The efficiency of adaptive search tactics for different prey distribution patterns: a simulation model based on the behaviour of juvenile plaice

Juvenile plaice Pleuronectes platessa are particularly useful for studying forager search behaviour because their search paths are essentially two dimensional, and punctuated by natural stops. Their prey occur in a range of natural distributions from highly aggregated to over‐dispersed. Juvenile plaice use area‐restricted search near aggregated prey and extensive search, consisting of longer moves and fewer turns, between aggregations and when searching for dispersed prey. They search for less conspicuous prey items mainly in the pauses between movements. This saltatory search behaviour contrasts with the continuous search that is usually assumed in search models. A simulation model of saltatory search behaviour showed that a strategy combining extensive and intensive search allows the efficient exploitation of a range of natural prey distribution patterns, and that it is particularly effective when the search behaviour is controlled by perceived prey density. This allows the predator to respond to the localized aggregations which often occur in nature. The selective use of intensive search was more efficient than the continuous use of extensive search even in prey distribution patterns that were statistically over‐dispersed.     

Increased turning per unit distance as an area-restricted search mechanism in a pause-travel predator, juvenile plaice, foraging for buried bivalves

During searching, discovery of a prey patch by juvenile plaice Pleuronectes platessa was associated with a change from extensive to intensive search behaviour several moves before an attack on a prey. Intensive search behaviour was characterized by reduced distance of moves, a greater rate of turning per unit distance and shorter pauses between moves. The increase in turn rate was associated with area-restricted seaching, while a decrease in distances moved suggests that plaice search more efficiently for prey when stationary than while moving. The klinokinetic mechanism that appears to regulate search behaviour in juvenile plaice should allow efficient exploitation of a range of prey distribution patterns based on localized cues alone. Such a mechanism is especially useful to a migratory predator, like plaice, whose foraging is subject to time constraints imposed by tidally available feeding areas.     

Sources of variability in the transition from extensive to intensive search in coccinellid predators (Homoptera: Coccinellidae)

In an environment structured by habitats, prey patches, and prey, predators such as coccinellids have two movement modes. The extensive search and the intensive search which results from prey capture are adopted for patch localization and exploration, respectively. The variability of changes from extensive search to intensive search was studied in larvae of the aphidophagous coccinellidSemiadalia undecimpunctata to find out their possibility of adaptation to a fluctuating environment. The temporal organization of coccinellid movements appears far more complicated than the generally accepted succession of extensive search, feeding, and intensive search. Their paths are characterized by the presence of time intervals devoted to intensive search before feeding, a highly variable path response after prey consumption (larvae may adopt intensive search immediately, later, or never), and the alternation of time periods devoted to either extensive search or intensive search after prey ingestion. This interindividual variability suggests that coccinellids have the ability to adapt to heterogeneity or short-term changes in environmental conditions, particularly in prey distribution. These results are in favor of the use of these predators in biological control programs.     

Functional response and area‐restricted search in a predator: seasonal exploitation of anurans by the European polecat,Mustela putorius

A study of the feeding habits and movements of 11 radiotracked polecats Mustela putorius in western France revealed that seasonal predation upon agile frogs, Rana dalmatina, was directly influenced by prey abundance and distribution. Although dietary structure showed the importance of mammalian prey (71.5%), polecats exploited nocturnal, terrestrial anurans in spring (31.6%). The periodic activity of anurans at spawning sites led both to a maximum density in spring and to a patchy distribution. The monthly variations in anuran dietary occurrences were associated with changes in frog availability. The functional response of polecats to frog density was sigmoidal shaped (type 3 response). Frog consumption rate increased more slowly than prey density but frogs were actively removed at higher density. It is therefore suggested that frog populations were moderately affected by the predator and this density dependent effect tends to stabilise anuran populations. Predation upon anurans was also correlated with a prey dispersion index as revealed by a polynomial regression. Polecats concentrated their predation on spawning congregations of the breeding adult frogs. Movements were smallest in spring and polecats changed their track length by increasing the difference between a succession of small movements and of longer journeys towards profitable sites. Changes in movements correlated with the anuran dispersion index and the response was sigmoidal (polynomial regression) revealing an area‐restricted search. This response may be regarded as an ‘aggregative response’ according to the first part of the definition of Begon et al. (1996) . Functional and area‐restricted search responses to the frog abundance and dispersion constitute an original example of predator‐prey coexistence strategies among vertebrates. I suggest that such predation could be favoured by the individualistic habits of the mustelid.     

