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.     

Adaptive search in juvenile plaice foraging for aggregated and dispersed prey

Juvenile plaice Pleuronectes platessa in a laboratory arena used intensive search behaviour, characterized by short movements and frequent turning, in the five movements before and after attacking a prey in an aggregated distribution. They used extensive search behaviour with, on average, longer movements and less turning at all other times. Intensive search was, apparently, triggered by a high local density of prey but not by isolated prey. This response to local prey density resulted in area-restricted search when prey were aggregated and win-shift behaviour when prey were dispersed. There was no evidence that the use of intensive search increased with experience of aggregated prey. It therefore appears that the fish were able to exploit encountered prey distribution patterns using their immediate perceptions rather than prior experience.     

Susceptibility of Atlantic herring and plaice larvae to predation by juvenile cod and herring at two constant temperatures

Predation encounters were staged in the laboratory to compare prey responsiveness, predator error rate, and predator capture success for juvenile cod Gadus morhua (a suction feeder) and herring Clupea harengus (a biting predator) preying on herring and plaice Pleuronectes platessa larvae. Trials were conducted at near natural temperature extremes for the larvae (8 and 13°C) to assess the importance of water temperature to the interaction. Herring larvae were significantly more responsive to attacks by herring than were plaice larvae (5·7 vs 0'0%). The two prey species were equally responsive to attacks by cod (2–6 vs 10%). Cod caught 91% of herring larvae attacked and juvenile herring caught 87%. Cod were successful in 96% of attacks on plaice, but juvenile herring caught significantly fewer (83%) plaice larvae. For each predator species, capture success did not vary significantly with prey species. Overall capture success for herring was significantly lower than that for cod. Responsiveness of herring larvae to attacks by juvenile herring increased with temperature, but predator error rate and capture success were not altered by water temperature.     

An optimal foraging and migration model for juvenile plaice

Summary A state-dependent model has been used to predict daily and tidal patterns of migration, feeding and inactivity in juvenile plaice (Pleuronectes platessa L.) in their intertidal and shallow subtidal nursery areas. Vertical position, quantity of energy reserves and fullness of the gut characterized the state of individual fishes. If feeding is visually mediated, the model predicts that, by night, plaice should move to areas of low predation risk and become inactive, whereas by day, plaice should migrate to feed in areas of high prey encounter rate. Vertical zones adopted by day and night and, hence, patterns of migration, should depend on the distributions of predators and prey. When prey are more abundant in the intertidal zone, plaice should move onshore to feed as the tide rises and when prey are more abundant offshore, plaice should move offshore to feed by day. If predators are equally abundant in all zones, the fish should behave as if no predators were present, having no effective refuge. An increase in the abundance of predators with depth results in the restriction of plaice activities to shallower vertical zones, depending on the magnitude of the predation threat. Zones adopted thus depend on the trade-off between energy intake and predation risk. Concordance between predicted behaviour and observed patterns is evident in contrasting habitats. Migration and feeding in the Wadden Sea, where prey are more abundant on intertidal flats, is dominated by the tidal component, whereas on impoverished exposed beaches of the west coast of Scotland, the diurnal component is dominant. Tidally related behaviour persists in the latter environment, not predicted by the model and may be a consequence of using endogenous rhythms to approach optimal behavioural patterns.     

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.     

Vulnerability of newly settled plaice (Pleuronectes platessa L.) to predation: effects of habitat structure and predator functional response

Plaice (Pleuronectes platessa) nursery grounds on the Swedish west coast have been subject to increasing cover of annual green macroalgae during recent years, with growth of algae starting at the time of plaice settlement in April to May. A laboratory experiment was performed to investigate how the vulnerability to predation of metamorphosing plaice was affected by the presence of filamentous algae. Predation by shrimps (Crangon crangon) on settling plaice larvae was higher on sand than among algae, whereas predation by crabs (Carcinus maenas) was unaffected by habitat type, suggesting a lower overall mortality of plaice in the vegetated habitat. When predators and prey were presented with a combination of the two habitats, predation by shrimps was as high as that in the sand treatment alone, whereas predation by crabs was lower than that in the two treatments with one habitat. Based on these results, an additional experiment was performed, investigating the functional response of shrimps to six densities of juvenile plaice in a sand habitat with alternative prey present. The proportional mortality of juvenile plaice (12-16 mm total length (TL)) was density-dependent and was best described by a type III (sigmoid) functional response of the predatory shrimps. The results suggested that the combined predation pressure from shrimps and crabs was lower among algae than on sand, but settling plaice and predatory shrimps chose the sand habitat. Plaice densities in the sigmoid part of the obtained functional response curve represented normal to high field densities of plaice on the Swedish west coast, suggesting that shrimp predation could have a stabilising effect on plaice recruitment. The formation of macroalgae mats could therefore lead to a concentration of plaice juveniles in the remaining sand habitat and increased mortality through density-dependent predation by shrimps.     

