13 Foraging and the Ecology of Fear Joel S. Brown and Burt P. Kotler 13.1 Prologue The reintroduction of wolves in 1995 changed Yellowstone National Park. Riparian habitats have seen a marked increase in willows and aspen. The streams running through these willow thickets meander more. Wetlands have reappeared. Birds and butterflies haveincreased in the taller and more complex galleries along the riparian stretches, and they breed more successfully than before. Can wolves really have such restorative power? Wolves reshaped the Yellowstone ecosystem through their effects on elk. Without wolves, elk could forage anywhere with impunity. They browsed their way through every aspen and willow grove and prevented regeneration. The riparian galleries gradually disappeared, which in turn led to the near-extinction of beavers. Without beavers, streams ran faster and eroded more, and the marshy wetlands im- pounded behind beaver dams and diggings were lost. Things changed when the wolves came back. Of course, wolves devour elk, but much more importantly, they scare them. Frightened elk spend more time vigilant and less time feeding. They bunch up more, which lowers their feeding efficiency. Most of all, fearful elk avoid dangerous habitats such as thickets. Frightened elk released the willows and the aspen, which formed thickets with tall canopies that 438 Joel S. Brown and Burt P. Kotler created new habitat for birds and brought about a recovery of beavers and their activities. Streamssloweddown and returnedto their earlier meandering form. Fear can be a powerful ecological force. 13.2 Introduction Predators kill prey. With this in mind, Schaller (1975), in his classic book The Serengeti Lion, documented just how many prey lions kill. Although lions kill large numbers of wildebeests and zebras, the number killed represents only a small fraction of the prey population. Schaller reasonably concluded that lions contribute little to the regulation of their prey’s population sizes. Lions kill too few individuals to regulate prey populations. Another feature of Serengeti grazers is their apparent restraint in grazing their pastures. Compared with domestic grazers such as goats, sheep, and cattle, the Serengeti’s natural grazers seem to leave a lot of food uneaten. Per- haps wild grazers are more sophisticated, prudently leaving some vegetation uneaten to generate new fodder for tomorrow. In domestic grazers, centuries of artificial selection for productivity have reduced vigilance and increased consumption (see chap. 6), a luxury that wild grazerscannot afford. However, fear, rather than prudence, probably drives the Serengeti grazers’ restraint. Gustafsson et al. (1999) ran domestic and wild-type pigs (Susscrofa) through an identical foraging challenge. The domestic pigs won. The researchers noted that the wild pigs seemed distracted and not fully attentive to their foraging tasks. Lions and other predators are important to their prey’s ecology more for the fear they instill than the mortality they cause directly (Sinclair and Arcese 1995). Death by a predator makes the threat credible, but the threat itself is enough to leave an indelible mark on the ecology of prey and predators. Fear induces prey to forage more tentatively, in fewer places, in larger groups, or at restricted times. Fear by prey induces behavioral countermea- sures on the part of their predators—predators use stealth, boldness, and habi- tat selection to manage fear in their prey. The prey species’ altered feeding patterns cascade down thefood chain to affect the prey’sresources—the vege- tation of the Serengeti would be radically different in the face of fearless graz- ers. Fear not only strongly affects the foraging behavior of prey (see chap. 9), but also affects the foraging behavior of predators (predator-prey foraging games), the population dynamics of predator and prey (see chap. 11), the food of the prey (via trophic cascades), community interactions among prey and predator species (mechanisms of coexistence; see chap. 12), coadaptations be- tween behaviors and morphologies (coevolution), and the conservation and Foraging and the Ecology of Fear 439 management of natural areas (see chap. 14). Allthese topics fall under the ecol- ogy of fear. Box 13.1 considers a mechanistic approach to fear, outlining the endocrine correlates of stress and the interplay between stress and starvation avoidance. BOX 13.1 Stress Hormones and the Predation-Starvation Trade-off Vladimir V. Pravosudov Animals usually elevate their levels of glucocorticoid hormones in re- sponse to stress. This response, which is considered a homeostatic mech- anism (Wingfield et al. 1997; Silverin 1998), is an important adaptation to short-term changes in the social and physical environment that directs behavior toward immediate survival. Long-lasting stress, however, can cause chronically elevated levels of glucocorticoid hormones that produce many deleterious side effects, such as wasting of muscle tissue, suppressed memory and immune function, neuronal