The Effects of Prey Patchiness, Predator Aggregation, and Mutual Interference on the Functional Response of Phytoseiulus persimilis Feeding on Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae)

The spatial distributions of two-spotted spider mites Tetranychus urticae and their natural enemy, the phytoseiid predator Phytoseiulus persimilis, were studied on six full-grown cucumber plants. Both mite species were very patchily distributed and P. persimilis tended to aggregate on leaves with abundant prey. The effects of non-homogenous distributions and degree of spatial overlap between prey and predators on the per capita predation rate were studied by means of a stage-specific predation model that averages the predation rates over all the local populations inhabiting the individual leaves. The empirical predation rates were compared with predictions assuming random predator search and/or an even distribution of prey. The analysis clearly shows that the ability of the predators to search non-randomly increases their predation rate. On the other hand, the prey may gain if it adopts a more even distribution when its density is low and a more patchy distribution when density increases. Mutual interference between searching predators reduces the predation rate, but the effect is negligible. The stage-specific functional response model was compared with two simpler models without explicit stage structure. Both unstructured models yielded predictions that were quite similar to those of the stage-structured model.     

Searching efficiency of the lady beetleCoccinella septempunctata larvae in uniform and patchy environments

Experiments were conducted on the searching behavior and searching efficiency of the lady beetleCoccinella septempunctata bruckii Mulsant under conditions of various prey distributions and prey densities. The larvae changed their searching behavior before and after feeding. Before feeding the larvae moved quickly and the searching paths were nearly linear. But after feeding the speed decreased and turning angle increased. The speed and turning angle reverted gradually and recovered the initial pattern 95 s after feeding. The searching efficiency differed depending on the prey distribution. At low prey density, searching was most efficient when prey were distributed uniformly. But at middle and high prey densities, searching was most efficient when prey items were highly aggregated. The observed searching behavior of 4th instarC. septempunctata larvae was likely to be optimal considering the natural distribution of colonies of their prey, aphids.     

Influence of larval rearing diet on the intensive searching behaviour ofHarmonia axyridis [Col.: Coccinellidae] Larvae

The capture of prey by last instar larvae of the aphidophagous coccinellidHarmonia axyridis Pallas (Col.,Coccinellidae) modified larval movement so that extensive search was replaced by intensive search. The continuous rearing of this species on eggs ofEphestia kühniella Zell. (Lep.,Pyralidae) or on the aphidAcyrthosiphon pisum Harris (Homopt.,Aphidae) led to conditioning. Only larvae that ate the same prey as they were reared on, adopted intensive searching movements after feeding. Using larvae reared on substitute prey in biological control systems may decrease the efficiency of the released predators.     

Quantitative analysis of bottlenose dolphin movement patterns and their relationship with foraging

1. Broad-scale telemetry studies have greatly improved our understanding of the ranging patterns and habitat-use of many large vertebrates. However, there often remains considerable uncertainty over the function of different areas or the factors influencing habitat selection. Further insights into these processes can be obtained through analyses of finer scale movement patterns. For example, search behaviour may be modified in response to prey distribution and abundance. 2. In this study, quantitative analysis techniques are applied to the movements of bottlenose dolphins, recorded from land using a theodolite, to increase our understanding of their foraging strategies. Movements were modelled as a correlated random walk (CRW) and a biased random walk (BRW) to identify movement types and using a first-passage time (FPT) approach, which quantifies the time allocated to different areas and identifies the location and spatial scale of intensive search effort. 3. Only a quarter of the tracks were classed as CRW movement. Turning angle and directionality appeared to be key factors in determining the type of movement adopted. A high degree of overlap in search effort between separate movement paths indicated that there were small key sites (0.3 km radius) within the study area (4 km(2)). Foraging behaviour occurred mainly within these intensive search areas, indicating that they were feeding sites. 4. This approach provides a quantitative method of identifying important foraging areas and their spatial scale. Such techniques could be applied to movement paths for a variety of species derived from telemetry studies and increase our understanding of their foraging strategies.     