The effect of prey density on foraging mode selection in juvenile lumpfish: balancing food intake with the metabolic cost of foraging

1. In many species, individuals will alter their foraging strategy in response to changes in prey density. However, previous work has shown that prey density has differing effects on the foraging mode decisions of ectotherms as compared with endotherms. This is likely due to differences in metabolic demand; however, the relationship between metabolism and foraging mode choice in ectotherms has not been thoroughly studied. 2. Juvenile lumpfish Cyclopterus lumpus forage using one of two modes: they can actively search for prey while swimming, or they can 'sit-and-wait' for prey while clinging to the substrate using a ventral adhesive disk. The presence of these easily distinguishable foraging modes makes juvenile lumpfish ideal for the study of foraging mode choice in ectotherms. 3. Behavioural observations conducted during laboratory experiments showed that juvenile lumpfish predominantly use the 'cling' foraging mode when prey is abundant, but resort to the more costly 'swim' mode to seek out food when prey is scarce. The metabolic cost of active foraging was also quantified for juvenile lumpfish using swim-tunnel respirometry, and a model was devised to predict the prey density at which lumpfish should switch between the swim and cling foraging modes to maximize energy intake. 4. The results of this model do not agree with previous observations of lumpfish behaviour, and thus it appears that juvenile lumpfish do not try to maximize their net energetic gain. Instead, our data suggest that juvenile lumpfish forage in a manner that reduces activity and conserves space in their limited aerobic scope. This behavioural flexibility is of great benefit to this species, as it allows young individuals to divert energy towards growth as opposed to activity. In a broader context, our results support previous speculation that ectotherms often forage in a manner that maintains a minimum prey encounter rate, but does not necessarily maximize net energy gain.     

Space Utilization and Swimming Depth of White Sharks, Carcharodon carcharias, at the South Farallon Islands, Central California

This paper presents information on the movements of white sharks, Carcharodon carcharias, at the South Farallon Islands (SFI), central California. Acoustic telemetry techniques provided preliminary data on the diurnal space utilization, movement patterns and swimming depths of four white sharks, ranging from approximately 3.7 to 4.9m in length. Sharks swam within about 10m of the bottom to depths of approximately 30m, but in deeper water they tended to stray more from the bottom. Activity spaces for time periods tracked ranged from 1.84 to 9.15km². Indications are that an inverse relationship exists between length and activity space. During the time tracked, larger individuals swam within particular areas around the islands whereas smaller individuals did not restrict their movements in the same manner. Values of a site attachment index were inversely related to length for all sharks tracked. The site attachment indices, apparent inverse relationship between total length and activity space and observations on telemetered and other known individuals support a hypothesis that larger sharks possess site fidelity in their search for prey at SFI, within and between years. With the high frequency of predation by white sharks on juvenile northern elephant seals at SFI in the fall, the majority of the sharks' movements are probably related to their search for these pinniped prey. These data provide preliminary evidence that white sharks at SFI may search for prey by swimming in a particular area over a number of days or weeks, traversing the area in a manner which maximizes coverage, and swimming close to the bottom or at a distance far enough from the surface to remain cryptic from prey.     

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.     

