Coyote prey selection and community stability during a decline in food supply

The foraging behavior of predators can have a large influence on community dynamics and has been shown to increase stability in some cases and decrease stability in others. I studied the foraging behavior of coyotes ( Canis latrans ) in the Alaska Range during the peak and decline of a snowshoe hare ( Lepus americanus ) population cycle (1999–2002). Coyote diet was compared with prey availability to test for changes in prey selection and to examine the effect of coyote predation on the vertebrate prey community. Coyotes responded to the hare decline by increasing selection for hares and porcupines, whereas selection for voles, ground squirrels and Dall sheep did not change. Although the study area was characterized by considerable habitat heterogeneity, coyotes utilized the area as a fine-grained environment. Coyote foraging behavior was driven primarily by changes in snowshoe hare abundance, and their sensitivity to change in alternative prey density was low. Predation by coyotes may therefore decrease the stability of alternative prey populations rather than dampening fluctuations. In order for predation to enhance the stability of prey populations, I hypothesize that prey profitability must be determined primarily by abundance.     

State-dependent risk-taking by predators in systems with defended prey

Even defended prey items may contain nutrients that can sustain predators in times of energetic need. Conversely, a well-fed predator might be expected to avoid attacking prey items that have a chance of being defended, particularly if there is an abundance of familiar palatable prey to support it. To further understand the implications of optimal state-dependent foraging behaviour by predators in systems that contain defended prey, I developed a stochastic dynamic programming model. This state-dependent approach formally accounts for the trade-off between avoiding starvation and minimising harm from attacking defended prey. It predicts that the mean attack probability of predators on defended models and their undefended mimics should decline in a sigmoidal fashion with increasing availability of alternative undefended prey, and that the foraging decisions of predators should in general be relatively insensitive to the probability that a potentially defended prey item is indeed defended. Some implications of these predictions are that conspicuous warning signals are more likely to evolve in systems that contain an abundance of alternative undefended prey, and that imperfect mimicry will provide almost complete protection to the mimic when predators are readily supported by alternative food sources. Somewhat surprisingly, increasing the density of nutritious undefended mimics while keeping the densities of all other prey types constant tended to decrease the attack rates of predators on encounter with mimics and their defended models. This increase in dietary conservatism arose because in these cases there would be more prey available to sustain the predator if it ever found itself critically low in energy.     

Impacts of Foraging Facilitation Among Predators on Predator-prey Dynamics

Whereas impacts of predator interference on predator-prey dynamics have received considerable attention, the “inverse” process—foraging facilitation among predators—have not been explored yet. Here we show, via mathematical models, that impacts of foraging facilitation on predator-prey dynamics depend on the way this process is modeled. In particular, foraging facilitation destabilizes predator-prey dynamics when it affects the encounter rate between predators and prey. By contrast, it might have a stabilizing effect if the predator handling time of prey is affected. Foraging facilitation is an Allee effect mechanism among predators and we show that for many parameters, it gives rise to a demographic Allee effect or a critical predator density in need to be crossed for predators to persist. We explore also the effects of predator interference, to make the picture “symmetric” and complete. Predator interference is shown to stabilize predator-prey dynamics once its strength is not too high, and thus corroborates results of others. On the other hand, there is a wide range of model parameters for which predator interference gives rise to three co-occurring co-existence equilibria. Such a multi-equilibrial regime is rather robust as we observe it for all the functional response types we explore. This is a previously unreported phenomenon which we show cannot occur for the Beddington–DeAngelis functional response. An interesting topic for future research thus might be to seek for general conditions on predator functional responses that would produce multiple co-existence equilibria in a predator-prey model.     

Numerical and functional responses of Common Buzzards Buteo buteo to prey abundance on a Scottish grouse moor

Predators will often respond to reductions in preferred prey by switching to alternative prey resources. However, this may not apply to all alternative prey groups in patchy landscapes. We investigated the demographic and aggregative numerical and functional responses of Common Buzzards Buteo buteo in relation to variations in prey abundance on a moor managed for Red Grouse Lagopus lagopus scotica in south‐west Scotland over three consecutive breeding and non‐breeding seasons. We predicted that predation of Red Grouse by Buzzards would increase when abundance of their preferred Field Vole Microtus agrestis prey declined. As vole abundance fluctuated, Buzzards responded functionally by eating voles in relation to their abundance, but they did not respond demographically in terms of either breeding success or density. During a vole crash year, Buzzards selected a wider range of prey typical of enclosed farmland habitats found on the moorland edge but fewer Grouse from the heather moorland. During a vole peak year, prey remains suggested a linear relationship between Grouse density and the number of Grouse eaten (a Type 1 functional response), which was not evident in either intermediate or vole crash years. Buzzard foraging intensity varied between years as vole abundance fluctuated, and foraging intensity declined with increasing heather cover. Our findings did not support the prediction that predation of Red Grouse would increase when vole abundance was low. Instead, they suggest that Buzzards predated Grouse incidentally while hunting for voles, which may increase when vole abundances are high through promoting foraging in heather moorland habitats where Grouse are more numerous. Our results suggest that declines in their main prey may not result in increased predation of all alternative prey groups when predators inhabit patchy landscapes. We suggest that when investigating predator diet and impacts on prey, knowledge of all resources and habitats that are available to predators is important.     

