asses, and camels (tens of millions each). Whether you look at numbers of species, numbers of individuals, total biomass, or rates of flow of mass and energy, there is no denying the practical significance, ecological dominance, and evolutionary importance of herbivory.

Elephants (ca. 6,000 kg) and grasshoppers (ca. 0.001 kg) differ in body mass by more than six orders of magnitude, yet they face essentially the same foraging problems: where to eat, what to eat, how fast to eat, and how long to spend eating. I ignore taxonomic boundaries for most of this chapter and focus on how herbivores answer these questions. I will use two important ideas as my framework: first, that the answer to each of these four questions lies in the animal's objectives and constraints; second, that the answer to any one question depends, at least in part, on the answers to the others. Her-bivory is a compromise or trade-off between these four related questions. Finally, I will consider the dynamic nature of the herbivore-plant interaction. Herbivory and plant growth are tightly coupled. Short-term studies of individual foraging behavior provide important glimpses of the herbivore's behavioral repertoire, but rarely provide a complete picture ofits interaction with its food plants. Plant and animal respond dynamically to each other, and ultimately we must understand this dynamic to solve important applied problems such as ecosystem management, agricultural production, and the conservation of rare plants and animals.

Herbivory is the concern of ecologists, entomologists, agricultural scientists, range scientists, animal welfare scientists, conservation biologists, and marine scientists; even plant biologists get into the act. As one might imagine, there is relatively little communication across these disciplines. The literature on herbivory is very extensive, and the amount that any scientist can read is necessarily limited. Moreover, it is unevenly distributed among fields. For example, there are many more publications on the grazing behavior of sheep and cattle than on that of all 70 species of African ungulates combined. Can we learn much about the behavior of wild animals from the investigation of domesticated animals, or vice versa? I believe that a cross-disciplinary approach is beneficial and offer the following personal experience to support this view. In the early 1990s, I proposed to some colleagues that we should look at how sheep respond to predation pressure. They were, of course, incredulous, because there are no predators on sheep in Southwest England. Of course, they were correct—but sheep have lived on farms for only a small fraction of their evolutionary history, and there was no a priori reason to suppose that their antipredator behaviors had been lost. Indeed, predator avoidance was probably so heavily selected that there might be little genetic variance left in this suite of traits! Sure enough, sheep responded behaviorally to increases in feeding aggregation size in much the same way that wild animals do, by increasing their feeding time and decreasing their vigilance behavior (Penning et al. 1993). The evidence was not merely correlational, as it would probably have had to be if the subjects were antelope on the Serengeti. The data came from an experiment in which we randomly assigned individuals to different group sizes—something impossible on the African plains. My colleagues doubted the role of predation partially because their training as agricultural scientists did not prepare them for this possibility, even though predator effects seem basic to someone trained as an ecologist.

I believe that we can gain insight into the behavior of domesticated herbivores by studying their wild relatives, and vice versa. However, we must also remember that agricultural animals often result from unnatural husbandry practices (e.g., abnormally early weaning ages, small enclosure sizes, etc.) that can cause lifelong behavioral abnormalities. Such abnormalities can influence the outcome of any foraging experiment, sometimes subtly, sometimes overtly. Furthermore, those interested in applied problems may have to consider these abnormalities when implementing management strategies (see box

Synthesizing the vast and disparate literature on herbivore foraging behavior across disciplines, taxonomy, and body size in one book chapter is a tall order for anyone. So let's start by limiting the scope just a bit. I will focus on terrestrial herbivores, specifically generalist insect herbivores and vertebrates that are always or predominantly herbivorous. I will ignore seed eaters and root feeders, sticking mainly with animals that remove photosynthetically active material (although I will occasionally mention sap-sucking insects). With these obvious limitations in mind, let's start by looking broadly at foraging behavior along traditional taxonomic lines.

6.3 Herbivory: A Traditional Taxonomic Viewpoint

Entomologists categorize insect herbivores along a continuum from strictly monophagous (feeding from a single plant genus or species) to oligophagous (feeding on several genera within the same plant family) to polyphagous (feeding on plants from different families). Although examples of each type occur in all major insect taxa, the Orthoptera (grasshoppers and katydids) are the most polyphagous. Proven cases ofmonophagy are rare in this order. In other insect orders, 70% or more of the species are mono- or oligophagous (Bernays and Chapman 1994). Among the more specialized insect herbivores, some use more or less the entire plant, but more commonly species tend to be associated with particular plant parts. Specialization is the norm among holometabolous larvae (flies, beetles, and Lepidoptera), and in particular among the leaf miners (Bernays and Chapman 1994). Another good example of specialization is the approximately 3,000 species of aphids that feed almost entirely on sap from the phloem of a single species of host plant.