Mechanism of the switchover from extensive to area-concentrated search behaviour of the ladybird beetle, Coccinella septempunctata bruckii

Area-concentrated search of predatory coccinellid adults, Coccinella septempunctata bruckii, is considered to be controlled by internal locomotory information, since the area-concentrated search is generated even if aphids are no longer present in the environment. To investigate what kind of cue elicits the switchover from extensive to area-concentrated search behaviour, the duration of area-concentrated search (giving-up time) was measured after each of the following five kinds of feeding stimuli was supplied: (a) contact with an aphid (Myzus persicae), (b) biting an aphid, (c) consumption of an aphid, (d) contact with an agar block of ca 2 × 2 × 2 mm, (e) consumption of an agar-block coated with a droplet of aphid body fluid. Switchover from extensive to area-concentrated search was observed as a response to all feeding stimuli. The cue to elicit the switchover is the contact with a prey rather than the consumption of it. The giving-up time is dependent on the intensity of feeding stimulus since giving-up time varied according to the type of feeding stimulus (d = a < b < e < c). The giving-up time was positively correlated with the duration of feeding on an aphid which represented the size of prey consumed. To test whether giving-up time is determined by the amount or by the size of prey consumed, it was measured after the ladybird beetle had fed first on a large then on a small aphid (Sequence A) and after it had fed first on a small then on a large aphid (Sequence B). Although the beetle consumed the same total amount of aphids in both sequences, the beetle showed the longer giving-up time in Sequence B than in Sequence A. Therefore, it can be concluded that giving-up time is determined by the size of prey most recently consumed rather than hunger level or prey capture rate.     

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.     

Diel activity pattern and food search behaviour in cod, Gadus morhua

Food search behaviour in cod, Gadus morhua, was studied by means of a stationary positioning system. Six fish in a fjord in northern Norway were tagged in situ by allowing them to shallow bait-wrapped acoustic tags, and their swimming behaviour was continuously recorded. The fish exhibited a diel activity rhythm, with higher swimming speeds and a larger range during the day than at night. Chemically mediated food search was studied in periods of both high and low activity by setting a string of baits in the morning and at night. During the period of high activity, more fish localized the baits (70 versus 45% of the observations) and the time to localization was 50% shorter, indicating that high swimming activity increased the probability of encountering the odour plume and the odour source. No diel variations in the response threshold to olfactory stimuli were found, as the proportion of fish in the odour plume that responded rheotactically, and their response distances were similar in the two periods (240 and 227 m respectively). Cod performed area-restricted searches on encountering the string of baits during the day. The probability of cod detecting prey by taste receptors, encountering the odour plume of prey or localizing a stationary food source after olfactory stimulation should be relatively independent of light, and this could explain why cod were active throughout the 24 h cycle. On the other hand, the visual detection distance and the ability to capture active prey are influenced by the light level, resulting in higher activity during the day.     

Piscivore efficiency and refuging prey: the importance of predator search mode

In predator-prey interactions, the efficiency of the predator is dependent on characteristics of both the predator and the prey, as well as the structure of the environment. In a field enclosure experiment, we tested the effects of a prey refuge on predator search mode, predator efficiency and prey behaviour. Replicated enclosures containing young of the year (0+) and 1-year-old (1+) perch were stocked with 3 differentially sized individuals of either of 2 piscivorous species, perch (Perca fluviatilis), pike (Esox lucius) or no piscivorous predators. Each enclosure contained an open predator area with three small vegetation patches, and a vegetated absolute refuge for the prey. We quantified the behaviour of the predators and the prey simultaneously, and at the end of the experiment the growth of the predators and the mortality and habitat use of the prey were estimated. The activity mode of both predator species was stationary. Perch stayed in pairs in the vegetation patches whereas pike remained solitary and occupied the corners of the enclosure. The largest pike individuals stayed closest to the prey refuge whereas the smallest individuals stayed farthest away from the prey refuge, indicating size-dependent interference among pike. Both size classes of prey showed stronger behavioural responses to pike than to perch with respect to refuge use, distance from refuge and distance to the nearest predator. Prey mortality was higher in the presence of pike than in the presence of perch. Predators decreased in body mass in all treatments, and perch showed a relatively stronger decrease in body mass than pike during the experiment. Growth differences of perch and pike, and mortality differences of prey caused by predation, can be explained by predator morphology, predator attack efficiency and social versus interference behaviour of the predators. These considerations suggest that pike are more efficient piscivores around prey refuges such as the littoral zones of lakes, whereas perch have previously been observed to be more efficient in open areas, such as in the pelagic zones of lakes.     

