Feeding rate and attack specialization: the roles of predator experience and energetic tradeoffs

Synopsis Individual mosquitofish, Gambusia affinis, can adopt a broad range of attack selectivities. In part, this variation can be explained by the past experiences of a fish. Individuals selected the more profitable Ceriodaphnia dubia (Cladocera) over less profitable cyclopoid copepods to a greater degree after being exposed to both prey types than did individuals experienced with only one of the prey types. Feeding rate (biomass ingested per unit time) declined with increased attack specialization on the profitable prey (Ceriodaphnia) when such prey were scarce, a result in agreement with assumptions of optimal diet theory. When profitable prey were abundant feeding rate was a bimodal function of the intensity of specialization on profitable prey; fish that specialized on cyclopoid copepods (the less profitable prey type) fed at higher rates than did generalists. This may be the result of antagonistic learning that precluded feeding efficiently on more than one type of prey at a time. The data are consistent with the hypothesis that rejection of unsuitable prey involves a time cost. The two preceeding aspects of foraging behavior, which are absent from most optimal diet models, could lead to failure in predicting the attack specialization of some predators, An additional aspect of the results was the generally weak relationship between feeding efficiency and specialization behavior. This suggests that feeding rate may not have been as tightly linked to the specialization behavior a predator adopts as is assumed by current foraging theory.     

Prey selection by thaidid gastropods: some observational and experimental field tests of foraging models

Summary Field observations and experiments revealed that predatory intertidal gastropods of the genus Thais (or Nucella) were able both to recognize the expected food value of encountered prey (expected energy or growth potential gained per unit handling time) and to monitor their average yield over time (average energy or growth potential gained per unit foraging time). They appeared to discriminate not only among prey species, but also among different sized individuals of the same prey species. The evidence supporting these interpretations included: 1) field observations of snails feeding preferentially on prey types of higher expected food value even though lower value prey types were available and abundant, 2) a very limited number of direct underwater observations of foraging snails rejecting encountered items that were either of lower expected value than the item finally eaten or not measurably different from it, and 3) field (=arena) experiments in which both average yield, and the distribution and abundance of potential prey were controlled: snails conditioned at a high average yield fed preferentially on high value items, while those animals conditioned at a low yield consumed prey in the proportions that they were encountered. These behaviors are all consistent with a prey-selection decision motivated by energetic considerations. Further, the field experiments indicated that these predatory gastropods could select items from a diverse array of prey so as to maximize growth in their natural environment. The behaviors were not consistent with three alternative foraging hypotheses: non-selective foraging, frequency-dependent foraging on prey types (here, sizes of particular prey species), and frequency-dependent foraging on prey species. Deviations from some of the quantitative predictions of optimal foraging theory appeared related to learning and risk.     

Effects of Individual and Group Characteristics on Feeding Behaviors in Wild Leontopithecus rosalia

Studies have linked variation in feeding and foraging success to variation in survival and reproductive success, which makes exploring influences on feeding invaluable. In the current study, we quantified energy contents of foods consumed by wild golden lion tamarins (Leontopithecus rosalia, GLT) and feeding behaviors of 34 GLT from March 1998 to March 1999. Our objective was to test predictions regarding effects of characteristics of the 1) individual, 2) group, 3) environment, and 4) other behaviors on 3 feeding behaviors: feeding on plant matter, searching for prey, and feeding on prey. We hypothesized that environmental characteristics, e.g., resource availability, in addition to group characteristics e.g., group size, would influence feeding on plant matter, because several individuals in a group often consume fruit in the same fruit tree. We hypothesized that environmental characteristics and individual characteristics, e.g., age, would influence searching for and consuming prey because the individual often searches for and consumes prey while it is alone at a substrate. We used SAS mixed models to determine the relative influence of these characteristics on the feeding behaviors. We found that group characteristics more significantly influenced feeding on plant matter, while individual characteristics more significantly influenced searching for prey. The results emphasize the distinctly different influences of individual and group characteristics on feeding. That influences other than competition may affect feeding on plant matter warrants further exploration.     