death, and reduced neurogenesis in the hippocampus (Sapolsky 1992; Wingfield et al. 1998; McEwen 2000; Gould et al. 2000). Stress and stress responses are relevant to the study of predation-star- vation trade-offs. Experiments increasing predationrisk, for example,have recorded effects on energy management (e.g., Witter and Cuthill 1993; Pravosudov and Grubb 1997), but in some cases individual birds reduced their body mass, while in others birds actually increased their mass after exposure to a model predator (e.g., Pravosudov and Grubb 1997, 1998; van der Veen and Sivars 2000). To interpret these results properly, it is im- portant to understand the hormonal mechanisms underlying mass change. Cockrem and Silverin (2002) recently demonstrated that captive great tits (Parus major) responded to the presentation of a stuffed owl with increasing corticosterone levels, whereas free-ranging tits exposed to a stuffed owl did not. These results suggest that studies of captive an- imals may not accurately reflect the response of free-ranging birds to heightened risk of predation. Animals confined to small laboratory spaces may show longer or stronger stress responses in response to a predator stimulus than the same stimulus would produce in the wild. For exam- ple, small rodents exposed to an owl call in a restricted laboratory space immediately showed elevated levels of glucocorticoid hormones (Eilam et al. 1999), but that does not mean that these animals would do so in natural conditions, or that the elevated levels would persist as long. (Box 13.1 continued) In fact, much of the research on energy regulation in birds has been car- ried out in captivity (e.g., Witter and Cuthill 1993; Pravosudov and Grubb 1997). The concentration of plasma corticosterone may increase not only as a result of experimental treatment, but also as a result of stressful con- ditions in captivity. For example, Swaddle and Biewener (2000) reported that additional exercise in captive starlings (Sturnus vulgaris) resulted in reduced flight muscle mass. They concluded that birds strategically reduce muscle mass to reduce flight costs. However, it seems possible that the experimental birds could have perceived the experimentally induced ex- ercise as stressful and responded with elevated corticosterone levels, which are known to result in loss of protein from flight muscles (Wingfield et al. 1998). Sadly, the birds’ corticosterone levels were not measured in this study, and the question becomes whether natural increases in flight ac- tivity would also result in corticosterone elevation. The possibility that the experimental birds were stressed because of the treatment in captiv- ity means that we must be careful in interpreting the results of such an experiment. With this caveat in mind, we should nevertheless recognize that short- term responses to predator exposure that increase an individual’s chances of escape—for example, by helping to mobilize energy reserves (Wingfield et al. 1998; Silverin 1998)—could be adaptive. Glucocorticoid hormones may also mediate other important antipredator behaviors, such as alarm calls and vigilance (Berkovitch et al. 1995). To understand how stress hor- mones can mediate antipredator tactics,we need tostudy the entirechain of events (stimulus → hormones → behavior), and it is especially important to establish experimentally the link between perception of predation risk and glucocorticoid hormones. The risk of starvation may serve as a stressor, either through hunger effects or through the perception of food unpredictability. Avian energy management tactics such as fat accumulation and food-caching behavior have been studied intensively (e.g., Witter and Cuthill 1993; Pravosudov and Grubb 1997). This work shows that birds accumulate more fat and cache more food when environmental conditions become unpredictable. For birds, higher fat loads increase flight costs and, importantly, reduce maneuverability, thus increasing an individual’s vulnerability to predation. Much theoretical and empirical research has studied this trade-off between the risks of starvation and predation (e.g., Lima 1986; McNamara and Houston 1990; Macleod et al. 2005). Unfortunately, the literature on fat (Box 13.1 continued) regulation in birds has paid little attention to the mechanisms regulating fattening processes. This is unfortunate, because many factors known to affect birds’ fattening decisions also affectbirds’ physiology. Unpredictable weather and limited food supplies are well known to affect levels of glu- cocorticoid hormones, which appear to strongly influence birds’ behavior (e.g., Wingfield et al. 1998). Furthermore, several studies have demon- strated that elevated corticosterone levels result in increased fat deposits and loss of protein from flight muscles (Wingfield and Silverin 1986; Sil- verin 1986; Gray et al. 1990). It seems likely that stress responses form a central part of this mechanism, and measures of corticosterone levels will undoubtedly add an important dimension to our