The searching behaviour of Anthocoris confusus (Reuter) in relation to prey density and plant surface topography

• 1 The searching behaviour of A.confusus females was investigated in an artificial arena.
• 2 Females showed an increase in the frequency of turning movements following feeding and this concentrated search in a small area. As a result more prey were found in areas where prey distribution was clumped.
• 3 If no prey was encountered within 5–8 min the search track straightened out.
• 4 First and second instar nymphs searching on broad bean plants moved faster on the undersides of leaves which were the sites most likely to support aphid populations. A considerable proportion of available time was wasted in periods of inactivity.
• 5 It was concluded that while plant topography strongly influences search pattern, the underlying trend demonstrated in these experiments was of advantage to predators searching for colonial prey.

     

Fluctuations in prey density: effects on the foraging tactics of scolopendrid centipedes

Foraging animals are faced with the problem of acquiring information about prey populations and utilizing that information in making foraging decisions. In this paper the effect of variation in prey density on the search tactics and mechanisms of prey density assessment in the centipede Scolopendra polymorpha are examined. Centipedes exhibited a prey density-dependent repertoire of search tactics. After 50 min of exposure to high prey density, centipedes switched from active search to ambush-like tactics, while maintaining a high rate of search at the lowest prey density. An initial period of sampling of prey density was involved in the switch in search behaviour and it is suggested that the encounter rate with prey was the key element in density assessment. When the prey density was changed from low to high, centipedes switched from active search to ambush tactics and when prey density was changed from high to low centipedes switched from ambush to active search within 40 min. Such behaviour may decrease the unreliability of sampling information and the risk involved in foraging decisions in variable environments.     

The consequences of partially directed search effort

Search effort is undirected when a forager has a stereotypical searching behaviour that results in fixed encounter rates with its prey (e.g. diet choice models), and is directed when the forager can bias its encounter with a ‘chosen’ prey. If the bias is complete, search is totally directed (e.g. habitat selection models). When the bias is incomplete (i.e. search modes are not exclusive to a single prey type), search is partially directed. The inclusion of a prey type in the diet is then the result of two decisions: (1) which prey to search for and (2) which prey to handle. The latter decision is determined by the ratio of energy to handling time and the abundance of the preferred prey. The former decision is a function of the encounter probabilities and densities of all potential prey types in addition to their ratio of energy to handling time. Assuming two prey types, there are three distinct behavioural strategies: (1) search for the preferred prey/forage selectively; (2) search for the preferred prey/forage opportunistically; and (3) search for the non-preferred prey/forage opportunistically. If prey are depletable (i.e. prey occur in resource patches), the forager may switch search modes such that prey are depleted to the point where the marginal values of the search modes are equalized. This revised version was published online in July 2006 with corrections to the Cover Date.     

Ambulatory dispersal behavior ofNeoseiulus fallacis (Acarina: Phytoseiidae) in relation to prey density and temperature

Ambulatory dispersal behavior ofNeoseiulus fallacis (Garman) was studied in the laboratory to evaluate within-plant movement in relation to temperature and prey density. Adult femaleN. fallacis were confined in 2.5-cm-diameter arenas on the abaxial surface of excised corn leaves. Four temperatures (23, 28, 33, and 39° C) and prey densities ranging from 0 to 55 spider mite eggs per cm² were used. The walking paths of these mites were traced, digitized and used to calculate turning angles, walking speeds and turning rates. A computer simulation of walking behavior used this information to model mite ambulatory behavior and predict dispersal rates.Neoseiulus fallacis behavior while on whole corn leaves was quantified to verify the results of the simulation. The results showed thatN. fallacis will follow a leaf or arena edge (edge-walking) at all temperatures and prey densities. In addition, this behavior was used to the exclusion of the other types of behavior such as resting, and random-walk type search when prey egg density was less than 4 eggs per cm². The exclusion of edge-walking behavior from the model caused the model to underestimate substantially the dispersal rates leaves. These data suggest that there are at least two recognizable types of ambulatory search used byN. fallacis—the random-walk type, which is used when prey density is high (searching within prey patches), and the edge-walking behavior, which is used when prey density is low. This behavior allows the mite to travel rapidly from leaf to leaf in search of new prey patches.     

