Predators use environmental cues to discriminate between prey

The cognitive processes of predators play a central role in the evolution of prey characters. Numerous studies have shown that vertebrate predators may learn to associate the characteristics of prey (e.g. color) with the cost or benefit of ingesting them, thus forming preferences and aversions for different kinds of prey. Although the distribution and quality of prey types can differ between environmental contexts, which may make it profitable to attack a prey type in some contexts but not in others, the influence of environmental cues in decisions to attack has rarely been addressed. Recent theory suggests that modification of prey preferences by environmental cues such as microhabitat or temperature may influence the evolution of prey characteristics. Here, we show that the environmental foraging context may determine prey choice in great tits (Parus major) through learned association between the prey phenotype (appearance and palatability) and a contextual background cue. The same individuals were able to learn and maintain two different sets of food preferences and aversions for use in two different environmental contexts (aviaries with red or blue wooden boards), indicating a role for contextual learning in vertebrate foraging behavior.     

Contrasting foraging tactics by northern gannets (<Emphasis Type="Italic">Sula bassana</Emphasis>) breeding in different oceanographic domains with different prey fields

In order to forage and to provision offspring effectively, seabirds negotiate a complex of behavioural, energetic, environmental and social constraints. In first tests of GPS loggers with seabirds in North America, we investigated the foraging tactics of free-ranging northern gannets (Sula bassana) at a large and a medium-sized colony that differed in oceanography, coastal position and prey fields. Gannets at Low Arctic colony (Funk Island) 50 km off the northeast coast of Newfoundland, Canada provisioned chicks almost entirely with small forage fish (capelin Mallotus villosus, 89%), while at boreal colony (Bonaventure Island) 3 km from shore in the Gulf of St. Lawrence, Quebec, Canada, large pelagic fish dominated parental prey loads (Atlantic mackerel Scomber scombrus 50%, Atlantic herring Clupea harengus 33%). Mean foraging range and the total distance travelled per foraging trip were significantly greater at the larger inshore colony (Bonaventure) than at the smaller offshore colony (Funk Island; 138 and 452 km vs. 64 and 196 km, respectively). Gannets from Funk Island consistently travelled inshore to forage on reproductive capelin shoals near the coast, whereas foraging flights of birds from Bonaventure were much more variable in direction and destination. Birds from the Low Arctic colony foraged in colder sea surface water than did birds from the boreal colony, and dive characteristics differed between colonies, which is concordent with the difference in prey base. Differences between the colonies reflect oceanographic and colony-size influences on prey fields that shape individual foraging tactics and in turn generate higher level colony-specific foraging “strategies”.     

Chemosensory responses and foraging behavior of the seastar<Emphasis Type="Italic"> Pycnopodia helianthoides</Emphasis>

Chemical cues released by damaged or dead organisms can affect how and where benthic organisms feed. These cues may cause predators to act as opportunistic scavengers in lieu of their normal predatory role. A scavenger, as defined in this study, is an organism that consumes damaged and/or dead organisms. In-situ experiments were performed to determine how the seastar Pycnopodia helianthoides (Brandt) reacts in the presence of chemical cues from one of its prey species, the butter clam Saxidomus giganteus (Deshayes), using both intact and damaged individuals. The results of these experiments suggest that P. helianthoides use their chemosensory abilities to locate damaged/dead prey. The role of current in propagating chemical cues was paramount in this foraging activity. P. helianthoides chose damaged prey over live prey even when live prey was encountered en route to the damaged individual. This study suggests that chemical cues emitted from damaged or dead individuals may cause significant changes in foraging tactics of key predators, thus altering food-web dynamics.Communicated by J.P. Grassle, New Brunswick     

Individual specialization in the hunting wasp <Emphasis Type="Italic">Trypoxylon</Emphasis> (<Emphasis Type="Italic">Trypargilum</Emphasis>) <Emphasis Type="Italic">albonigrum</Emphasis> (Hymenoptera,Crabronidae)