Foraging speed in staging flocks of semipalmated sandpipers: evidence for scramble competition

Foraging speed is a key determinant of fitness affecting both foraging success and predator attack survival. In a scramble for food, for instance, evolutionary stable strategy models predict that speed should increase with competitor density and decrease when the risk of attack by predators increases. Foraging speed should also decrease in richer food patches where the level of competition is reduced. I tested these predictions in fall staging flocks of semipalmated sandpipers (Calidris pusilla) foraging for an evasive prey. Capture rate of these prey decreased with sandpiper density as the presence of competitors reduced the availability of resources for those behind. Foraging speed was evaluated indirectly by measuring the time needed to cross fixed boundaries on mudflats over 6 years. As predicted, foraging speed increased with sandpiper density and decreased with food density, but, unexpectedly, increased closer to obstructive cover where predation risk was deemed higher. When foraging closer to cover, from where predators launch surprise attacks, the increase in foraging speed may compensate for an increase in false alarms that interrupted foraging. While foraging in denser flocks decreases foraging success, joining such flocks may also increase safety against predators. In semipalmated sandpipers that occupy an intermediate position in the food chain, foraging behavior is influenced simultaneously by the evasive responses of their prey and by the risk of attack from their own predators.     

Sexual and seasonal variation in the diet and foraging behaviour of a sexually dimorphic carnivore, the honey badger (Mellivora capensis)

The honey badger, or ratel, Mellivora capensis has not been well studied despite its extensive distribution. As part of the first detailed study, visual observations of nine habituated free-living individuals (five females, four males) were used to investigate seasonal, annual and sexual differences in diet and foraging behaviour. Theory predicts that generalist predators 'switch' between alternative prey species depending on which prey species are currently most abundant, and diet breadth expands in response to decreased availability of preferred food types. There were significant seasonal differences in the consumption of eight prey categories related to changes in prey availability but no seasonal differences in food intake per kg of body mass. As predicted, the cold-dry season diet was characterized by low species richness and low foraging yield but high dietary diversity, while the reverse was true in the hot-dry and hot-wet seasons. In accordance with these predictions, results suggest that the honey badger maintains its intake level by food switching and by varying dietary breadth. Despite marked sexual size dimorphism, male and female honey badgers showed no intersexual differences in prey size, digging success, daily food intake per unit body weight or foraging behaviour. Results do not support the hypothesis that size dimorphism is primarily an adaptation to reduce intersexual competition for food.     

How does the presence of a conspecific individual change the behavioral game that a predator plays with its prey?

Behavioral games predators play among themselves may have profound effects on behavioral games predators play with their prey. We studied the behavioral game between predators and prey within the framework of social foraging among predators. We tested how conspecific interactions among predators (little egret) change the predator–prey behavioral game and foraging success. To do so, we examined foraging behavior of egrets alone and in pairs (male and female) in a specially designed aviary consisting of three equally spaced pools with identical initial prey (comet goldfish) densities. Each pool was comprised of a risky microhabitat, rich with food, and a safe microhabitat with no food, forcing the fish to trade off food and safety. When faced with two versus one egret, we found that fish significantly reduced activity in the risky habitat. Egrets in pairs suffered reduced foraging success (negative intraspecific density dependence) and responded to fish behavior and to their conspecific by changing their visiting regime at the different pools—having shorter, more frequent visits. The time egret spent on each visit allowed them to match their long-term capture success rate across the environment to their capture success rate in the pool, which satisfies one aspect of optimality. Overall, egrets in pairs allocated more time for foraging and changed their foraging tactics to focus more on fish under cover and fish ‘peeping’ out from their shelter. These results suggest that both prey and predator show behavioral flexibility and can adjust to changing conditions as needed in this foraging game.     

