The costs and benefits of predator inspection behaviour in Thomson's gazelles

Summary When Thomson's gazelles (Gazella thomsoni) detect stalking predators, such as cheetahs (Acinonyx jubatus) and lions (Panthera leo), they often approach and follow the predator for up to 72 min (average 14 min). Coursing predators are rarely approached. Gazelle groups were more likely to approach cheetahs if the groups were larger, if the vegetation was low, or if the cheetahs came closer to the group. Immature gazelles were more likely to approach than adults, and a higher proportion of group members participated in inspection behaviour in small groups than in large ones. Gazelles approached closer in less risky situations: if they were in larger groups or if the vegetation was low. Inspection behaviour caused cheetahs to move further between rests and between hunting attempts. Approaching cheetahs was risky, particularly for younger gazelles (probability of being killed while inspecting a cheetah was 1 in 5000 approaches for adults and 1 in 417 approaches for half-grown/adolescent gazelles), and the risks were higher than monitoring cheetahs from a distance. The time costs of predator inspection were also considerable (less than 4.2% of daylight time budget), suggesting that the benefits must be substantial to offset these costs. The results suggested that inspection behaviour was multifunctional, causing stalking predators to move out of the vicinity, enabling gazelles to monitor the predators' movements, and providing an opportunity, particularly for younger animals, to learn about predators. By approaching, gazelles also inform predators that they have been detected and alert other gazelles to the predators' presence.     

Meta-analysis of foraging and predation risk trade-offs in terrestrial systems

Although there is ample evidence for the generality of foraging and predation trade-offs in aquatic systems, its application to terrestrial systems is less comprehensive. In this review, meta-analysis was used to analyze experiments on giving-up-densities in terrestrial systems to evaluate the overall magnitude of predation risk on foraging behavior and experimental conditions mediating its effect. Results indicate a large and significant decrease in foraging effort as a consequence of increased predation risk. Whether experiments were conducted under natural or artificial conditions produced no change in the overall effect predation had on foraging. Odor and live predators as a correlate of predation risk had weaker and nonsignificant effects compared to habitat characteristics. The meta-analysis suggests that the effect of predation risk on foraging behavior in terrestrial systems is strongly dependent on the type of predation risk being utilized.     

Predation risk affects courtship and attractiveness of competing threespine stickleback males

The effect of predation risk and male-male competition on male courtship behaviour and attractiveness to females was studied in the threespine stickleback (Gasterosteus aculeatus) by presenting dummy or live females to solitary and competing males under different predation risks. In the presence of a predator, males decreased courtship activity. Different courtship components were, however, adjusted to different extents and in opposing directions to predation risk, probably because the single components may have varied in riskiness. The presence of a competing male decreased overall courtship activity, but increased the frequency of zigzags, suggesting zigzagging to be a competitive strategy against other males. In the presence of a predator male courtship activity was not affected by a competitor. Female mate choice correlated with the males' previous frequency of zigzags towards a dummy female. However, when a live female paid attention to a male, the male decreased zigzagging and instead increased leading and fanning behaviours, probably trying to attract the female to the nest to mate. Predation risk affected the attractiveness of males as females reduced their attention to a male when he faced a predator and reduced his courtship activity. As females instead increased their attention to a competing male that had increased his courtship activity, due to decreased competition, males clearly are balancing mating opportunities against predator avoidance. When males vary in their susceptibility to predators, predation risk may thus affect mating success of competing males. Received: 31 January 1997 / Accepted after revision: 15 April 1997     

Assessment of predation risk via illumination level: facultative central place foraging in the cricetid rodent Phyllotis darwini

It is well known that the risk of predation affects prey decision making. However, few studies have been concerned with the cues used by prey to assess this risk. Prey animals may use indirect environmental cues to assess predation hazard since direct evaluation may be dangerous. I studied the assessment of predation risk, manipulated via environmental illumination level, and the trade-off between foraging and predation hazard avoidance in the nocturnal rodentPhyllotis darwini (Rodentia: Cricetidae). In experimental arenas I simulated dark and full moon nights (which in nature correlate with low and high predation risk, respectively) and measured the immediate responses of animals to flyovers of a raptor model. Second, varying illumination only, I evaluated patch use, food consumption, central place foraging, and nocturnal variation of body weight. During flyover experiments, animals showed significantly more evasive reactions under full moon illumination than in moonless conditions. In the patch use experiments, rodents significantly increased their giving-up density and decreased their total food consumption under moonlight. On dark nights, rodents normally fed in the food patch, but when illumination was high they became central place foragers in large proportion. Moreover, the body weight of individuals decreased proportionately more during bright nights. These results strongly suggest thatP. darwini uses the level of environmental illumination as a cue to the risk of being preyed upon and may sacrifice part of its energy return to avoid risky situations.     