Individual-level variation in resource use occurs in a broad array of vertebrate and invertebrate taxa and may have important ecological and evolutionary implications. In this study, we measured the degree of individual-level variation in prey preference of the hunting wasp Trypoxylon albonigrum, which inhabits the Atlantic Forest in southeastern Brazil. This wasp captures several orb-weaving spider genera to provision nests. Individuals consistently specialized on a narrow subset of the prey taxa consumed by the population, indicating the existence of significant individual-level variation in prey preferences. The population niche was broader in the wet season in terms of both prey size and taxa. In the case of prey size, the population niche expansion was achieved via increased individual niche breadths, whereas in the case of prey taxa, individual niches remained relatively constrained, and the population niche expanded via increased interindividual variation. The observed pattern suggests the possibility of functional trade-offs associated with the taxon of the consumed prey. The nature of the trade-offs remains unknown, but they are likely related to learning in searching and/or handling prey. We hypothesize that by specializing on specific prey taxa, individuals increase foraging efficiency, reducing foraging time and ultimately increasing reproductive success.     

Threat-sensitive learning of predators by larval mosquitoes <Emphasis Type="Italic">Culex restuans</Emphasis>

A prerequisite for prey to show adaptive behavioural responses to predators is that the prey has the ability to recognise predators as threats. While predator recognition can be innate in many situations, learning is often essential. For many aquatic species, one common way to learn about predators is through the pairing of a novel predator odour with alarm cues released from injured conspecifics. One study with fish demonstrated that this mode of learning not only allows the prey to recognise the predatory cues as a threat, but also mediates the level of threat associated with the predator cues (i.e. threat-sensitive learning). When the prey is exposed to the novel predator with a high concentration of alarm cues, they subsequently show a high intensity of antipredator response to the predator cues alone. When exposed to the predator with a low concentration of alarm cues, they subsequently show a low-intensity response to the predator cues. Here, we investigated whether larval mosquitoes Culex restuans have the ability to learn to recognise salamanders as a threat through a single pairing of alarm cues and salamander odour and also whether they would learn to respond to salamander cues in a threat-sensitive manner. We conditioned individual mosquitoes with water or a low, medium or high concentration of crushed conspecific cues (alarm cues) paired with salamander odour. Mosquitoes exposed to salamander odour paired with alarm cues and subsequently exposed to salamander odour alone responded to the salamander as a threat. Moreover, the intensity of antipredator response displayed during the conditioning phase matched the response intensity during the testing phase. This is the first demonstration of threat-sensitive learning in an aquatic invertebrate.     

Search behavior of the checker-throated antwren foraging in aerial leaf litter

Summary Checker-throated antwrens (Formicariidae: Myrmotherula fulviventris) live in lowland neotropical forests and forage from dead curled leaves in the understory. Because they search each leaf individually they provide an opportunity to study the use of potential visual cues by an insectivorous bird. Long and highly curled leaves contain the most arthropods and checker-throated antwrens were more successful when foraging at those leaves. Yet, they used leaves at random with respect to these potential cues. Antwrens spent longer searching for arthropods in each highly curled leaf than in less curled leaves. Because of this additional search time, prey capture success per unit foraging time was only slightly greater for highly curled leaves than at the average dead leaf in the aerial leaf litter. Thus, the cues that antwrens could use to locate richer leaves are those features that obscure the prey from avian predators. Unlike other foraging systems, the antwrens appear to have no reliable cues indicating more profitable foraging sites.Address for correspondence     

Social information,conformity and the opportunity costs paid by foraging fish

Animals pay opportunity costs when pursuing one of several mutually exclusive courses of action. We quantified the opportunity costs of conforming to the behaviour of others in foraging sticklebacks (Pungitius pungitius), using an arena in which they were given the option of shoaling in one area or searching for food in another. Fish foraging in the absence of stimulus conspecifics found the prey patch sooner and spent longer exploiting it than those in trials where a stimulus shoal was present. Furthermore, in trials where the stimulus shoal exhibited feeding cues, subjects approached them sooner and spent more time shoaling with them, exploring less of the arena than in trials where the stimulus shoal exhibited no such cues. This suggests sensitivity not only to the mere presence of conspecifics, but also to the social information that they produce. We also saw that groups of focal fish, compared to single individuals, were less influenced by the stimulus shoal and explored more of the arena, a behaviour that may be attributed to facilitation, competition or both. Such opportunity costs are likely to be offset by benefits such as reduced predation risk, and we discuss this in terms of the trade-offs associated with living in groups.     