These observations about herbivorous insects lead to two remarks about the literature. First, much of the literature on their foraging behavior (in particular, on diet choice) consists of work on grasshoppers (over 2,500 papers in the last 25 years, more than 300 of which were on feeding behavior; CAB Agricultural Abstracts). Second, because many herbivorous insects are monophagous, students of insect herbivory see diet choice (host plant selection) as uninteresting. However, as Bernays and Chapman (1994) point out, females do not always select the most appropriate host, and some do not even lay eggs on the host plant, but rather nearby. Even when on the proper host species, larvae often need to move as the quality ofthe present host individual declines, so it is probably safe to say that the majority of insect herbivores show some form ofhost plant choice. When entomologists have studied host plant selection, they have typically focused on chemical cues in the form of attractants, repellents, phagostimulants, and deterrents. A quick survey of this literature will give the impression that we know a great deal about the mechanisms of host plant selection, but this impression would be wrong, since we've studied only a small fraction of the total number of phytophagous insects.

Vertebrate herbivores are less numerous and less diverse than insect herbivores, but their sheer size means that they have large effects on plant communities. For this reason, they have attracted the attention ofecologists. Pastoral agriculture occupies some 20% of the global land surface and is the focus of agricultural and range scientists. It is obviously economically important, and as a predominant form ofland use in some ofthe more fragile areas ofthe world, it is of considerable interest to conservation biologists (Hodgson and Illius 1996, ix).

In comparison with animal tissue, plant material is low in nitrogen and high in fiber, and animals can digest it only slowly. While animals can easily digest the contents ofplant cells, they cannot digest the cellulose and hemicellulose that constitute plant cell walls, in most cases because they lack cellulase enzymes. Many vertebrate herbivores solve this problem using fermentation in the gut, where symbiotic bacteria digest the cell walls. The rate of clearance ofthe indigestible plant components from the gastrointestinal tract limits the ability ofmost vertebrate herbivores to process large quantities offood. David Raubenheimer considers this topic further in box 6.1.

BOX 6.1 Herbivory versus Carnivory: Different Means for Similar Ends

David Raubenheimer

When the nineteenth-century American psychologist William James (James 1890) wrote that living organisms are characterized by attaining "consistent ends using variable means," he was referring to the fact that an animal's homeostatic responses (e.g., alterations in the rate of food intake) counteract environmental variations (e.g., in the nutrient density of foods), thus maintaining a constant outcome (e.g., satisfying its nutrient requirements). He could just as well have been referring to the nutritional responses of animals at the longer, evolutionary time scale. There is, for instance, no evidence that groups as trophically divergent as herbivores and carnivores differ substantially in their tissue-level requirements for nutrients, but there are major differences in their means of satisfying those requirements.

The means ofsatisfying tissue-level nutrient requirements can, broadly speaking, be separated into two processes: the acquisition of foods from the environment (foraging) and the acquisition of nutrients from foods (food processing). Broadly speaking, the nutritional challenge for carnivores is to find, capture, and subdue scarce or behaviorally sophisticated packages of high-quality food, while herbivores target abundant but nutritionally inferior foods. Not surprisingly, therefore, the conspicuous nutritional adaptations ofcarnivores are concerned with acquiring food from the environment, and those of herbivores with extracting nutrients from foods. Here I will briefly outline some of the behavior-related adaptations involved in food acquisition by carnivores before turning to the food-processing adaptations of herbivores.

Food Acquisition

As a consequence ofthe relative scarcity of their food, carnivores typically maintain larger home ranges than do herbivores (McNab 1963; Schoener 1968; for an exception, see Garland et al. 1993). Their body size, too, tends to be larger than that of their quarry (Carbone et al. 1999). While this helps in subduing prey, it also has disadvantages, such as reduced maneuverability (Harvey and Gittleman 1992) and a reduction in nutritional gain per prey captured. Not surprisingly, therefore, there are predators that have adapted to eating prey larger than themselves; among the most spectacular examples are some snakes that eat animals up to 160% of their body weight (Secor and

Diamond 1998). Some mammalian predators use cooperative hunting as a means of capturing prey larger than themselves (Caro and Fitzgibbon 1992).