Lyapunov functions for Lotka–Volterra predator–prey models with optimal foraging behavior

 The theory of optimal foraging predicts abrupt changes in consumer behavior which lead to discontinuities in the functional response. Therefore population dynamical models with optimal foraging behavior can be appropriately described by differential equations with discontinuous right-hand sides. In this paper we analyze the behavior of three different Lotka–Volterra predator–prey systems with optimal foraging behavior. We examine a predator–prey model with alternative food, a two-patch model with mobile predators and resident prey, and a two-patch model with both predators and prey mobile. We show that in the studied examples, optimal foraging behavior changes the neutral stability intrinsic to Lotka–Volterra systems to the existence of a bounded global attractor. The analysis is based on the construction and use of appropriate Lyapunov functions for models described by discontinuous differential equations. Received: 23 March 1999     

The effects of interspecific competition and prey odor on foraging behavior in the rock crab, Cancer irroratus (Say)

The effects of competitor pressure and prey odor on foraging behavior of the rock crab, Cancer irroratus (Say), were investigated. The Jonah crab, Cancer borealis (Stimpson), was chosen as the interspecific competitor because it shares resources with C. irroratus. Four treatments were tested for their effect on foraging: the presence or absence of a competitor and two types of prey odor; body odor (living mussel) and tissue extract (dead mussel tissue). The presence of Jonah crabs did not influence location time, search time, prey size selected, or handling time of the rock crabs. However, rock crabs responded differently to the presence of body odor and tissue extract cues. The presence of extract odor decreased the time to locate prey while increasing the number of prey manipulated and prey size selected. When prey body odor was present, rock crabs displayed less investigative behaviors than in the presence of extract odor, illustrated by reduced location time. Extract odor provided a stronger and more attractive cue than body odor, but increased prey manipulation and search time. Extract odor induced increases in manipulation and searching for prey but canceled out the benefits of decreased location time, resulting in crabs from both treatments displaying similar search times. These elevated behaviors may be associated with foraging for injured and cracked prey or may indicate an area of conspecific feeding.     

Effects of Individual and Group Characteristics on Feeding Behaviors in Wild <Emphasis Type="Italic">Leontopithecus rosalia</Emphasis>

Studies have linked variation in feeding and foraging success to variation in survival and reproductive success, which makes exploring influences on feeding invaluable. In the current study, we quantified energy contents of foods consumed by wild golden lion tamarins (Leontopithecus rosalia, GLT) and feeding behaviors of 34 GLT from March 1998 to March 1999. Our objective was to test predictions regarding effects of characteristics of the 1) individual, 2) group, 3) environment, and 4) other behaviors on 3 feeding behaviors: feeding on plant matter, searching for prey, and feeding on prey. We hypothesized that environmental characteristics, e.g., resource availability, in addition to group characteristics e.g., group size, would influence feeding on plant matter, because several individuals in a group often consume fruit in the same fruit tree. We hypothesized that environmental characteristics and individual characteristics, e.g., age, would influence searching for and consuming prey because the individual often searches for and consumes prey while it is alone at a substrate. We used SAS mixed models to determine the relative influence of these characteristics on the feeding behaviors. We found that group characteristics more significantly influenced feeding on plant matter, while individual characteristics more significantly influenced searching for prey. The results emphasize the distinctly different influences of individual and group characteristics on feeding. That influences other than competition may affect feeding on plant matter warrants further exploration. An erratum to this article can be found at     

Effect of spatial heterogeneity on the role of Coccinella septempunctata as an intra-guild predator of the aphid pathogen Pandora neoaphidis

The foraging behavior of starved and non-starved adult and larval Coccinella septempunctata on groups of plants in the presence of Pandora neoaphidis-infected Acyrthosiphon pisum, uninfected aphids or a mixture of these two prey types was compared. In general results of these studies confirmed the results of previous work comparing foraging behavior on a smaller spatial scale in Petri dishes. However, behaviors were modified in response to spatial complexity, prey quality, and the host plant. Starved C. septempunctata adults and larvae fed for longer and consumed more aphids than non-starved coccinellids. Both larvae and adults fed on infected aphids and in some cases entirely consumed them. This was thought to be due to the ease of capture of infected (dead) aphids and the feeding stimuli provided by the presence of the host plant and, where there was a choice of prey, uninfected aphids in the environment. Both larvae and adults spent the majority of the time foraging in the upper regions of plants and visited more plants when they were not starved or when they were in the presence of less suitable, infected aphid prey.     