Effects of predation risk and hunger on the behaviour of two species of tadpoles

Predation and hunger are threats for most organisms, and appropriate behavioural responses to both factors should be shaped by natural selection. In combination, however, the behavioural demands of predation avoidance and effective foraging often cannot be satisfied at the same time and lead to a conflict within organisms. We examined the behavioural responses of two closely-related species of tadpoles, Rana lessonae and R. esculenta, to simulated predation by fish and hunger. Tadpoles, hatched and reared in the laboratory, were tested in a three-way factorial (predation risk × hunger × species) experiment with four predation levels and four hunger levels. Both species decreased their swimming activity with increasing predation risk. Predation risk did not influence the amount of activity time invested in feeding but caused the tadpoles to spend less time in patches with food. Refuges were not used to avoid predation. R. esculenta was more sensitive to predation risk than R. lessonae. Hunger increased both the activity of tadpoles and the amount of activity time invested in feeding, thus indicating an increased energy intake. No interactions were observed between predation risk and hunger. These results show that tadpoles possess genetically-based behavioural mechanisms that allow them to respond in a graded manner to predation and hunger. However, they did not balance the two conflicting demands of predation avoidance and effective foraging; the two mechanisms appeared to act independently. Correspondence to: R.D. Semlitsch     

Migratory fuelling in blackcaps (Sylvia atricapilla) under perceived risk of predation

It has been argued that the body mass levels achieved by birds are determined by the trade-off between risks of starvation and predation. Birds have also been found to reduce body mass in response to an increased predation risk. During migration, the need of extra fuel for flights is obvious and crucial. In this study, migratory blackcaps (Sylvia atricapilla) were subject to an experimental stopover situation where the predation risk was manipulated by exposure to a stuffed predator. Blackcaps that perceived an imminent risk of predation increased their food intake and fuel deposition rate during the first period of stopover compared with a control group. The pattern of night activity indicates that birds that were exposed to the predator also chose to leave earlier than birds in the control group. Since there was no cover present at the stopover site, birds might have perceived the risk of predation as higher regardless of whether they were foraging or not. Under such circumstances it has been predicted that birds should increase their foraging activity. The findings in this study clearly indicate that birds are able to adjust their stopover behaviour to perceived predation risk. Received: 8 January 1997 / Accepted after revision: 11 April 1997     

Male-male competition ensures honest signaling of male parental ability in the three-spined stickleback (Gasterosteus aculeatus)

The importance of socially imposed costs for the evolution and maintenance of honest sexual signals has received less attention than other costs. Here I show that male-male competition can increase the honesty of sexual signaling in relation to male parental ability in a species with flexible signaling. When four three-spined stickleback (Gasterosteus aculeatus) males were allowed to court a female first separately and then in competition, red nuptial coloration under competition reflected male parental ability more accurately than red coloration when separated. Parental ability was determined as the ability of the male to raise a clutch of eggs to the hatching stage under interaction with other breeding and non-breeding males. The increased honesty under competition was probably due to subordinate males of poor parental ability decreasing their color expression under interaction to reduce the risk of fights with superior males. However, socially imposed costs of signaling were probably not the main factors maintaining honest signaling, as red coloration reflected male parental ability also in the absence of competition, although less accurately. Nevertheless, the small-scale differences that male-male competition induced can significantly facilitate adaptive female choice and have large impacts on sexual selection. Received: 7 July 2000 / Revised: 31 August 2000 / Accepted: 4 September 2000     

Subhabitat selection by foraging threespine stickleback (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>): previous experience and social conformity

Any mechanism that allows animals to increase their foraging efficiency is likely to be selected for, including the ability to learn to recognise and subsequently discriminate between habitat types based on their profitability. In a series of laboratory studies, we manipulated prey densities across two different experimental subhabitats and demonstrated that threespine stickleback (Gasterosteus aculeatus) can develop foraging preferences for subhabitats that have previously yielded prey. Fish were not recalling the spatial location of prey patches; rather, they were discriminating between subhabitats based on foraging experience there and allocating foraging effort accordingly. Foraging preferences took around 14 days to develop, and once established, they persisted independently of experimental prey density, suggesting that fish were using experience rather than real-time sampling to select foraging grounds. When we presented focal fish with social information cues, we found that they preferentially used local enhancement and current public information cues when they conflicted with previous experience, but that they did not use prior public information. This suggests that in the presence of conspecifics, individuals prioritise social conformity over the use of private information. We discuss our results in the context of optimal foraging and the trade-offs associated with balancing conflicting private and social information.     