Behavioural aspects of predation by juvenile Atlantic salmon (Salmo salar L.) on particulate,drifting prey

A recirculatory flume tank simulating a simplified stream environment was used to study the feeding behaviour of juvenile Atlantic salmon (Salmo salar L.), 5.1 to 9.4 cm in fork length (from tip of snout to fork of tail), on artificial particulate prey passively drifting in the water current. Changes in feeding behaviour at two different times of the year and when fish were presented with prey of different sizes are described and quantified. Responsiveness to food was greatly reduced in autumn as compared to summer. The maximum distances at which prey elicited a response decreased in autumn to 40% of the summer value, and the maximum distances which fish traversed in order to capture prey decreased by 80% over the same period. During the peak growing season, the response to a range of prey sizes from 0.013 to 0.102 × fish fork length was directly related to prey size and could be accounted for on the basis of visual theory alone. Capture distances were closely related to fixation distances. Maximum capture distance increased to a peak value for prey of between 0.025 and 0.069 × fork length, while larger prey were never captured and the smallest prey rarely evoked a response. Prey size selectivity also operated after capture, through rejection versus retention of the prey.     

Quantifying the effects of habitat structure on prey detectability and accessibility to farmland birds

For species that rely on visual cues to detect prey items, increasing the structural complexity of a patch can greatly influence forager behaviour through consequent reductions in prey detectability and accessibility. These effects are likely to manifest themselves in terms of foraging site selection and there is plentiful evidence for preferential site selection for a suite of taxa. However, the underlying effects of habitat structure on foraging behaviour, which are likely to drive these observed site selections, are much less well understood. We present the results of two studies designed to quantify the effects of vegetation structure on prey detectability and accessibility to avian invertebrate feeders and granivores on farmland. There was a significant negative relationship between potential prey detectability and both distance and vegetation height in cereal crops and stubbles for Northern Lapwings Vanellus vanellus . The interscan distance travelled by Lapwings differed significantly between habitats, with longer distances travelled in cereal crops and harrowed compared with ploughed soil and grasses. The peck rate, head-up rate and mean search period of foraging Chaffinches Fringilla coelebs were not affected by increasing vegetation structure but forager mobility was significantly reduced. We hope that by quantifying the effects of vegetation structure on prey detectability and accessibility we can highlight the importance of considering these factors, as well as prey abundance, when developing management strategies for farmland birds.     

The role of sense organs in the feeding behaviour of juvenile sole and plaice

An infra-red video recording system was used to observe and compare the feeding activity of juvenile sole and plaice. Experiments in light or dark and chemical ablation of the neuromasts with streptomycin sulphate allowed all or a limited set of senses to be used by the fishes. Both species were able to feed on dead prey when only chemical stimuli were available. Plaice showed a greater dependence on vision for feeding but sole relied principally on chemoreception and mechanoreception. When any one sense was removed plaice became less active whereas sole became more active.     

Depth selection behaviour during activity cycles of juvenile plaice on a simulated beach slope

Juvenile plaice Pleuronectes platessa on a sand slope in a laboratory tank showed depthselection behaviour consistent with offshore migration by day and onshore by night, as seen in natural conditions. Plaice stayed deep (0·5 m) and avoided the shallowest water (<10 cm depth) during light periods, but ventured up the slope and into the shallows in darkness. The freshly caught fish showed circatidal cycles of activity, but showed no change in depth selection between periods of high (time of expected high water) and low activity (expected low water). This suggests that changing direction of movements in tidal migration is controlled by responses to changing environmental conditions. Further analysis showed movements of fish up the slope to be slower, covering less distance and with shorter pauses in between than moves down the slope. Frequency, distance travelled and speed of moves up and down the slope did not change with tidal or light-dark cycles, and so such modulation could be ruled out as a mechanism for migration.     