understanding of how animals manage their energy reserves. Studies have documented a variety of effects. Limited and unpredictable food supplies affect levels of glucocorticoid hormones (Marra and Holber- ton 1998; Kitaysky et al. 1999; Pravosudov et al. 2001; Reneerkens et al. 2002). Reneerkens et al. (2002) suggested that elevated corticosterone lev- els may induce more exploratory behavior. Moderately elevated levels of glucocorticoids caused by limited and unpredictable food supplies could result in improved spatial memory and cognitive abilities(e.g., Pravosudov et al. 2001; Pfeffer et al. 2002). For example, data presented by Pravosudov and Clayton (2001) and Pravosudov et al. (2001) suggest that corticos- terone may be mediating seasonal changes in spatial memory performance in food-caching birds. It has often been suggested that high levels of stress and high levels of stress hormones have a negative effect on memory per- formance and the hippocampus (McEwen and Sapolsky 1995; McEwen 2000), but in fact not much is known about the effect of moderately el- evated levels of glucocorticoid hormones. Diamond et al. (1992) showed that, below a certain threshold, there is a positive correlation between hippocampal neuron firing rate and corticosterone concentration, and a negative correlation above that threshold. These results suggest that mod- erate elevation of baseline corticosterone may result in improved spatial memory performance. Similarly, Breuner and Wingfield (2000) showed that Gambel’s white-crowned sparrows (Zonotrichia leucophrys gambeli)in- crease their activity with moderately increased corticosterone levels, but after the concentration of corticosterone exceeds a certain threshold, activ- ity strongly decreases. In food-caching mountain chickadees (Poecile gam- beli), individuals with corticosterone implants designed to maintain moder- ately elevated corticosterone levels over more than a month demonstrated 442 Joel S. Brown and Burt P. Kotler (Box 13.1 continued) enhanced spatial memory in addition to caching and consuming more food than placebo-implanted birds (Pravosudov 2003). Thus, it appears that chronic but moderate elevations in baseline levels of glucocorticoid hor- mones might effect several important changes, such as improved cognitive abilities, increased exploratory, feeding, and food-caching behavior, and maintenance of optimal fat reserves, which all could be important adaptive responses to prevailing foraging conditions rather than “stress.” It also seems that corticosterone may be mediating cognitive tasks be- yond spatial memory. For example, greylag goslings (Anser anser)that successfully solved a novel foraging task had higher levels of fecal corticos- terone than unsuccessful goslings (Pfeffer et al. 2002). The meaning of this intriguing finding can at the moment only be speculated upon, and much work is needed to establish the role of glucocorticoid hormones in memory and cognition in particular, and the mediating role of hormones as a mech- anism within the general framework of starvation-predation trade-offs in general. Thischapter considersfear asacost offoraging,the ecologicalconsequences of animals using time allocation to ameliorate predation risk, the ecological consequences of vigilance behaviors, fear responses and population dynamics, and foraging games between clever predators and fearful prey. Throughout, the chapter combines concepts from foraging theory with concepts from population and community ecology. Its goal is to show how ideas from the study of foraging under predation risk can help us understand predator-prey interactions and the role of predators in ecological communities. 13.3 Fear and the Predation Cost of Foraging Fear as a noun describes “an unpleasant emotional state characterized by an- ticipation of pain or great distress and accompanied by heightened autonomic activity; agitated foreboding . . . of some real or specific peril.” The definition goes on to describe fear as “reasoned caution” (Webster’s Unabridged Dictionary, 3rd edition, G. & C. Merriam, 1981). Is fear merely an organism’s assessment of risk, or does it involve more? We will argue that fear combines an or- ganism’s assessment of (1) danger, (2) other benefits and costs associated with the dangerous activity or situation, and (3) the fitness loss to the organism in Foraging and the Ecology of Fear 443 the case of injury or death. We define fear as an organism’s perceived cost of injury or mortality. When foraging under predation risk, the organism can and should treat predation risk as a cost of foraging (Brown and Kotler 2004). Combat pay or hazardous duty pay in human occupations reflects an attempt to place a monetary value on risk. Similarly, animals place an energy value on predation risk. Titration experiments with ants (Nonacs and Dill 1990), tits (Todd and Cowie 1990), desert rodents (Kotler and Blaustein 1995), and fish (Abrahams and Dill 1989) all show that a higher harvest rate or food reward can coax an animal into accepting a