Carnivores typically have morphological and sensory features in common. These features include forward-facing eye sockets, which help in judging distances (Westheimer 1994) and also enhance visual sensitivity at low light levels (Lythgoe 1979). The eye sockets of prey species, by comparison, tend to be laterally placed, increasing the overall angle ofvision in which predators can be perceived (Hughes 1971). The retinas of predators typically have specialized areas of high-resolution vision called foveae and areae. These are particularly well developed in birds of prey (Meyer 1977), but are also found in mammals (Dowling and Dubin 1984), and analogous structures occur in the compound eyes of insect predators (Land 1985). Predatory fishes, too, have specialized visual adaptations. Game fishes often feed in twilight, since they have a visual advantage over their prey at low light intensities. This advantage is achieved by having unusually large, and hence more sensitive, photoreceptors compared with those of their prey (Munz and McFarland 1977).

The challenges of a predatory lifestyle are also reflected in brain structure (Striedter 2005). Among small mammals, for instance, those that prey on insects tend to have larger relative brain sizes than do herbivores (Mace et al. 1981). However, Bennett and Harvey (1985) failed to find an overall correlation between diet and relative brain size in birds. This might be because it is not the size ofthe brain asawhole that is selected in relation to the animal's lifestyle, but rather the relative sizes of a number of functionally distinct subsystems (Barton and Harvey 2000). For example, the relative size ofthe tectospinal tract, a pathway involved in movements associated with the pursuit and capture ofprey, increases with the proportion ofprey in the diets of different mammalian species (Barton and Dean 1993). Interpreting such differences as evolutionary adaptations for predation should, however, be done with caution, since brain size and structure are notably susceptible to activity-dependent developmental influences (Elman et al. 1996). Thus, London taxi drivers have an enlarged posterior hippocampus (involved in spatial memory) (Maguire et al. 2000); I doubt whether even the most ardent adaptationist would attribute this to differential survival in the urban jungle!

(Box 6.1 continued) Nutrient Acquisition

Compared with animal prey, plant tissue is generally more abundant and more easily captured and subdued, but once ingested, it is nutritionally less compliant. The contents of plant cells are enclosed in fibrous cell walls consisting predominately of compounds such as lignin and cellulose that are difficult to degrade enzymatically. These structural compounds both impede access to the nutrients contained in the cytoplasm (Abe and Hi-gashi 1991) and lower the concentration of nutrients such as protein and digestible carbohydrate (Robbins 1993). Plant tissue is also highly variable in its ratios of component nutrients (Dearing and Schall 1992) and often contains deterrents and toxins (Rosenthal and Berenbaum 1992).

Foragers can ameliorate these problems to some extent via food selection, as suggested by the observation that many mammalian herbivores favor foliage with a relatively high nitrogen and low fiber content (Cork and Foley 1991). Since the fiber that produces leaf toughness is likely to be tasteless, it has been suggested that this selectivity might be achieved through perceiving toughness directly (Choong et al. 1992; Lucas 1994); it is, however, also possible that taste perception of low levels of nutrients is involved (Simpson and Raubenheimer 1996). The avoidance of plant fiber might be particularly important for small endothermic animals, which have a high relative metabolic rate and hence high energy requirements. Evidence from mammals supports this prediction: the proportion of species eating fibrous plant tissues declines, and the proportion selecting low-fiber plant and animal tissues increases, with decreasing body size (Cork 1994). This might explain the scarcity of herbivorous species among birds (Lopez-Calleja and Bozinovic 2000).