Saltatory search in a lateral line predator

The dwarf scorpionfish Scorpaena papillosa detected the hydrodynamic signals produced by prey with the mechanosensory lateral line. This species displayed a pause and move search pattern that is consistent with a saltatory search. The pause phase of the search cycle was probably used to detect prey because pauses often ended early in order to initiate an approach at prey and prey were detected throughout the search space. The move phase of the search cycle repositioned the fish so that it moved approximately a third of the reactive distance. Move distance was found to be the most important factor in gaining novel search space. Turning was shown to be relatively unimportant in gaining novel search space with a high frequency of low turn angles made by the fish. The dwarf scorpionfish, however, exhibited a spiralling or looping pattern over a search path exhibiting a turn bias towards either the left or right. The dwarf scorpionfish adopted a search behaviour that is consistent with a saltatory search and efficient for lateral line predation.     

Local search in the housefly Musca domestica after feeding on sucrose

Local search behaviour of the housefly, Musca domestica, released by ingestion of sucrose, was recorded on a bitpad digitizer. Local search is characterized by an initial increase in turning rate and a decrease in locomotory rate followed by an exponential return to control (unfed) levels for both functions. Greater variation in the slope of the exponential return to control levels was observed between runs of different flies than between runs of an individual fly, suggesting a possible internal basis for locomotory and turning functions. The local search pattern, based on decrease in relative turning rate generates a spiral configuration. A zig-zag component increases path width and increases the chances of a fly relocating the drop residue. Looping patterns correlate with successive recontacts with the drop residue and associated changes in turn direction and stopping. The results are discussed with respect to sources of internal and external orientation information controlling local search.     

Lévy flight and Brownian search patterns of a free-ranging predator reflect different prey field characteristics

1. Search processes play an important role in physical, chemical and biological systems. In animal foraging, the search strategy predators should use to search optimally for prey is an enduring question. Some models demonstrate that when prey is sparsely distributed, an optimal search pattern is a specialised random walk known as a Lévy flight, whereas when prey is abundant, simple Brownian motion is sufficiently efficient. These predictions form part of what has been termed the Lévy flight foraging hypothesis (LFF) which states that as Lévy flights optimise random searches, movements approximated by optimal Lévy flights may have naturally evolved in organisms to enhance encounters with targets (e.g. prey) when knowledge of their locations is incomplete. 2. Whether free-ranging predators exhibit the movement patterns predicted in the LFF hypothesis in response to known prey types and distributions, however, has not been determined. We tested this using vertical and horizontal movement data from electronic tagging of an apex predator, the great white shark Carcharodon carcharias, across widely differing habitats reflecting different prey types. 3. Individual white sharks exhibited movement patterns that predicted well the prey types expected under the LFF hypothesis. Shark movements were best approximated by Brownian motion when hunting near abundant, predictable sources of prey (e.g. seal colonies, fish aggregations), whereas movements approximating truncated Lévy flights were present when searching for sparsely distributed or potentially difficult-to-detect prey in oceanic or shelf environments, respectively. 4. That movement patterns approximated by truncated Lévy flights and Brownian behaviour were present in the predicted prey fields indicates search strategies adopted by white sharks appear to be the most efficient ones for encountering prey in the habitats where such patterns are observed. This suggests that C. carcharias appears capable of exhibiting search patterns that are approximated as optimal in response to encountered changes in prey type and abundance, and across diverse marine habitats, from the surf zone to the deep ocean. 5. Our results provide some support for the LFF hypothesis. However, it is possible that the observed Lévy patterns of white sharks may not arise from an adaptive behaviour but could be an emergent property arising from simple, straight-line movements between complex (e.g. fractal) distributions of prey. Experimental studies are needed in vertebrates to test for the presence of Lévy behaviour patterns in the absence of complex prey distributions.     