Feeding and aggressive behaviours in juvenile coho salmon (Oncorhynchus kisutch) under chemically-mediated risk of predation

Summary Juvenile coho salmon (Oncorhynchus kisutch) spend the first year of their lives in their natal streams, where they may often hold feeding territories. They also face significant risk of predation by birds and fish, and should alter their behaviour to reduce risk of mortality when these predators are present. Although there is laboratory evidence that coho react to predator visual stimuli, chemoreception of avian predator presence has not previously been reported. We tested the influence of chemical stimuli of common merganser (Mergus merganser), preying on juvenile coho, on two aspects of coho territorial behaviour, foraging and aggression, in flow-through aquaria. After a mixture of merganser- and coho-conditioned water was introduced into the system, juvenile coho significantly reduced their attack distance on drifting prey. The fish also significantly decreased their aggressive behaviour directed towards mirrors (total number of acts, intensity of acts and time spent) when the same odour was present. They did not change their behaviour in either experiment after control introductions of water treated with fish alone. These results are interpreted within the framework of a trade-off between juvenile growth and mortality.     

Disentangling the effects of group size and density on shoaling decisions of three-spined sticklebacks (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>)

Many animals live in groups most of their life. One function of this behaviour is an increased predator protection whereas larger groups provide better protection than smaller ones. A causal explanation is that due to a higher number of shoal members the individual risk of being predated will decrease (“dilution effect”). Additionally, shoaling leads to increased predator confusion. This “confusion effect” can be strengthened by an increased group density, which often correlates with group size. Many studies found that individuals prefer the larger of two groups. However, whether this preference is due to a larger group size or because of an increased density of the larger group remained unclear. To disentangle these factors we gave three-spined sticklebacks (Gasterosteus aculeatus) the choice between shoals of (1) different group size and density, (2) different group size, but equal density and (3) equal group sizes, but different densities. As expected, test fish preferred the larger and denser shoal over the smaller, less dense one. This preference was lost when shoal size differed but density was kept constant. When shoal size was equal but density differed, test fish preferred the less dense shoal. However, this was only the case when test fish chose between two relatively dense shoals. On the other hand, when overall density was low, test fish did not discriminate between shoals of different densities. This result may be explained in terms of predator avoidance. The results show that shoaling preferences might not always be influenced by a higher number of group members but also by the density and cohesiveness of the respective groups. An erratum to this article can be found at     

Heritable variation in learning performance affects foraging preferences in the honey bee (Apis mellifera)

There has now been an abundance of research conducted to explore genetic bases that underlie learning performance in the honey bee (Apis mellifera). This work has progressed to the point where studies now seek to relate genetic traits that underlie learning ability to learning in field-based foraging problems faced by workers. Accordingly, the focus of our research is to explore the correlation between laboratory-based performance using an established learning paradigm and field-based foraging behavior. To evaluate learning ability, selected lines were established by evaluating queens and drones in a proboscis extension reflex (PER) conditioning procedure to measure learning in a laboratory paradigm—latent inhibition (LI). Hybrid queens were then produced from our lines selected for high and low levels of LI and inseminated with semen from many drones chosen at random. The genetically diverse worker progeny were then evaluated for expression of LI and for preference of pollen and/or nectar during foraging. Foragers from several different queens, and which had resulted from fertilization by any of several different drone fathers, were collected as they returned from foraging flights and analyzed for pollen and nectar contents. They were subsequently evaluated for expression of LI. Our research revealed that pollen foragers exhibited stronger learning, both in the presence (excitatory conditioning) and absence (LI) of reinforcement. The heightened overall learning ability demonstrated by pollen foragers suggests that pollen foragers are in general more sensitive to a large number of environmental stimuli. This mechanism could contribute toward explanations of colony-level regulation of foraging patterns among workers.Communicated by R. Page     

Variable predation risk and the dynamic nature of mosquito antipredator responses to chemical alarm cues