Optimal foraging and feeding mode shifts in fishes

Synopsis Most optimal foraging models for fishes are based on particulate feeding behavior. But many obligate planktivores also filter zooplankton. I suggest that feeding mode shifts (e.g. from particulate feeding to filtering) may be predictable from the costs and benefits of foraging in various modes. Quantitative examples of feeding mode shifts in three species of fishes (northern anchovy, pacific mackerel and alewife) from 3 different families support this hypothesis. Feeding mode shifts seem to depend on relative profitability of each mode, but improvements in model predictions will need to include the effects of spatial and temporal patchiness on encounter rates of prey of various sizes.     

A stochastic foraging model with predator training effects. II. Optimal diets

Standard optimal diet models require that a predator's behavior while searching for food does not change in response to experiences with individual prey. There is evidence for rapid and reversible changes in feeding behavior caused by as few as one or two prey encounters. When these “training effects” occur, a given prey type is more likely to be captured next if it was the last type with which the predator had experience. This is not compatible with the standard foraging model. I present a stochastic model which incorporates predator training effects, and three types of training are explored: training in the ability to detect prey (search image formation), training in the probability of succeeding in an attempted capture, and training in the time to pursue, capture, and eat prey. The main result is that all three types of training can result in optimal diets which do not obey the standard optimal diet rules. Conditions under which these rules will suffice are discussed.     

Individual specialization in diet by a generalist marine predator reflects specialization in foraging behaviour

1. We studied chick diet in a known-age, sexed population of a long-lived seabird, the Brünnich's guillemot (Uria lomvia), over 15 years (N = 136; 1993-2007) and attached time-depth-temperature recorders to examine foraging behaviour in multiple years (N = 36; 2004-07). 2. Adults showed specialization in prey fed to offspring, described by multiple indices calculated over 15 years: 27% of diet diversity was attributable to among-individual variation (within-individual component of total niche width = 0.73); average similarity of an individual's diet to the overall diet was 65% (mean proportional similarity between individuals and population = 0.65); diet was significantly more specialized than expected for 70% of individuals (mean likelihood = 0.53). These indices suggest higher specialization than the average for an across-taxa comparison of 49 taxa. 3. Foraging behaviour varied along three axes: flight time, dive depth and dive shape. Individuals showed specialized individual foraging behaviour along each axis. These foraging strategies were reflected in the prey type delivered to their offspring and were maintained over scales of hours to years. 4. Specialization in foraging behaviour and diet was greater over short time spans (hours, days) than over long time spans (years). Regardless of sex or age, the main component of variation in foraging behaviour and chick diet was between individuals. 5. Plasma stable isotope values were similar across years, within a given individual, and variance was low relative to that expected from prey isotope values, suggesting adult diet specialized across years. Stable isotope values were similar among individuals that fed their nestlings similar prey items and there was no difference in trophic level between adults and chicks. We suggest that guillemots specialize on a single foraging strategy regardless of whether chick-provisioning and self-feeding. With little individual difference in body mass and physiology, specialization likely represents learning and memorizing optimal feeding locations and behaviours. 6. There was no difference in survival or reproductive success between specialists and generalists, suggesting these are largely equivalent strategies in terms of evolutionary fitness, presumably because different strategies were advantageous at different levels of prey abundance or predictability. The development of individual specialization may be an important precursor to diversification among seabirds.     

Prey capture and selection throughout the breeding season in a deep‐diving generalist seabird,the thick‐billed murre