riskier feeding situation. Several foraging models (Brown 1988, 1992;Houston et al.1993) have triangulated onthe form of this predation cost of foraging. If we define fitness as the product of a survivor’s reproductive success, F, and the probability of surviving to enjoy that success, p, then we can write the following equation for fear as a foraging cost: P = µF (∂ F/∂e ) , (13.1) where P is the predation cost of foraging (units of joules per unit time), µ is the forager’s estimate of predation risk (units of per unit time), F is survivor’s fitness (unitless as a finite growth rate), and ∂F/∂ e (units of per joule) is the marginal fitness value of energy, e. Note that p does not appear in the expression, as it cancels out (see Brown 1988, 1992). Accordingto equation(13.1), ananimal’ssense offearcan risein three ways. First, an animal should be more fearful in a risky (high µ) than a safe situation (low µ), all else being equal. Second, an animal with a lot to lose (high survivor’s fitness, F) should be more fearful than one with less to lose (Clark [1994] has referred to this phenomenon as the asset protection principle). Third, an animal that gains less from an additional unit of energy (lower marginal value of energy, ∂F/∂ e) should be more fearful than one that has muchto gain.Inhuman experience,whena well-intentionedfriendwarns you against an activity because “it’s dangerous,” this often reveals the worrier’s judgment that the activity offers a “pointless risk”: some danger with little benefit. For the ecology of fear, the predation cost of foraging has two useful properties. First, it reveals more than just predation risk. It integrates other aspects of the forager’s condition; namely, its current state or prospects (F ) and the contribution of additional energy to those prospects (∂F/∂ e). Second, it shows how food and safety behave as complementary resources in the sense that safety is valuable only if the organism has something to live for, and having excellent prospects is valuable only if the organism survives to 444 Joel S. Brown and Burt P. Kotler realize this potential. Formally, food and safety are complementary because increasing the energy state of an organism (giving it more food and increasing e) increases the marginal rate of substitution of energy for safety (increasing e probably increases F and decreases ∂F/∂ e). A species of sparrow, the dark-eyed junco, reveals these aspects of the cost of predation in its foraging behavior. Lima (1988a) fed one group of juncos and withheld food from another before releasing them to feed on a complex of artificial habitats. Consistent with the idea of predation risk as a cost of foraging, the juncos biased their feeding effort toward the safer habitat, which for these small birds lies closer to cover into which they can escape. Consistent with the complementarity of food and safety, the hungry juncos spent more time feeding in dangerous habitats away from cover. We (Brown, Kotler, and Valone 1994) estimated the size of the predation cost of foraging to desert rodents foraging for seeds. We did this by measuring the giving-updensity offree-living rodentsin standardizedexperimental food patches. Using laboratory measurements of therodents’ gain curves, we could convert giving-up densities into quitting harvest rates (joules per minute). Subtracting estimates of the metabolic cost of foraging (adjusted for ambient temperature and activity intensity) from the quitting harvest rate leaves an estimate of the predation cost of foraging. For a kangaroo rat (Dipodomys merriami) and ground squirrel (Spermophilus tereticaudus) inhabiting a creosote- bush habitat in Arizona’s Sonoran Desert, we estimated that predation costs were roughly three times higher than the metabolic costs of foraging. For two gerbil species (Gerbillus pyramidum and G. andersoni) inhabiting sand dunes in the Negev Desert, similar studies found that the costs of predation were four to five times higher than metabolic costs. While one would like to have many more studies for many more species, these studies support the idea that predation risk represents a considerable cost of foraging. The cost of predation does not necessarily have to correlate with actual mortality caused by predators (Lank and Ydenberg 2003). The predation a species experiences has already been filtered through the lens of antipredator behaviors. If cautious behavior pays big dividends in safety, then cautious animalsmay payarelativelyhigh costofpredationin lostfoodgains evenwhile experiencing little actual mortality. Brown and Alkon (1990) saw this with the Indian crested porcupine (Hystrix indica). Its spines bespeak antipredator morphology, and indeed, the porcupine is virtually impervious to predation by the leopards, wolves, hyenas, and jackals inhabiting its environment in the Negev Desert. However, measures of its foraging behavior showed that the porcupine paid a high predation cost of foraging when active on moonlit nights or in habitats free from perennial shrub cover. How can