Feeding behaviour determining differential capture success of evasive prey in underyearling European perch (<Emphasis Type="Italic">Perca fluviatilis</Emphasis> L.) and roach (<Emphasis Type="Italic">Rutilus rutilus</Emphasis> (L.))

The effect of feeding behaviour on the prey capture efficiency of young-of-the-year European perch and roach was investigated in laboratory experiments using planktonic crustaceans possessing different escape abilities—Daphnia sp. and Cyclops sp. Two sets of experiments were performed. In the first set, the feeding efficiency and behaviour of 270 fish individuals were determined by stomach content analyses and video record evaluations. In the second set of experiments, analysis of attack-effort, which was evaluated as attack-distance and repeated strikes, was undertaken. Except for situations in which Daphnia was offered at high densities, the feeding efficiency of perch was significantly higher compared to roach in all other combinations of prey types and densities. Roach consumed significantly less prey compared to perch when feeding exclusively on the evasive Cyclops and when it was offered in a 1:1 ratio mixture with Daphnia. The mean swimming speed was similar in both fish species, but behavioural differences were evident during prey search and capture. Perch swam through the aquaria in short and fast movements that were interrupted by many stops. Roach exhibited rather continuous swimming that was punctuated by slowdowns instead of stops. The perch attacks were very intensive and repeated strikes occurred, particularly when feeding on evasive Cyclops. On the other hand, roach revealed strong schooling behaviour restricting the fish during inspection of the experimental aquaria. The distinct differences in feeding efficiency between perch and roach were demonstrated to be closely related to differences in their feeding behaviour. Discontinuous searching for prey, vigorous attacks, occurrence of repeated strikes and the absence of schooling increased perch prey capture efficiency, particularly when foraging on evasive copepods.     

The advantage of alternative tactics of prey and predators depends on the spatial pattern of prey and social interactions among predators

Individual variation in behavioral strategies is ubiquitous in nature. Yet, explaining how this variation is being maintained remains a challenging task. We use a spatially-explicit individual-based simulation model to evaluate the extent to which the efficiency of an alternative spacing tactic of prey and an alternative search tactic of predators are influenced by the spatial pattern of prey, social interactions among predators (i.e., interference and information sharing) and predator density. In response to predation risk, prey individuals can either spread out or aggregate. We demonstrate that if prey is extremely clumped, spreading out may help when predators share information regarding prey locations and when predators shift to area-restricted search following an encounter with prey. However, dispersion is counter-selected when predators interact by interference, especially under high predator density. When predators search for more randomly distributed prey, interference and information sharing similarly affect the relative advantage of spreading out. Under a clumped prey spatial pattern, predators benefit from shifting their search tactic to an area-restricted search following an encounter with prey. This advantage is moderated as predator density increases and when predators interact either by interference or information sharing. Under a more random prey pattern, information sharing may deteriorate the inferior search tactic even more, compared to interference or no interaction among predators. Our simulation clarifies how interactions among searching predators may affect aggregation behavior of prey, the relative success of alternative search tactics and their potential to invade established populations using some other search or spacing tactics.     

Does prey capture induce area-restricted search? A fine-scale study using GPS in a marine predator, the wandering albatross

In a patchy environment, predators are expected to increase turning rate and start an area-restricted search (ARS) when prey have been encountered, but few empirical data exist for large predators. By using GPS loggers with devices measuring prey capture, we studied how a marine predator adjusts foraging movements at various scales in relation to prey capture. Wandering albatrosses use two tactics, sit and wait and foraging in flight, the former tactic being three times less efficient than the latter. During flight foraging, birds caught large isolated prey and used ARS at scales varying from 5 to 90 km, with large-scale ARS being used only by young animals. Birds did not show strong responses to prey capture at a large scale, few ARS events occurred after prey capture, and birds did not have high rates of prey capture in ARS. Only at small scales did birds increase sinuosity after prey captures for a limited time period, and this occurred only after they had caught a large prey item within an ARS zone. When this species searches over a large scale, the most effective search rule was to follow a nearly straight path. ARS may be used to restrict search to a particular environment where prey capture is more predictable and profitable.     