Predatory behavior of Polybia sericea (Olivier), a tropical social wasp (Hymenoptera: Vespidae)

Summary Polybia sericea (Olivier) (Hymenoptera: Vespidae) foragers were trained to visit experimental foraging plots and tests were conducted to determine the role of visual, olfactory, and chemotactile cues in prey location. Foragers approached prey from downwind and hovered downwind of visual and olfactory stimuli. Olfactory cues were more likely to elicit landing than were visual cues. Biting of potential prey was most consistently elicited by a combination of visual, tactile, and chemotactile cues. Foragers encountering large prey carried a piece back to the nest and returned for prey remains. These returning foragers used visual cues to direct intensive aerial search; olfactory prey cues elicited landing.     

Social recognition in sticklebacks: the role of direct experience and habitat cues

The social organisation of animals relies on recognition. However, there are many means by which animals may recognise one another and a variety of cues are available to any individual at any one time. We tested the effects of cues based on direct experience and of cues based on habitat and diet on association decisions in the three-spined stickleback (Gasterosteus aculeatus). Our results show that sticklebacks rapidly acquire association preferences for novel con- and heterospecifics (nine-spined sticklebacks, Pungitius pungitius) which had experienced the same habitat and diet conditioning as themselves over novel con- and heterospecifics which had experienced a different habitat and diet conditioning, a preference which may be based on self-referent matching. Association preferences were observed after only 24 h and were independent of the number of tank mates (treatments with 20 and 100 fish). Evidence for the influence of direct social experience on association preferences was weak and may be confounded by other factors.Communicated by K. Lindström     

The dynamics of social learning in an insect model,the bumblebee (<Emphasis Type="Italic">Bombus terrestris</Emphasis>)

Bumblebees (Bombus terrestris) are attracted to those particular inflorescences where other bees are already foraging, a process known as local enhancement. Here, we use a quantitative analysis of learning in a foraging task to illustrate that this attraction can lead bees to learn more quickly which flower species are rewarding if they forage in the company of experienced conspecifics. This effect can also be elicited by model bees, rather than live demonstrators. We also show that local enhancement in bumblebees most likely reflects a general attraction to conspecifics that is not limited to a foraging context. Based on the widespread occurrence of both local enhancement and associative learning in the invertebrates, we suggest that social influences on learning in this group may be more common than the current literature would suggest and that invertebrates may provide a useful model for understanding how learning processes based on social information evolve.     

Primary versus secondary drivers of foraging activity in sandeel schools (<Emphasis Type="Italic">Ammodytes tobianus</Emphasis>)

The commercially and ecologically valuable sandeel (Ammodytes ssp.) make distinct vertical shifts between an inactive stage, during which they seek refuge in the sand, and a pelagic schooling stage, during which they forage. This characteristic discontinuous foraging pattern constitutes a challenge to fishery biologists and has consequences for a wide range of predators ranging from birds and mammals to commercially important species. However, experimental studies that shed light on the primary drivers of foraging activity in fish are rare. In the present study, whole schools of sandeel (A. tobianus) were caught in August in east Denmark (65°02′30N; 12°37′00E) and kept in large tanks in the laboratory. It was found that the amount of food ingested and memory of past days feeding history are primary drivers of foraging activity at the level of the entire school, whereas external factors such as prey concentration and temperature are merely secondary drivers.     

Mate-choice copying by female zebra finches, <Emphasis Type="Italic">Taeniopygia guttata</Emphasis>: what happens when model females provide inconsistent information?