Rather than avoiding plant fiber, many herbivores have structures that are adapted for degrading it mechanically, releasing the cell contents for digestion and absorption. These structures include specially adapted teeth andjaws in mammals (Lucas 1994), mandibles in insects (Bernays 1991), and teeth, jaws, and post-oral pharyngeal mills in fishes (Clements and Raubenheimer 2005). An alternative, or complement, to mechanical breakdown is the enzymatic degradation of plant fiber. In mammals, which do not produce cellulytic enzymes, fiber digestion is achieved with the aid of symbiotic microorganisms, usually bacteria or protozoans and occasionally fungi (Langer 1994). Some herbivorous fishes (Clements and Choat 1995), birds (Grajal 1995), and insects likewise have microbe-mediated fermentation, while some insects and other arthropods can synthesize endogenous cellulases (Martin 1991; Slaytor 1992; Scrivener and Slaytor 1994; Watanabe and Tokuda 2001). Enzymatic degradation of structural carbohydrates has the added advantage ofmaking the energetic breakdown products available to the herbivore, and where microbes are involved, mi-crobial proteins and B-complex vitamins are further useful by-products (Stevens and Hume 1995).

Despite (and in many instances because of) these mechanisms for cellulose digestion, the guts of many herbivores have structural specializations for subsisting on plant tissue. Gut size is known to increase with decreasing nutrient content of foods (both within and between species) in a wide range of animals, including mammals (Martin et al. 1985; Cork 1994), birds (Sibly 1981), fishes (Horn 1989; Kramer 1995), reptiles (Stevens and Hume 1995), insects (Yang and Joern 1994a), and polychaete annelids (Penry and Jumars 1990). Larger guts allow a greater rate of nutrient uptake and, in some cases, greater efficiency of digestion (Sibly 1981).

Not only the size, but also the shape of the gut is modified in many herbivores. All else being equal, digestion is thought to occur most rapidly where there is a continuous flow of food through a slender tubular gut, with little opportunity for the mixing of foods ingested at different times (Alexander 1994). Such "plug-flow reactors" (Penry and Jumars 1986, 1987) are often found in carnivores (Penry and Jumars 1990; Alexander 1991). They are less suitable for herbivores that rely on microbial symbioses for cellulose degradation, because in such a system the microbes would be swept away in the flow of food through the gut (Alexander 1994). A population ofmicrobes can, however, be maintained indefinitely in a digestive chamber wide enough to ensure continuous mixing of its contents (a "continuous-flow, stirred-tank reactor"), and indeed, such chambers are a conspicuous feature of the guts of herbivores. Many, including ruminants such as cows, have developed fermentation chambers in the foregut, while others (e.g., horses) have an enlarged hindgut (caecum and/or colon). Fore-gut and hindgut fermentation are very different strategies for dealing with low-quality foods; the former is associated with long digestion times and particularly poor-quality foods, and the latter with differentially retaining the more rapidly fermented component and egesting the rest (Alexander 1993; Bjornhag 1994). Not surprisingly, therefore, mammalian herbivores tend to be either foregut or hindgut fermenters, but not both

(Martin et al. 1985). It is generally only large herbivores, with low mass-specific metabolic rates, that can afford the slow passage times associated with foregut fermentation of high-fiber foods (Cork 1994). Interestingly, some herbivorous mammals (Hume and Sakaguchi 1991) and fishes (Mountfort et al. 2002) have significant levels of microbial fermentation without appreciably specialized gut morphology.

An important but relatively neglected problem associated with herbivorous diets is nutritional balance (Raubenheimer and Simpson 1997; Simpson and Raubenheimer 2000). Compared with animal-derived foods, plants are believed to be more variable in the ratios of nutrients they contain (Dearing and Schall 1992), and they are generally poor in nutrients, such that "most single plant foods are inadequate for the growth of juvenile animals and their development to sexual maturity" (Moir 1994). This observation leads to the expectation that herbivores should be significantly more adept than carnivores at independently regulating the levels of different nutrients acquired (i.e., at balancing their nutrient intake). Some insect herbivores do, indeed, have a remarkable ability to compose a balanced diet by switching among nutritionally imbalanced but complementary foods (Chambers et al. 1995; Raubenheimer and Jones 2006). Such responses are mediated largely by the taste receptors, which "monitor" simultaneously the levels of proteins and sugars in the food and in the hemolymph, and also involve longer-term feedbacks due to learning (Simpson and Raubenheimer 1993a; Raubenheimer and Simpson 1997). Mechanisms for nutrient balancing might also exist at the level ofnutrient absorption (Raubenheimer and Simpson 1998).