Foraging behavior of an estuarine predator, the blue crab Callinectes sapidus in a patchy environment

To define general principles of predator‐prey dynamics in an estuarine subtidal environment, we manipulated predator density (the blue crab, Callinectes sapidus) and prey (the clam, Macoma balthica) patch distribution in large field enclosures in the Rhode River subestuary of the central Chesapeake Bay. The primary objectives were to determine whether predators forage in a way that maximizes prey consumption and to assess how their foraging success is affected by density of conspecifics. We developed a novel ultrasonic telemetry system to observe behavior of individual predators with unprecedented detail. Behavior of predators was more indicative of optimal than of opportunistic foraging. Predators appeared responsive to the overall quality of prey in their habitat. Rather than remaining on a prey patch until depletion, predators appeared to vary their patch use with quality of the surrounding environment. When multiple (two) prey patches were available, residence time of predators on a prey patch was shorter than when only a single prey patch was available. Predators seemed to move among the prey patches fairly regularly, dividing their foraging time between the patches and consuming prey from each of them at a similar rate. That predators more than doubled their consumption of prey when we doubled the number of prey (by adding the second patch) is consistent with optimizing behaviors ‐ rather than with an opportunistic increase in prey consumption brought about simply by the addition of more prey. Predators at high density, however, appeared to interfere with each other's foraging success, reflected by their lower rates of prey consumption. Blue crabs appear to forage more successfully (and their prey to experience higher mortality) in prey patches located within 15–20 meters of neighboring patch, than in isolated patches. Our results are likely to apply, at least qualitatively, to other crustacean‐bivalve interactions, including those of commercial interest; their quantitative applicability will depend on the mobility of other predators and the scale of patchiness they perceive.     

Effects of prey refuges on a predator-prey model with a class of functional responses: The role of refuges

In this paper, the effects of refuges used by prey on a predator-prey interaction with a class of functional responses are studied by using the analytical approach. The refuges are considered as two types: a constant proportion of prey and a fixed number of prey using refuges. We will evaluate the effects with regard to the local stability of the interior equilibrium point, the values of the equilibrium density and the long-term dynamics of the interacting populations. The results show that the effects of refuges used by prey increase the equilibrium density of prey population while decrease that of predators. It is also proved that the effects of refuges can stabilize the interior equilibrium point of the considered model, and destabilize it under a very restricted set of conditions which is disagreement with previous results in this field.     

Non-lethal effects of predators on prey growth rates depend on prey density and nutrient additions

A number of studies show that predators can depress prey growth rates by inducing reductions in foraging activity, but the size of this non-lethal effect is quite variable. Here I investigate how prey density and resource productivity may alter the extent to which predators depress the growth rates of their prey. Theory predicts that when resources are overgrazed, an increase in predation risk will have little net effect on individual food intake because the decline in foraging effort will be offset by an increase in resource level. Thus, the non-lethal effects of predators on prey growth rates should depend upon prey density and resource productivity in a predictable manner, with the growth penalty imposed by predators being strongest when resources are undergrazed and weakest when resources are overgrazed. I tested this hypothesis by manipulating predation risk, prey density, and nutrient additions in a mesocosm experiment with the pulmonate snail Helisoma trivolvis . Refuge use by snails was 45% higher in the presence of caged crayfish than in their absence. Snail growth rates were reduced, on average, by 24% in the presence of caged crayfish. However, the magnitude of the growth penalty exacted by crayfish depended on snail density and nutrient additions. When snails were stocked at high density and nutrient additions were low, growth suppression was just 2.6%. At the other extreme, when snails were at low density and nutrient additions were high, growth suppression was 44.6%. Thus, the non-lethal effects of predators on prey growth depend on environmental context, illustrating an important link between individual traits and system-level properties.     

Grape powdery mildew as a food source for generalist predatory mites occurring in vineyards: effects on life-history traits

In several perennial cropping systems, generalist or omnivorous species represent important biocontrol agents. They can persist on plants by feeding on alternative foods when prey is scarce and potentially limit pest outbreaks. Among beneficials characterised by a wide food range, those belonging to the acarine family Phytoseiidae represent important biocontrol agents. Generalist predatory mites can develop and reproduce using various food sources as alternatives to their tetranychid prey. The presence of alternative food sources can also induce switching feeding behaviour of generalist predators from prey to alternative foods. We evaluated in the laboratory the role of the grape powdery mildew (GPM) for the survival, development and reproduction of Amblyseius andersoni and Typhlodromus pyri , two important beneficial phytoseiid mites, in European and North-American vineyards. We also compared life-history parameters obtained when feeding on GPM with those obtained feeding on tetranychids mite prey or cattail pollen. Results indicated that GPM is an adequate food source for generalist mite survival and development. Results suggest that GPM can sustain mite populations in the absence of higher quality food sources. Based on optimal foraging theory, comparison of life-history parameters on GPM and mite prey suggests that the disruption of phytophagous mite control by these predatory mites in the presence of GPM appears unlikely. Implications for biological control in vineyards are discussed.     