For a long time, mate-choice copying was thought to be restricted to lekking and polygynous species. Yet, recent experimental studies revealed that social information can play a role in the evolution of mate preferences in monogamous species with biparental care. However, this phenomenon has been demonstrated only under particular conditions and the prevalence and importance of this phenomenon therefore remains to be evaluated. In particular, previous laboratory experiments have consisted in exposing test females to only one paired male at a time, while under natural conditions monogamous females are likely to observe the choice of several females before making a decision. Thus, in the present study, female zebra finches (Taeniopygia guttata) could observe two model females simultaneously, that provided either inconsistent or consistent information, depending on whether they were interacting with different types of males or with males of a same phenotype. We found that the relative importance given to private and social information on females’ preferences varied with the consistency of social information and females significantly changed their preference only when social information was consistent. There was, nevertheless, a large variation in their responses. We suggest that such variations could be due to the fact that the benefits of mate-choice copying are frequency-dependent, and that this constrain would further contribute to limit the use of social information in monogamous species.     

The paradox of risk assessment: comparing responses of fathead minnows to capture-released and diet-released alarm cues from two different predators

Summary. Many aquatic prey are known to use chemical alarm cues to assess their risk of predation. In fishes, such alarm cues can be released either through damage of the epidermis during a predatory attack (capture-released) or through release from the predator feces (diet-released). In our study, we compared the importance of capture- versus diet-released alarm cues in risk assessment by fathead minnows (Pimephales promelas) that were na?ve to fish predators. We utilized two different fish predators: a specialized piscivore, the northern pike (Esox lucius) and a generalist predator, the brook trout (Salvelinus fontinalis). Handling time of pike consuming minnows was much shorter than for trout consuming minnows, likely resulting in less epidermal damage to the minnows during attacks by pike. In accordance with this, minnows showed a less intense antipredator response to capture-released cues from pike than capture-released cues from trout. This represents a paradox in risk assessment for the minnows as they respond to the specialized piscivore, the more dangerous predator, with a less intense antipredator response. In contrast, the minnows showed a stronger antipredator response to the specialized piscivore than to the generalist when given diet cues. This work highlights the need for researchers to carefully consider the nature of the information available to prey in risk assessment.     

Mate choice plasticity in the field cricket <Emphasis Type="Italic">Teleogryllus oceanicus</Emphasis>: effects of social experience in multiple modalities

Social experience can elicit phenotypically plastic changes in mate choice, but little is known about the degree to which social information from one modality can influence mating decisions based on information from a different modality. I used the field cricket Teleogryllus oceanicus to test whether experience of chemical cues mimicking a high density of sexually mature males causes changes in mate choice based on acoustic signals. T. oceanicus males produce long-range calling songs to attract females for mating, but they also produce waxy, non-volatile hydrocarbons on their cuticle (CHCs) which, when deposited on a substrate, can be detected by females and may provide demographic information. I manipulated female experience of substrate-bound male CHCs and then performed acoustic mate choice trials. When CHCs were present on the substrate during trials, females showed greater motivation to respond to male calling song. This effect diminished with repeated exposure to male songs, demonstrating that the importance of olfactory cues in altering acoustic mate choice decreased with increasing exposure to acoustic signals. However, the temporal nature of CHC experience mattered: previous experience of CHCs did not alter subsequent female choice for male calling song traits. Exposure to male song increased the threshold of mate acceptance over time, and individuals varied considerably in overall levels of responsiveness. Taken together, the results demonstrate that mate choice is dependent on social context mediated by multiple modalities in T. oceanicus, but they do not support the idea that prior experience of social cues in one modality necessarily influences later mating decisions based on other signalling modalities.     

Risk level of chemical cues determines retention of recognition of new predators in Iberian green frog tadpoles

In aquatic environments, many prey rely on chemosensory information from injured (alarm cues) or stressed conspecifics (disturbance cues) to assess predation risk. Alarm cues are considered as a sign of higher risk than disturbance cues. These cues could be used by prey to learn potential new predators. In this study, we tested whether Iberian green frog tadpoles (Pelophylax perezi) exhibited antipredator responses to alarm and disturbance cues of conspecifics and whether tadpoles could associate new predators with alarm or disturbance cues. Tadpoles reduced their activity in the presence of disturbance cues, but only weakly when compared with their response to alarm cues. Also, tadpoles learned to recognize new predators from association with alarm or disturbance cues. However, the period of retention of the learned association was shorter for disturbance than alarm cues. Our results indicate that tadpoles are able to modify their antipredatory behavior according to (1) the degree of risk implied by the experimental cues (2) their previous experience of chemical cues of the predator.     