Generalist seabirds forage on a variety of prey items providing the opportunity to monitor diverse aquatic fauna simultaneously. For example, the coupling of prey consumption rates and movement patterns of generalist seabirds might be used to create three‐dimensional prey distribution maps (‘preyscapes’) for multiple prey species in the same region. However, the complex interaction between generalist seabird foraging behaviour and the various prey types clouds the interpretation of such preyscapes, and the mechanisms underlying prey selection need to be understood before such an application can be realized. Central place foraging theory provides a theoretical model for understanding such selectivity by predicting that larger prey items should be 1) selected farther from the colony and 2) for chick‐feeding compared with self‐feeding, but these predictions remain untested on most seabird species. Furthermore, rarely do we know how foraging features such as handling time, capture methods or choice of foraging location varies among prey types. We used three types of animal‐borne biologgers (camera loggers, GPS and depth‐loggers) to examine how a generalist Arctic seabird, the thick‐billed murre Uria lomvia, selects and captures their prey throughout the breeding season. Murres captured small prey at all phases of a dive, including while descending and ascending, but captured large fish mostly while ascending, with considerably longer handling times. Birds captured larger prey and dove deeper during chick‐rearing. As central place foraging theory predicted, birds travelling further also brought bigger prey items for their chick. The location of a dive (distance from colony and distance to shore) best explained which prey type was the most likely to get caught in a dive, and we created a preyscape surrounding our study colony. We discuss how these findings might aid the use of generalist seabirds as bioindicators.     

Solitary Floral Specialists Do Not Respond to Cryptic Flower-Occupying Predators

The impacts of predators on bee foraging behavior are varied, but have been suggested to depend on both the type of predator (namely their hunting strategy) and also risk assessment by the prey (i.e., ability to perceive predators and learn to avoid them). However, nearly all studies have explored these impacts using social bees, despite the fact that solitary bees are extremely diverse, often specialized in their floral interactions, and may exhibit different behaviors in response to flower-occupying predators. In this study, we examined foraging behaviors of wild solitary long-horned bees (Melissodes spp.) in response to a cryptic predator, the ambush bug (Phymata americana) on the bees’ primary floral host, the prairie sunflower (Helianthus petiolaris). We found sex-specific differences in foraging behaviors of bees, but little evidence that ambush bugs affected either pre-landing or post-landing foraging behaviors. Male bees visited flowers three times more often than females but female bees were five times more likely to land than males. Ambush bugs did not reduce visitation in either sex. Spectral analysis through a bee vision model indicated that ambush bug dorsal coloration was indistinguishable from the disc flowers of sunflowers, suggesting that ambush bugs are indeed cryptic and likely rarely detected by solitary bees. We discuss the implications of these findings for the perceived risk of predation in solitary bees and compare them to other studies of social bees.     

Meal Size Effects on Antipredator Behavior of Hatchling Trinket Snakes, Elaphe helena

Current foraging models limit the decision‐making process of animals to the food searching and consuming phase. The post‐consummatory phase of feeding may influence optimal meal size for some species as a morphologic change often results from feeding. In snakes, a single prey item can lead to abrupt increases in body mass, thus influencing locomotor performance. Identifying factors affecting locomotor performance can help predict behaviors that should maximize an animal's chance of evading predators. Although many snakes ingest large percentages of their body mass, not much work has examined the post‐consummatory effects of ingesting bulky prey differing in relative mass. I examined the locomotor performance and antipredator tactics of hatchling trinket snakes (Elaphe helena) after subjecting snakes to mice prey varying by relative mass differences of 20–35%, 50–59% or 70–79% of an individual hatchling's body mass. Snakes in treatment groups were compared with snakes in a control group (0%). Meal size‐affected locomotor parameters such as burst speed, endurance, and endurance times for hatchlings that ingested 50–59% and 70–79% of their body mass (p < 0.001). Recent feeding also affected the types of antipredator modes employed. Hatchlings in the 0% and 20–35% treatments exhibited behaviors that were categorized as active and threatening, while hatchlings in the 50–59% and 70–79% treatments exhibited stationary, neutral, and cryptic behaviors. Although snakes may become more reclusive following a meal, this study demonstrates that relative prey mass affects the ability of hatchling trinket snakes to flee from a predator. In turn, these results suggest that the post‐consummatory effects of foraging should be considered in optimal foraging models for organisms that consume a substantial portion of their body mass during a single feeding.     