Incidental predation, enemy-free space and the coexistence of incidental prey

Many communities consist of a generalist predator that consumes multiple prey species whose persistence is thereby threatened through the indirect effect of apparent competition. However, uncommon and/or ephemeral prey may be encountered only incidentally through the predator's effort expended to consume primary prey. In such instances, the functional response to incidental prey is driven entirely through the density of primary prey. Moreover, rarity and brevity in the predator's diet precludes a numerical response to incidental prey. Instead, the persistence of incidental prey may be critically linked to gaps in space unexploited by predators, i.e. enemy-free space. I use optimal foraging theory to derive a mechanism by which enemy-free space is created as a result of a predator's forging aptitude and patch-use behavior. In non-competitive environments enemy-free space provides a behavioral refuge for incidental prey that may prevent their extinction. In competitive environments, greater enemy-free space is associated with higher incidental prey densities and concomitantly greater competitive effects. As a result, incidental prey diversity declines with an increase in enemy-free space.     

Foraging activity of a dominant epigeal predator: molecular evidence for the effect of prey density on consumption

Despite the widely held assumption that ‘generalist’ predators consume most prey available to them, there is a growing body of evidence suggesting otherwise. Generalists are expected to perform well in disturbed areas because they can switch between prey pathways when one food source becomes depleted. Indeed, these predators have the potential to promote diversity by switching to prey in a frequency dependent manner and consume prey groups in relation to local abundance. It is therefore important to understand how predation rates fluctuate as local availability changes. We performed open‐field and mesocosm experiments in a corn and soybean agroecosystem to delineate the role prey density plays in determining predation frequency of a dominant epigeal predator. To track trophic pathways, molecular gut‐content analysis using enzyme‐linked immunosorbent assay (ELISA) was performed to track foraging behavior of the wolf spider Pardosa milvina feeding on dipterans, flies. Extensive monitoring of foraging activity and prey populations revealed that predation varied temporally. Importantly, the frequency of individuals testing positive for flies was lower than predicted when flies were extremely abundant but higher when they were scarce, relative to the prey community as a whole. Furthermore, isolating predators in mesocosms revealed an effect of Diptera density on the likelihood of consumption, as determined by ELISA, only when flies were at low levels (12.5% of prey provided). The molecular results suggest that these spiders do not appear to be consuming flies in a frequency‐dependent manner where the decision to switch between different prey pathways is driven by relative abundance. Rather, selectivity of prey is somewhat independent of variation of other prey groups, which is indicative of their consistent reliance on dipterans and may be related to nutritional requirements and/or capture success.     

Natural selection and population density-feedback II. The evolution of functional response curves

The nature of the functional response may be qualitatively understood as follows. Sigmoid responses to one food type may arise, in the presence of alternate foods, as a result of optimal feeding and foraging behavior. Sigmoid curves resulting from this cause I term class A curves. The same curve may also arise in the absence of alternate foods as a result of learning, individual variations in the level of food density at which predators begin feeding, or training effects. The latter I have termed class B curves. At very high food densities, a drop in food intake per predator might occur because of the tendency for predators to take easily found and captured items first and to become more selective when food is very common. Such “dome-shaped” curves have been found in the laboratory but should be rare in nature. Computer simulation of a three trophic-level system, using the phenotypic selection model of Emlen, indicates that natural selection acting on prey should encourage sigmoidality in the predator's class B functional response, at least in disturbed environments. The opposite force arises from selection acting on predators. However, given the magnitudes of growth efficiencies (see Eq. (8), it appears that at least for terrestrial vertebrates, selection on prey species is more important than selection on predators for determining functional responses. Accordingly, prey-predator systems occupying highly variable environments are expected to show more marked type III (class B) curves than systems in more stable areas. Finally, the role of functional response for prey-predator stability is discussed. Class A (alternate food) responses may result in population control for prey in multiple prey systems. Peterman and Pikitch have modeled systems in which type III functional response by predators, in systems where predation varies independently of prey, may lead to double equilibria. This picture is clouded, however, when predator populations are interactive with their food, though double equilibria are still possible (J. M. Emlen, 1984, “Population Biology: The Coevolution of Population Dynamics and Behavior,” Macmillan, New York, in press).     