It remains uncertain, however, whether nutrient balancing is in general better developed in herbivores because some carnivores, too, have been shown to perform better on mixed diets (Krebs and Avery 1984; Uetz et al. 1992) and to select a nutritionally balanced diet (Mayntz et al. 2005). One possibility, suggested by physiological data, is that both groups are adept nutrient balancers, but with respect to different nutrients. For example, domestic cats (which are obligate carnivores) apparently lack taste receptors for sugars and have low sensitivity to sodium chloride (neither of which are important components of meat), but have impressive sensitivity for distinguishing among amino acids (Bradshaw et al. 1996). Similarly, unlike some omnivores and herbivores, cats are unable to regulate the density of carbohydrate absorption sites in the gut in response to nutritionally imbalanced diets, but do regulate the activities of amino acid transporters (Buddington et al. 1991).

Why should carnivores have evolved mechanisms for nutrient balancing? Perhaps the nutritional variability of their food has been underestimated. Alternatively, the answer might be found not on the nutritional supply side, but on the demand side. Ifvariation in tissue-level demand for, say, different amino acids by a predator is high (e.g., with different activity levels, diurnal cycles, reproductive state, etc.), then no single food composition will be balanced, and the animal will require specific adaptations to differentially regulate acquisition ofthe various amino acids. Although little is known about such variation in the nutrient needs of either carnivores or herbivores, if it turns out to be significant, then William James's dictum might need revising: animals are characterized by attaining "variable ends using variable means."

The nutritional limitations of plant material have important consequences for body size. Comparative work shows that the metabolic requirements of mammals increase with body mass0 75, but the capacity ofthe gastrointestinal tract increases with body mass10 (Iason and Van Wieren 1999). Therefore, smaller animals have higher mass-specific energy requirements, but lack proportionally large gut capacities, and therefore require more nutritious forage (sometimes known as the Bell-Jarman principle, after Bell 1970 and Jarman 1974). These allometric considerations suggest that the smallest ruminant mammal should be at least 15 kg and the smallest nonruminant mammal at least 1 kg (see, e.g., Iason and Van Wieren 1999 for more discussion).

For much of the remainder of this chapter, I will ignore taxonomy and attempt an organization ofthe current state ofthe field around what I call the big questions. Herbivores can differ in many ways, but they all must answer the four questions listed above.

Four Big Questions

In the study of herbivore foraging behavior, four big questions interest us.

Where Will the Animal Eat?

Although I pose this as a single question, the problem exists at several spatial scales. At large scales, the question is one ofhabitat selection. Should the animal forage in the uplands or the lowlands? Should it graze near the forest edge or by the river? Within a habitat, at a smaller spatial scale, the question is one of patch selection. Should the animal graze from patches of tall vegetation, sacrificing plant quality for a faster intake rate, or should she graze from shorter patches where the plant quality is higher, but the intake rate is lower? At even finer spatial scales, some animals choose among parts ofa single plant. For example, aphids prefer to feed at the base of grass plants, rather than out on the leaves.

This question may concern patch exploitation (see chap. 1 in Stephens and Krebs 1986), but it is important to consider both the "attack" decision (which patches to use) and the "exploitation" decision (how long to use a patch). An example may help to clarify this distinction: consider the cows from the prologue (section 6.1). What may seem to be a homogeneous pasture is likely to comprise patches that differ in plant species composition, vegetation height and density, presence of parasites, plant quality (often due to previous grazing and dung and urine deposition), and so on. These patterns may follow an environmental gradient (e.g., the slope), or they may arise through the previous grazing patterns of the cows or other animals. How does a cow choose among these patches? The patch exploitation model in its simplest form is ill equipped to deal with such heterogeneity.

What Will the Animal Eat?

What to eat is, principally, a question of diet selection. It is the kind of question addressed by the classic diet model, but often complicated by the continuous nature ofsome vegetation and the postingestive consequences offood choice (see chap. 5 in this volume). When the animal is faced with an array of potential food sources, which should be included in the diet and which ignored? This question applies not only to different plant species, but also to plants of the same species that differ in growth or regrowth states. Should a grasshopper eat young ryegrass leaves but avoid older leaves? Should a sheep graze patches of tall fescue when they are 5 to 7 days from their last defoliation, but not sooner (because the bite mass is too low) or later (because the plant quality is too low)?