Morphological and functional bases of durophagy in the queen triggerfish,Balistes vetula (Pisces,tetraodontiformes)

Tetraodontiform fishes are characterized by jaws specialized for powerful biting and a diet dominated by hard-shelled prey. Strong biting by the oral jaws is an unusual feature among teleosts. We present a functional morphological analysis of the feeding mechanism of a representative tetraodontiform, Balistes vetula. As is typical for the order, long, sharp, strong teeth are mounted on the short, robust jaw bones of B. vetula. The neurocranium and suspensorium are enlarged and strengthened to serve as sites of attachment for the greatly hypertrophied adductor mandibulae muscles. Electromyographic recordings made from 11 cranial muscles during feeding revealed four distinct behaviors in the feeding repertoire of B. vetula. Suction is used effectively to capture soft prey and is associated with a motor pattern similar to that reported for many other teleosts. However, when feeding on hard prey, B. vetula directly bit the prey, exhibiting a motor pattern very different from that of suction feeding. During buccal manipulation, repeated cycles of jaw opening and closing (biting) were coupled with rapid movement of the prey in and out of the mouth. Muscle activity during buccal manipulation was similar to that seen during bite-captures. A blowing behavior was periodically employed during prey handling, as prey were forcefully “spit out” from the mouth, either to reposition them or to separate unwanted material from flesh. The motor pattern used during blowing was distinct from similar behaviors described for other fishes, indicating that this behaviors may be unique to tetraodontiforms. Thus B. vetula combines primitive behaviors and motor patterns (suction feeding and buccal manipulation) with specialized morphology (strong teeth, robust jaws, and hypertrophied adductor muscles) and a novel behavior (blowing) to exploit armored prey such as sea urchins molluscs, and crabs. © 1993 Wiley-Liss, Inc.     

Indirect risk effects reduce feeding efficiency of ducks during spring

Indirect risk effects of predators on prey behavior can have more of an impact on prey populations than direct consumptive effects. Predation risk can elicit more vigilance behavior in prey, reducing the amount of time available for other activities, such as foraging, which could potentially reduce foraging efficiency. Understanding the conditions associated with predation risk and the specific effects predation risk have on prey behavior is important because it has direct influences on the profitability of food items found under various conditions and states of the forager. The goals of this study were to assess how ducks perceived predation risk in various habitat types and how strongly perceived risk versus energetic demand affected foraging behavior. We manipulated food abundance in different wetland types in Illinois, USA to reduce confounding between food abundance and vegetation structure. We conducted focal‐animal behavioral samples on five duck species in treatment and control plots and used generalized linear mixed‐effects models to compare the effects of vegetation structure versus other factors on the intensity with which ducks fed and the duration of feeding stints. Mallards fed more intensively and, along with blue‐winged teal, used longer feeding stints in open habitats, consistent with the hypothesis that limited visibility was perceived to have a greater predation risk than unlimited visibility. The species temporally nearest to nesting, wood ducks, were willing to take more risks for a greater food reward, consistent with an increase in a marginal value of energy as they approached nesting. Our results indicate that some duck species value energy differently based on the surrounding vegetation structure and density. Furthermore, increases in the marginal value of energy can be more influential than perceived risk in shaping foraging behavior patterns. Based on these findings, we conclude that the value of various food items is not solely determined by energy contained in the item but by conditions in which it is found and the state of the forager.     

Study on foraging mechanism of leeches with different feeding habits based on chemoreception and foraging behavior

The leeches Whitmania pigra and Hirudo nipponia live in similar environments but have different feeding habits. At present, there are few studies of the foraging mechanism of leeches with different feeding habits. In this study, we first used maze tests to show that these two species of leeches could locate and distinguish their prey through chemosensory activity without mechanical stimulation. However, the two leech species have different foraging behaviors: Individuals of W. pigra move slowly and repeatedly adjust direction through probing and crawling to detect the location of prey (snails), whereas individuals of H. nipponia move quickly, and after determining the location of food (porcine blood), they quickly swim or crawl to the vicinity of their prey. Scanning electron microscopy (SEM) revealed that there are two types of sensory cilia and pore structures related to mucus secretion in the heads of both leeches. There are two differently sized types of chemoreceptors on the dorsal lip in W. pigra, which may have different functions during foraging, whereas in H. nipponia there is only one type of chemoreceptor, which is small. We detected the chemical components in the natural food of these two leech species by UHPLC–MS. There were 934 metabolites in the body fluid of snails and 751 metabolites in porcine serum; five metabolites unique to the body fluid of snails and to porcine serum were screened as candidate feeding attractants. Of these metabolites, betaine and arginine effectively attracted individuals of W. pigra and H. nipponia, respectively. In summary, leeches with different feeding habits use chemoreceptors to sense external chemical signals when foraging, and there are significant differences between species in foraging behavior, chemoreceptors, and attractants.     