Foraging behavior in early Atlantic cod larvae (Gadus morhua) feeding on a protozoan (Balanionsp.) and a copepod nauplius (Pseudodiaptomussp.)

Food limitation is likely to be a source of mortality for fish larvae in the first few weeks after hatching. In the laboratory, we analyzed all aspects of foraging in cod larvae (Gadus morhua Linnaeus) from 5 to 20 d post-hatching using protozoa (Balanion sp.) and copepod nauplii (Pseudodiaptomus sp.) as prey. A camera acquisition system with two orthogonal cameras and a digital image analysis program was used to observe patterns of foraging. Digitization provided three-dimensional speeds, distances, and angles for each foraging event, and determined prey and fish larval head and tail positions. Larval cod swimming speeds, perception distances, angles, and volumes increased with larval fish size. Larval cod swam in a series of short intense bursts interspersed with slower gliding sequences. In 94% of all foraging events prey items were perceived during glides. Larval cod foraging has three possible outcomes: unsuccessful attacks, aborted attacks, and successful attacks. The percentage of successful attacks increased with fish size. In all larval fish size classes, successful attacks had smaller attack distances and faster attack speeds than unsuccessful attacks. Among prey items slowly swimming protozoans were the preferred food of first-feeding cod larvae; larger larvae had higher swimming speeds and captured larger, faster copepod nauplii. Protozoans may be an important prey item for first-feeding larvae providing essential resources for growth to a size at which copepod nauplii are captured. Received: 20 April 1999 / Accepted: 12 January 2000     

Diet of young Atlantic bluefin tuna (<Emphasis Type="Italic">Thunnus thynnus</Emphasis>) in eastern and western Atlantic foraging grounds

Atlantic bluefin tuna (Thunnus thynnus) are highly migratory predators whose abundance, distribution, and somatic condition have changed over the past decades. Prey community composition and abundance have also varied in several foraging grounds. To better understand underlying food webs and regional energy sources, we performed stomach content and stable isotope analyses on mainly juvenile (60–150 cm curved fork length) bluefin tuna captured in foraging grounds in the western (Mid-Atlantic Bight) and eastern (Bay of Biscay) Atlantic Ocean. In the Mid-Atlantic Bight, bluefin tuna diet was mainly sand lance (Ammodytes spp., 29% prey weight), consistent with historic findings. In the Bay of Biscay, krill (Meganyctiphanes norvegica) and anchovy (Engraulis encrasicolus) made up 39% prey weight, with relative consumption of each reflecting annual changes in prey abundance. Consumption of anchovies apparently declined after the local collapse of this prey resource. In both regions, stable isotope analysis results showed that juvenile bluefin tuna fed at a lower trophic position than indicated by stomach content analysis. In the Mid-Atlantic Bight, stable isotope analyses suggested that >30% of the diet was prey from lower trophic levels that composed <10% of the prey weights based upon traditional stomach content analyses. Trophic position was similar to juvenile fish sampled in the NW Atlantic but lower than juveniles sampled in the Mediterranean Sea in previous studies. Our findings indicate that juvenile bluefin tuna targeted a relatively small range of prey species and regional foraging patterns remained consistent over time in the Mid-Atlantic Bight but changed in relation to local prey availability in the Bay of Biscay.     