Prediction of Switching and Counter-Switching Based on Optimal Foraging

It is shown that optimally foraging predators can switch or counter-switch depending on prey types and on environmental conditions, due to changes in the profitability of the prey types involved. Subsequently rules are developed to predict switching or counter-switching by the predator when prey densities change, using examples from the literature as well as new data on prey selection in sticklebacks.     

Responses of Australian wading birds to a novel toxic prey type, the invasive cane toad Rhinella marina

The impact of invasive predators on native prey has attracted considerable scientific attention, whereas the reverse situation (invasive species being eaten by native predators) has been less frequently studied. Such interactions might affect invasion success; an invader that is readily consumed by native species may be less likely to flourish in its new range than one that is ignored by those taxa. Invasive cane toads (Rhinella marina) in Australia have fatally poisoned many native predators (e.g., marsupials, crocodiles, lizards) that attempt to ingest the toxic anurans, but birds are more resistant to toad toxins. We quantified prey preferences of four species of wading birds (Nankeen night heron, purple swamphen, pied heron, little egret) in the wild, by offering cane toads and alternative native prey items (total of 279 trays offered, 14 different combinations of prey types). All bird species tested preferred the native prey, avoiding both tadpole and metamorph cane toads. Avoidance of toads was strong enough to reduce foraging on native prey presented in combination with the toads, suggesting that the presence of cane toads could affect predator foraging tactics, and reduce the intensity of predation on native prey species found in association with toads.     

How predator functional responses and Allee effects in prey affect the paradox of enrichment and population collapses

In Rosenzweig-MacArthur models of predator-prey dynamics, Allee effects in prey usually destabilize interior equilibria and can suppress or enhance limit cycles typical of the paradox of enrichment. We re-evaluate these conclusions through a complete classification of a wide range of Allee effects in prey and predator's functional response shapes. We show that abrupt and deterministic system collapses not preceded by fluctuating predator-prey dynamics occur for sufficiently steep type III functional responses and strong Allee effects (with unstable lower equilibrium in prey dynamics). This phenomenon arises as type III functional responses greatly reduce cyclic dynamics and strong Allee effects promote deterministic collapses. These collapses occur with decreasing predator mortality and/or increasing susceptibility of the prey to fall below the threshold Allee density (e.g. due to increased carrying capacity or the Allee threshold itself). On the other hand, weak Allee effects (without unstable equilibrium in prey dynamics) enlarge the range of carrying capacities for which the cycles occur if predators exhibit decelerating functional responses. We discuss the results in the light of conservation strategies, eradication of alien species, and successful introduction of biocontrol agents.     

Multiple stable equilibria in a predator-prey system

Necessary and sufficient conditions are given for three equilibria to occur in a predatorprey model and conditions are given for two of these to be stable. The existence of two stable equilibria requires predator intraspecific competition for either space or food, and the lower the prey growth rate the stronger this predator self-regulation must be. A prey growth rate that is skewed to the right, the ability of a few predators to survive at low prey densities, and predators with high searching effectiveness, long handling times, and large maximum per capita rate of increase all make two stable equilibria more likely.     

Potential of an alternative prey to disrupt predation of the generalist predator, Orius insidiosus, on the pest aphid, Aphis glycines, via short-term indirect interactions

Generalist insect predators can significantly impact the dynamics of pest populations; and, using alternative prey, they can rapidly establish in disturbed agroecosystems. However, indirect interactions between prey can occur, leading to either increased or decreased predation on focal prey. The present paper demonstrates how alternative prey can disrupt predation by the hemipteran Orius insidiosus on the soybean aphid Aphis glycines via short-term indirect interactions. We used laboratory microcosms to measure the impact of the predator on the population growth of the aphid in the presence of alternative prey, soybean thrips Neohydatothrips variabilis, and we characterized the foraging behaviour of the predator to assess prey preference. We showed that O. insidiosus predation on aphids was reduced in the presence of thrips and that this positive impact on aphids increased as thrips density increased. Results from the behavioural experiment support the hypothesis of a prey preference toward thrips. When prey-pest ratio is aphid-biased, short-term apparent commensalism between prey occurs in favour of the most abundant prey (aphids) with no switching behaviour appearing in O. insidiosus. These results demonstrate that potential indirect interactions should be taken into account when considering O. insidiosus as a biocontrol agent against the soybean aphid.