we reconcile the observation of little mortality due to predators with the observation of Foraging and the Ecology of Fear 445 Figure 13.1. The giving-up densities of porcupines (Hystrix indica) in experimental food patches set in the Negev Desert, Israel. A high giving-up density suggests a high perceived cost of predation. Food patches began with 50 chickpeas mixed into 8 liters of sifted sand. The porcupine’s perceived cost of predation increases with moonlight, and decreases with the amount of perennial shrub cover. The authors observed higher giving-up densities (shown as the mean number of chickpeas left behind in a food patch) on moonlit nights (bright) than on nights with less than a quarter moon (dark). Giving-up densities were highest in a habitat without any perennial shrub cover (BARREN), lowest in a habitat with ca. 12% shrub cover (VEG), and intermediate in the habitat immediately adjacent to the porcupine’s burrow (< 5% shrub cover, WADI). (After Brown and Alkon 1990.) a very high predation cost of foraging? Two factors probably contribute to this pattern: harassment from predators and the need for the porcupine to respond to this harassment. On moonlit nights or in open habitats, predators may easily spot porcupines. Furthermore, it may pay predators to deviate from their path and challenge encountered porcupines—an ill or otherwise incapacitated porcupine may be vulnerable. To deter the unwanted attentions of a predator, a healthy porcupine may be obliged to raise it quills and take up a defensive posture. In this way, predators represent more of a harassment cost than a mortality cost to the porcupines (fig. 13.1). In Aberderes National Park, Kenya, the black rhinoceroses suffer ha- rassment from spotted hyenas,and many exhibit missing tailsfrom suchen- counters. However, we know of only one instance in which hyenas killed a black rhinoceros. In this case (reported by a ranger in 1998), a pack of hy- enas set upon the rhino when it became mired in wet clay. Before killing the rhino, the hyenas dehorned it. These hyenas had probably never killed a rhino before. However, their experience harassing rhinos, and the rhinos’ responses to this harassment, suggest that the hyenas had ample experience with rhinos and their defensive tactics. In response to hyena harassment, rhinos perceive a lower foragingcost of predation in the more open habitatsof 446 Joel S. Brown and Burt P. Kotler the forests and glades of Aberderes. In these habitats, they have more room to maneuver. Berger and Cunningham (1994) reported that dehorning of black rhinoceroses in Namibia to discourage poaching led to attacks by hyenas on mothers and their young. The speed of the hyenas’ response suggests that the hyenas and rhinos had considerable behavioral experience with each other’s tactics. A tension exists between rhinos and large carnivores even though the carnivores almost never kill rhinos. It is unlikely thatany organism, regardless of taxon, is free from a foraging cost of predation. Even top predators experience a foraging cost of predation. They probably have two sources of predation-like costs. First, top carnivores often inflict injury or death on one another in the form of direct interference. The claws and teeth that make predators dangerous to prey also make them dangerous to one another. Examples include dragonfly larvae attacking each other, the susceptibility of venomous snakes to conspecifics’ venom, and the posturing and fighting within groups of mammalian carnivores. Great-horned owlsmay raid the nests of red-tailed hawks, and vice versa. Lions steal the captures of spotted hyenas, and spotted hyenas reciprocate by harassing or killing lone lionesses or their young. The presence of conspecifics or other predator taxa can increase the foraging costs of an individual predator. Second, prey can injure carnivores. If oblivious to injury or pain, a moun- tain lion can probably kill a North American porcupine easily. However, a muzzle or paw full of quills may incapacitate and starve a lion. Sweitzer and Berger (1992) found that mountain lions increased their consumption of porcupines during an extreme winter with deep snow. J. Laundr ´ e (personal communication) found porcupine quills embedded in several dead mountain lions retrieved during a period of low mule deer abundance. A predator faced with the risk of injury while capturing prey should add a cost of “predation” to its other hunting costs. A predator down on its luck (in a low energy state or with a high marginal value of energy) should be willing to broaden its diet to include higher-risk prey or to take on bolder hunting tactics that simultaneously increase the probabilities of success and injury. More generally, one can think of the predation costs of foraging as the opportunity costs a forager pays while trying to avoid a catastrophic loss. This catastrophic loss can emerge from the risk of mortality or injury from predators, amensals, prey, competitors, combatants, and even accidents. The giving-up density of raccoons increases with height in a tree (Lic 2001), presumably as a consequence of the greater risk of falling from increasing heights. The examples developed here show the importance and pervasiveness of the predation costs of foraging. The next step in our analysis considers how animals respond to these costs. Three classes of responses can affect the [...].. .Foraging and the Ecology of Fear organism’s ecology, the ecology of its predators, and the ecology of its own resources: time allocation, vigilance, and social behaviors The next two sections explore some of the ecological consequences of time allocation and vigilance (chap 10 deals with social foraging) 13. 