At some finer spatial scales, we may ask what parts of the plant the animal feeds from, but I don't view this as the big question. I include host plant selection by invertebrate herbivores here, rather than in the previous question, although this may be just an issue ofsemantics.

How Fast Will the Animal Eat?

How fast to eat is the question of intake rate. The animal's environment and morphology sometimes constrain its intake rate, but often intake rate is a behavioral choice. I will elaborate on this distinction in section 6.5. There are digestive consequences that accompany the choice of intake rate. An animal can increase ingestion by chewing less thoroughly, but this can slow passage rate and reduce digestion.

How Long Will the Animal Spend Eating?

While how long to eat might be a question of bout length, for most herbivores the big question is total foraging time. Time spent foraging incurs opportunity costs because it is time not spent avoiding predators, engaging in social interactions, reproducing, ruminating, and so on. There are environmental and physical/morphological constraints on foraging time, and I will elaborate on these in section 6.6, but often foraging time is a behavioral choice.

Reductionism and the Big Questions

Animals rarely answer the big questions piecemeal. Available diet choice and intake rate can determine habitat choice. Intake rate can determine diet choice, and vice versa. Diet choice can determine grazing time, and vice versa. Ultimately, herbivory is the integration of these four questions. The study of one question in isolation may help us to determine how these questions are integrated, but it will rarely yield the total picture. In the next four sections, I will consider what we know about herbivore behavior in light of each of these questions, but remain mindful ofthe interactions among the questions.

Different animals have different constraints and objectives, and so they come to different compromises between the answers to these questions. There is no "grand unified theory of herbivory," but an understanding of these tradeoffs and accommodations will help to provide a coherent framework for studying herbivory. I will discuss the experimental treatment of interactions among the questions in section 6.8.

6.4 Diet Selection

To understand herbivore diet selection, we need to think about how the animal's goals and constraints operate. Students of herbivory have expressed considerable interest in classic "optimal" foraging theory, but the literature contains a variety of misconceptions, owing perhaps to the fact that many researchers who study herbivory come from a background not in behavioral ecology, but in agriculture, range science, or entomology. As Ydenberg et al. make clear in chapter 1, foraging theory is not synonymous with intake rate maximization (cf. Dumont 1995). Foraging theory is about maximizing an objective function. In early studies of "optimal foraging," the objective function of interest was the rate of energy intake, as it was thought that, in some cases at least, the rate of energy intake might be a good surrogate for evolutionary fitness. A smaller family of models considered minimizing the foraging time required to meet a fixed intake requirement. It should be obvious that these two objective functions are similar, although not identical.

Authors have used the term "rate maximization" rather cavalierly in recent publications on herbivory, particularly in the agricultural literature. The original foraging theory models clearly hypothesized that the objective being maximized was net energy intake rate, not gross energy intake rate. Tactics that maximize gross intake rate also maximize net intake rate if there are no differences in digestibility or foraging costs. Vegetation varies dramatically in gross energy content, digestibility, passage rates, concentrations ofsecondary metabolites, and so on; thus, maximization ofgross energy intake is rarely an appropriate objective.

Both intake rate maximization and time minimization remain popular objective functions in models of herbivory and as alternative hypotheses in experiments (e.g., Distel et al. 1995; Focardi and Marcellini 1995; Forchhammer and Boomsma 1995; Farnsworth and Illius 1996, 1998; Van Wieren 1996; Torres and Bozinovic 1997b; Ferguson et al. 1999; Illius et al. 1999; Fortin

2001), but there are other objective functions that one should consider. For some animals, a particular nutrient acts as a limiting resource (for example, crude protein); in these cases, energy is clearly the wrong surrogate for fitness (see Berteaux et al. 1998). Researchers have considered several currencies other than rate maximization, including optimization of growth rate (Smith et al. 2001), ruminal conditions (Cooper et al. 1996), oxygen use efficiency (Ketelaars and Tolkamp 1991, 1992; Emmans and Kyriazakis 1995; Nolet

2002), and survival maximization (Newman et al. 1995). I will come back to the question of objective functions when I consider intake behavior. For now, I will simply state that the appropriate objective function surely differs among herbivores of differing body sizes, guilds, and digestive physiologies.