Flexible search tactics and efficient foraging in saltatory searching animals

Summary Foraging is one of the most important endeavors undertaken by animals, and it has been studied intensively from both mechanistic-empirical and optimal foraging perspectives. Planktivorous fish make excellent study organisms for foraging studies because they feed frequently and in a relatively simple environment. Most optimal foraging studies of planktivorous fish have focused, either on diet choice or habitat selection and have assumed that these animals used a cruise search foraging strategy. We have recently recognized that white crappie do not use a cruise search strategy (swimming continuously and searching constantly) while foraging on zooplankton but move in a stop and go pattern, searching only while paused. We have termed thissaltatory search. Many other animals move in a stop and go pattern while foraging, but none have been shown to search only while paused. Not only do white crappie search in a saltatory manner but the components of the search cycle change when feeding on prey of different size. When feeding on large prey these fish move further and faster after an unsuccessful search than when feeding on small prey. The fish also pause for a shorter period to search when feeding on large prey. To evaluate the efficiency of these alterations in the search cycle, a net energy gain simulation model was developed. The model computes the likelihood of locating 1 or 2 different size classes of zooplankton prey as a function of the volume of water scanned. The volume of new water searched is dependent upon the dimensions of the search volume and the length of the run. Energy costs for each component of the search cycle, and energy gained from the different sized prey, were assessed. The model predicts that short runs produce maximum net energy gains when crappie feed on small prey but predicts net energy gains will be maximized with longer runs when crappie feed on large prey or a mixed assemblage of large and small prey. There is an optimal run length due to high energy costs of unsuccessful search when runs are short and reveal little new water, and high energy costs of long runs when runs are lengthy. The model predicts that if the greater search times observed when crappie feed on small prey are assessed when they feed on a mixed diet of small and large prey, net energy gained is less than if small prey are deleted from the diet. We believe the model has considerable generality. Many animals are observed to move in a saltatory manner while foraging and some are thought to search only while stationary. Some birds and lizards are, known to modify the search cycle in a manner similar to white crappie.Components of the search cycle and dimensions of the location space SST (sec) Successful search time — the average time stationary prior to a pursuit - USST (sec) Unsuccessful search time — the average time stationary prior to a run - PT (sec) Pursuit time-PL/SS — the time to pursue prey at a given distance away. It is calculated by dividing the pursuit distance by swim speed - RT (sec) Run time-RL/SS — the time to complete a run of a given length. It is calculated by dividing the run length, by swim speed - PL (cm) Pursuit length-distance moved to attack prey - RL (cm) Run length-distance moved between consecutive searches - SS (cm/sec) Swim speed — the speed of movement during a pursuit or run - LS (l) Location space — the area or volume within which prey are located. In the case of white crappie the search space is shaped like a pie wedge with the fish positioned at the apex of the wedge - LA (^o) Location angle—the angle of the wedge-shaped search space - LH (cm) Location height—the height of the wedge-shaped search space - LD (cm) Location distance—the length of long axis of the wedge-shaped search space. Components of the location probability model RND Random number-random number generated through BASICA - SV (l) Search volume—the volume of water actually searched after one run of given length - SV_MAX (l) Maximum search volume—the greatest search volume that can be based upon LA, LH, LD and unaffected by the previous search - SV_R (l) Search volume researched—that volume of SV_MAX that is researched where RLo Search volume unsearched—that volume of SV_MAX not previously searched - AD (#/1) Absolute density—the density of zooplankton prey in numbers per liter - VD (#) Visual density—the number of zooplankton prey in the search volume - LP (%) Location probability—the probability that one or more prey are in the search volume Components of the net energy gain model NEG (cal/sec) Net energy gain-total calories ingested, less total calories used, divided by total time. - E _e (cal) Energy expended on the search cycle - E _i (cal) Energy intake - e _p (cal) Energy content of a given individual prey - P _i Total number of prey ingested - e _r (cal) Energy expended while searching - e _s (cal) Energy expended while swimming - T _t (sec) Total time-time expended to eat a given number of prey     

Macrobenthic prey availability and the potential for food competition between 0 year group Pleuronectes platessa and Limanda limanda

This study describes the feeding habits of plaice Pleuronectes platessa and dab Limanda limanda during early juvenile development and relates differences between nursery grounds and sampling years to spatial and temporal variabilities in macrobenthic prey availability. The main prey taxa of both species were copepods, bivalves, amphipods, polychaetes and oligochaetes and size-related variation in diet was found. Despite considerable similarity in the prey items, differences in food composition between the two species were observed and spatial variability in diet confirmed their opportunistic feeding behaviour. A high degree of dietary overlap was found in June and decreased steadily throughout the season. The prey composition in the guts of both species largely reflected the composition of the main macrobenthic taxa in the sediment. The overall data suggest that resources were not limiting in the littoral sandy nursery areas in the west of Ireland and no indications were found that exploitative competitive forces upon the benthic prey assemblages occurred between P. platessa and L. limanda. Feeding success, Fulton's K condition and dietary overlap, however, showed spatial and temporal variations, and were probably affected by the availability and density of macrobenthic prey.