4 Ecological Consequences of Time Allocation Animals should balance the conflicting demands... ecosystems (the three-trophic-level model without vigilance and with exploitative competition), top-down versus bottom-up regulation of ecosystems, and ratio-dependent models of predator-prey interactions When herbivores have effective fear responses toward their predators, exploitation ecosystems become intricate Top-down and bottom-up effects become flip sides of the same vigilance-induced direct effects... direct mortality Classic predator-prey models (Rosenzweig and MacArthur 1963) fall into this category Current interpretations of the lynx-hare cycle and weasel-vole cycle fall into the category of N-driven predator-prey systems Despite some behavioral responses, the populations of hares (Krebs et al 1995) and voles (Hanski et al 2001) rise and fall with the tide of lynx and weasels, respectively, as these... margins and gray squirrels occupy the interiors of many of the same woodlots and forests (Brown and Yeager 1945; Nixon et al 1968; Brown and Batzli 1984) It seems that gray squirrels are better at interference and exploitative competition, but are more sensitive to predators, than fox Foraging and the Ecology of Fear squirrels (Stapanian and Smith 1984; Lanham 1999; Steele and Wiegl 1992) This trade-off... (recall the lions and zebras) exerts considerable top-down control via the herbivore’s feeding rate and vigilance Remove the predators and the herbivores will overgraze, not because their population size increases (N-driven), but because each less vigilant herbivore now feeds more (µ-driven) 467 Foraging and the Ecology of Fear To an ecologist, a fear-driven system also looks like “ratio-dependent predation”—the... use and moonlight (Bouskila 1995; Mandelik et al 2003) GUDs have also been used to examine the effects of predator odors on small mammal foraging behavior (Pusenius and Ostfeld 2002; Thorson et al 1998; Herman and Valone 2000) In conjunction with patch use theory, GUDs become a concept that can be used to estimate foraging costs, measure predation risk, and link individual behaviors with population- and. .. community-level consequences (see chap 12) In behavioral studies, GUDs complement other measures of feeding behaviors such as patch residence times, giving-up times, and measures of vigilance behavior In population and community studies, GUDs complement measures of population sizes and habitat distributions In conservation biology, GUDs can provide a behavioral indicator of habitat suitability and population... 1998; Sih et al 1998) 13. 6 Fear and Population Dynamics Foragers can pay the cost of predation either by directly feeding their predators (in N-driven systems) or by changing their behavior and thereby reducing their fecundity (in µ-driven systems) Here we examine how one can incorporate fear into predator-prey dynamics and how µ-driven systems determine the shape of predator and prey isoclines (Holt... anticipate and respond to the prey’s fear responses Clever prey and clever predators produce a foraging game of fear and stealth The abilities of prey and predator to respond to each other contribute to the character and stability of the predator-prey interaction (Abrams 2000) Although relatively few studies have addressed this problem, some recent work has done so (Lima 2002) Foraging and the Ecology. .. sand and seeds every night, creating a resource that is renewed 471 472 Joel S Brown and Burt P Kotler Figure 13. 6 Density-dependent habitat selection when both predator and herbivore distribute themselves according to an ideal free distribution In both habitats, plant, herbivore, and predator population dynamics follow the three-trophic-level model with type I functional responses for herbivores and . be- tween behaviors and morphologies (coevolution), and the conservation and Foraging and the Ecology of Fear 439 management of natural areas (see chap. 14). Allthese topics fall under the ecol- ogy. population- and community-level consequences (see chap. 12). Inbehavioral studies,GUDs complement othermeasures offeed- ing behaviors such as patch residence times, giving-up times, and measures of. population dynamics, and foraging games between clever predators and fearful prey. Throughout, the chapter combines concepts from foraging theory with concepts from population and community ecology. Its