Empiricists often use simple foraging models a straw man. These models may fail because, as a mathematical convenience and as a first level ofsimplification (one goal of a model, after all), they ignore important constraints. Foraging theory says that animals should maximize their fitness (or some appropriate surrogate) subject to their constraints. Indeed, the goal of an optimality research strategy is to identify the objective function and important constraints—not to test whether animals are optimal per se (Mitchell and Valone 1990). Let's consider the potential constraints, which I will refer to broadly as environmental and physiological/morphological. In many cases, the constraints are those that the animal has evolved to work within or around, but in other instances (e.g., intensive farming), they are not.

Herbivores face many of the same constraints as nonherbivores. For example, many large vertebrate herbivores are social animals, and social context often plays a role in determining their diet choice. Dumont and Boissy (1999, 2000) have shown that sheep may forgo an opportunity to graze more selectively if this means they must leave their social group, even temporarily (though Sevi et al. [1999] failed to find this effect). Rearing conditions also may alter diet selection (Sutherland et al. 2000; box 6.2). We'll revisit the issue ofgregariousness when we look at intake rate decisions.

BOX 6.2 Animal Farm: Food Provisioning and Abnormal Oral Behaviors in Captive Herbivores

Georgia Mason

Drooling, the stalled cow rhythmically twirls her tongue in circles. She does this for hours a day, as do many of her barnmates. Next door, the stabled horse repeatedly bites his manger, pulling on the wood with his teeth (fig. 6.2.1). He has done this for years—all his adult life. A foraging biologist should find such bizarre activities interesting because they raise new questions about the control of herbivore feeding. They also highlight a real need for more fundamental research—one made urgent by the welfare problems that these behaviors probably indicate. Here I will describe these abnormal behaviors before discussing their possible causes and the research questions they raise.

Figure 6.2.1. Stabled horses may perform a number of abnormal oral behaviors, including crib biting. (After a photo by C.J. Nicol.)

Figure 6.2.1. Stabled horses may perform a number of abnormal oral behaviors, including crib biting. (After a photo by C.J. Nicol.)

Strange, apparently functionless oral behaviors are common in ungulates on farms and in zoos. Some, like the tongue twirling and crib biting described above, resemble the pacing of caged tigers and other "stereotypies" (Mason 1991) in having an unvarying, rhythmic quality and no obvious goal or function (e.g., Redbo 1992; Sato et al. 1992; McGreevy et al. 1995; Nicol 2000). Others, like wool eating by farmed sheep or wood chewing by stabled horses (e.g., Sambraus 1985; McGreevy et al. 1995), involve more variable motor patterns and an apparent goal, but still puzzle us by seeming functionless and different from anything seen in the wild. These activities can be time-consuming—stall-housed sows may spend over 4 hours a day in sham chewing, bar biting, and similar behaviors— and common—for example, shown by over 40% of the cattle in a barn (reviewed in Bergeron et al. 2006). Dietary regime seems to be the main influence, with abnormal behaviors most evident in populations fed only processed foodstuffs (e.g., milled, highly concentrated pellets; reviewed in Bergeron et al. 2006). Sometimes it is unclear what elicits individual bouts, but often it is eating, with the behaviors being displayed soon after the animal has consumed its food (e.g., Terlouw et al. 1991; Gillham et al. 1994).

In form and timing, this pattern differs from the typical picture for captive carnivores, which pace, and do so before feeding, even when they are fed highly processed food (e.g., Clubb and Vickery 2006). But are these differences caused by underlying biological traits or merely by differences in husbandry (Mason and Mendl 1997)? Would captive carnivores bar-bite and tongue-roll if taken from their mothers before natural weaning (as happens to most pigs and cattle), underfed (the case for many pigs), or kept in narrow, physically restrictive stalls? A survey controlling for these factors (Mason et al. 2006) showed that ungulates are inherently prone to abnormal oral behaviors (fig. 6.2.2), with wall-licking giraffes (Bashaw et al. 2001), tongue-rolling okapis, and dirt-eating Przewalski's horses (e.g., Hintz et al. 1976; Ganslosser and Brunner 1997) just some of the cases adding to the agricultural data. These observations do not provide sufficient phylogenetically independent contrasts to link abnormal oral behaviors with herbivory per se, but their form, timing, and links with feeding regimes strongly implicate foraging. How could ungulates' specializations for herbivory lead to these behaviors? Three hypotheses have been advanced, each essentially untested.

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