Behavioral response of a generalist predator to chemotactile cues of two taxonomically distinct prey species

Chemotactile cues unintentionally left by animals can play a major role in predator–prey interactions. Specialized predators can use them to find their prey, while prey individuals can assess predation risk. However, little is known to date about the importance of chemotactile cues for generalist predators such as ants. Here, we investigated the response of a generalized predatory ant, Formica polyctena, to cues of two taxonomically distinct prey: a spider (Pisaura mirabilis) and a cricket (Nemobius sylvestris). In analogy, we studied whether crickets and spiders showed antipredator behavior in response to ant cues. When confronted with cues of the two prey species, Formica polyctena workers showed increased residence time and reduced movement speed, which suggests success-motivated searching behavior and thus increased foraging effort. The ants’ response did not differ between cues of the two prey species, coinciding with similar aggression and consumption rates of dead prey. However, the cuticular hydrocarbons, which likely resemble part of the potential cues, differed strongly between the species, with only few methyl-branched alkanes in common. This suggests that ants respond to multiple compounds left by other organisms with prey-search behavior. The two prey species, in turn, showed no detectable antipredator behavior in response to ant cues. Our study shows that ants can detect and respond to chemotactile cues of taxonomically and ecologically distinct prey species, probably to raise their foraging success. Using such chemotactile cues for prey detection may drastically increase their foraging efficiency and thus contribute to the high ecological success of ants.     

Fish feeding on mobile benthic invertebrates: influence of spatial variability in habitat associations

Patterns of habitat association and foraging were examined for a group of tropical goatfishes (family Mullidae) that feed on mobile benthic invertebrates at Lizard Island (Great Barrier Reef). All goatfish possess barbels that disturb the substratum during feeding. Foraging methods were examined for the six most common species and used in conjunction with data on habitat associations to estimate the distribution and potential impact on the benthic invertebrate assemblage of foraging-related disturbance. Particular species exhibited broad habitat associations which differed little over two surveys (January 1989, January 1990). All species showed different preferences for the substrata they foraged. Preferences for substrata exhibited by the most common reef-associated species, Parupeneus multifasciatus, differed among locations separated by 1 km, between sites 150 m apart, and between depths (shallow and deep). Habitat preferences changed with ontogeny. Based on their habitat associations and foraging preferences, species were divided into habitat generalists and specialists. Specialists associated primarily with soft sediments. Habitat generalists, such as P. multifasciatus and P. cyclostomus, are likely to have an impact on their mobile invertebrate prey that is localised, diffuse and transitory, making any experimental analysis difficult and expensive. Habitat specialists form a guild of fishes with complementary feeding modes that efficiently exploit soft sediments and are more amenable to experimental manipulation. Experiments designed to detect the impact of foraging by these fishes must be repeated at different locations and times and must account for depth differences in foraging pressure.     

Diet of the Humboldt penguin (<Emphasis Type="Italic">Spheniscus humboldti</Emphasis>) in northern and southern Chile

The diet of the Humboldt penguin (Spheniscus humboldti) was examined and compared in two colonies in Chile. Field work was conducted on Pan de Azúcar Island in northern Chile in the breeding season 1998/1999 and on the Puñihuil Islands in southern Chile over two successive breeding seasons during 1997/1998 and 1998/1999. Penguin diet was studied by stomach-pumping birds and analysed by species composition, size and mass of prey. Fish were the dominant prey item at both sites, the contribution of cephalopods and crustaceans varying between sites. The fish prey consisted predominantly of school fish, but there were clear latitudinal differences in fish prey taken. Penguins in the northern colony consumed primarily garfish (Scomberesox saurus), while birds at the southern colony of Puñihuil fed primarily on anchovy (Engraulis ringens), Araucanian herring (Strangomera bentincki) and silverside (Odontesthes regia). The results showed significant differences in terms of numbers of fish taken between the two breeding seasons at Puñihuil. In 1997/1998 penguins consumed almost exclusively anchovy, while they fed primarily on silversides in the successive year. Almost all prey, except stomatopods, were characterised as being pelagic species that occur in relatively inshore water, consistent with the foraging behaviour of Humboldt penguins. The dependence of Humboldt penguins on commercially exploited, schooling prey species makes the species particularly susceptible to changes in prey stocks, due to non-sustainable fisheries management.Communicated by O. Kinne, Oldendorf/Luhe