Rorqual whale (Balaenopteridae) surface lunge‐feeding behaviors: Standardized classification,repertoire diversity,and evolutionary analyses

Rorqual whales (Family: Balaenopteridae) are the world's largest predators and sometimes feed near or at the sea surface on small schooling prey. Most rorquals capture prey using a behavioral process known as lunge‐feeding that, when occurring at the surface, often exposes the mouth and head above the water. New technology has recently improved historical misconceptions about the natural variation in rorqual lunge‐feeding behavior yet missing from the literature is a dedicated study of the identification, use, and evolution of these behaviors when used to capture prey at the surface. Here we present results from a long‐term investigation of three rorqual whale species (minke whale, Balaenoptera acutorostrata; fin whale, B. physalus; and blue whale, B. musculus) that helped us develop a standardized classification system of surface lunge‐feeding (SLF) behaviors. We then tested for differences in frequency of these behaviors among the three species and across all rorqual species. Our results: (1) propose a unified classification system of six homologous SLF behaviors used by all living rorqual whale species; (2) demonstrate statistically significant differences in the frequency of each behavior by minke, fin, and blue whales; and (3) provide new information regarding the evolution of lunge‐feeding behaviors among rorqual whales.     

Variation in foraging behavior facilitates resource partitioning in a polymorphic cichlid, Herichthys minckleyi

We examined foraging behavior (microhabitat use and feeding behavior) in a trophically polymorphic cichlid fish, Herichthys minckleyi, to address several questions regarding resource partitioning in this threatened species. These include: (1) do morphotypes demonstrate different foraging behaviors? (2) do individuals within a morphotype vary in their foraging behavior (e.g. are some individuals specialists, only using a subset of available resources, while other are generalists)? (3) do foraging behaviors vary between isolated pools? (4) do foraging behaviors vary across seasons? We quantified microhabitat use and feeding behavior for over 100 individuals (of two morphotypes) feeding freely in two isolated pools (populations) and across two seasons (winter and summer). We found differences in foraging behavior between morphotypes and individual specializations within morphotypes; i.e. some individuals specialize on certain food resources by using a few feeding behaviors within a subset of microhabitats, whereas others employ a range feeding behaviors across many microhabitats. Foraging behavior also varied between pools and across seasons. This spatial and temporal variation in foraging behavior and resource use may serve to maintain this polymorphism, as the relative fitness of the each morph may vary over space and time.     

Foraging Decision Rules and Prey Species Preferences of Northwestern Crows (Corvus caurinus)

Categorization of similar prey types and the application of decision rules by dietary generalists can enhance the efficiency of foraging decisions and facilitate the inclusion of novel prey types in the diet. While considerable research attention has been directed toward investigation of these concepts in invertebrates, few have assessed categorization and decision rules used by generalist vertebrate predators. In this study, we experimentally investigated decision rules and prey preferences of northwestern crows (Corvus caurinus) feeding on littleneck clams (Tapes philippinarum) and whelks (Nucella lamellosa). We presented crows with three species‐size combinations: small clams (2.0–2.9 cm length) paired with large whelks (4.0–4.9 cm), small clams paired with medium whelks (3.0–3.9 cm), and large clams (4.0–4.9 cm) with large whelks. Profitability estimates based on observations of crows feeding on these prey species indicated that clams were always the more energetically profitable option; however, in prey choice trials crows consistently selected the heavier prey species, regardless of differences in profitability. These results show that crows apply a general decision rule according to which they select heavier prey items when feeding on hard‐shelled prey requiring similar handling techniques, and that while such decision rules may approximate optimal choices they may not always follow predictions based solely on prey profitability. We discuss these results in the context of behavioural flexibility of generalist predators, and predicting impacts of intertidal avian predators on prey populations.