Influence d'une alimentation préalable et du jeûne sur l'apparition de la recherche intensive des proies chez Semiadalia undecimnotata

Résumé Les prédateurs qui vivent aux dépens de ressources alimentaires groupées, modifient leur mode de déplacement après la capture et l'ingestion d'une proie. Ils passent de la recherche extensive (déplacements rapides et linéaires) à la recherche intensive (déplacements lents et sinueux). Chez les adultes et les larves de dernier stade de la coccinelle Semiadalia undecimnotata Schn. (Col., Coccinellidae), dans les premières heures qui suivent leur naissance ou leur mue, l'ingestion d'un premier puceron ne modifie pas les caractéristiques locomotrices individuelles: les déplacements restent de type extensif. Au début de chaque stade, cette coccinelle présente une période de sensibilisation à la proie rencontrée. Durant ces laps de temps, elle doit consommer plusieurs proies avant d'être capable d'adopter la recherche intensive. L'existence d'une période de jeûne avant cette première prise alimentaire favorise, au contraire, l'adoption de la recherche intensive.

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The ladybird, Semiadalia undecimnotata, like all other entomophagous insects feeding on relatively sedentary prey, exhibits two types of walking pattern during the search for prey: xtensive and intensive search. The latter is engaged following detection of visual or chemical cues. Changes in the ladybird search pattern: extensive search—a single prey capture—intensive search, were investigated in relation to experience of prior feeding-periods (experienced coccinellids) or to lack of such experience (naïve coccinellids) and with respect to changes in duration of fasting. The analysis of their pathways was performed initially by comparison of three locomotory paramètres: the number of stops (number/s), the walking speed (mm/s) and the turning-rate (degrees/s), and subsequently by statistical classification (principle components analysis). Unlike experienced coccinellids, observations of naïve coccinellids, indicate that a single feeding session during the three to five hours after emergence of an adult, or ecdysis of the larva, will change the walking pattern slightly. These animals will maintain extensive search or adopt a particular, intermediate locomotory pattern which is a development of extensive search but do not adopt intensive search. Fasting, for periods over twelve hours, favoured intensive search in populations studied. It is probable that the requirement to feed on more than one prey item before adopting intensive search involves concepts such as forms of learning (sensitization).

     

Effects of prey density and spatial distribution on prey consumption of the adult predatory ladybird beetle

The effects of prey density and spatial distribution on prey consumption of the adult predatory ladybird, Harmonia axyridis , were investigated by using a 2 × 2 factorial design in large scale cages. Prey density influenced prey consumption of the ladybirds, and the frequency with which predation occurred was quite different between the prey distributions. The ladybirds consumed a relatively constant and small number of aphids when the prey were uniformly distributed, whereas the number of prey consumed per day when predation occurred was large and much more variable when the prey were contagiously distributed. At high prey density, the number of prey consumed was highest during the first day of the experiment; thereafter, only 10–20 aphids were consumed during the following 3 days. However, these patterns of prey consumption were not observed at low prey density. The percentage of aphids that remained on the host plants when the experiments were terminated was higher at low prey density than at high prey density, suggesting that predator foraging efficiency at low prey density was lower than at high prey density. Ladybirds foraging for high prey density were more frequently observed on the plants with aphids than ladybirds foraging for low prey density. Prey distribution also influenced the frequency of residence of ladybirds on the plants. The different predation patterns observed in the two spatial distributions, in which prey consumption was much more variable for the contagious distribution, might be explained by the difference in prey encounter rate of the predator between the distributions. This study indicated that the ladybirds had limited ability to search out prey over large spatial scales.