Summary. Predation is a pervasive selective agent highly variable in space and time. Due to the costs associated with antipredator responses, prey would be at a selective advantage if they respond to predation threats with an intensitfy matching the threat posed by the predator. Many aquatic organisms have been shown to use chemical alarm cues present in the water to assess the level of risk in their environment. This includes mosquito larvae which show antipredator responses to conspecific alarm cues. In this study, we investigated the nature of the responses of larval mosquitoes Culex restuans to those cues. In our initial observations, we showed pond/population differences in the response intensity of C. restuans to alarm cues. In experiment 1, we showed that the response intensity to alarm cues could be increased by increasing the background level of risk in the mosquitoes’ environment (by adding salamander predators) and once turned on, the response intensity to alarm cues was likely maintained for the remainder of the mosquitoes’ aquatic life. In experiments 2 and 3, we investigated if the increase in response intensity to alarm cues was directly correlated with the level of background risk in the mosquitoes’ environment. When given increasing levels of background risk, mosquito larvae subsequently showed a graded response to conspecific alarm cues. This series of experiments demonstrates that the response intensity of larval mosquitoes to a standard concentration of alarm cues is not fixed, but rather dependent on the background level of risk in the environment. An understanding of the background level of risk is particularly important for comparing antipredator responses of prey between habitats.     

Bright plumage in the magpie: does it increase or reduce the risk of predation?

Conspicuous color patterns in birds may lead to increased risk of predation. Alternatively, bright birds may be aposematic or unprofitable prey, which leads to decreased predation. During four autumns, I examined whether the black-and-white plumage of (stuffed) magpies Pica pica increases or reduces the risk of attack by migrating goshawks Accipiter gentilis. Attack risk was higher for normal magpies than for cryptic, brown magpies whether the mounts were placed near one another or far apart. However, the brown magpie may have been avoided because of its novelty. For magpies and cryptic jays Garrulus glandarius exposed together, the attack risk was similar. In 2 years, magpie and jay mounts were also exposed far apart. In 1994, with an invasion of migrating jays, attack risk was much higher for jays than for magpies. In 1995, with a normal density of jays, hawks attacked the magpies more often. The results demonstrate frequency-dependent prey selection by goshawks, which would influence any predation cost of bright plumage. The attacks on normally colored magpie mounts suggest that magpies are not aposematic. Trials with photographs and human observers indicated that normal magpies were somewhat easier to detect than jays. The plumage of the magpie possibly increases the risk of predation, but may be favoured by sexual or social selection. Received: 18 January 1996 / Accepted after revision: 6 October 1996     

The effects of size-dependent predation risk on the interaction between behavioral and life history traits in a stream-dwelling isopod

In field surveys, laboratory observations and field-based assays of behavior, I examined the effects of size-dependent predation risk on the interaction between size at reproductive maturity and maternal care behavior in the stream-dwelling isopod, Lirceus fontinalis. L. fontinalis exhibit population-specific sizes at reproductive maturity which result in population differences in predation risk during the adult phase. Females from streams containing salamander larvae (that prefer small prey) mature at large sizes and then become relatively safe from predation. Females from streams containing fish (that consume all size classes of prey equally) mature at small sizes and remain at risk. I tested whether these differences in expected survival were reflected in the behavior of females during the maternal phase (i.e., the period during which females exhibit maternal care). Female L. fontinalis carry developing juveniles inside a brood pouch. I simulated predatory attacks on gravid female L. fontinalis from the different population types and found that female behavior correlated with population differences in risk. When “attacked”, females from streams with predatory fish (that experience high risk to adult females) released juveniles from the brood pouch, whereas females from populations with predatory salamander larvae (that pose relatively little risk to adult females) did not release juveniles. I discuss the results with reference to the joint evolution of behavioral and life history traits. Received: 6 March 1996 /Accepted after revision: 12 August 1996     

The role of internal and external information in foraging decisions of Melipona workers (Hymenoptera: Meliponinae)

Social insect foragers have to make foraging decisions based on information that may come from two different sources: information learned and memorised through their own experience (“internal” information) and information communicated by nest mates or directly obtained from their environment (“external” information). The role of these sources of information in decision-making by foragers was studied observationally and experimentally in stingless bees of the genus Melipona. Once a Melipona forager had started its food-collecting career, its decisions to initiate, continue or stop its daily collecting activity were mainly based upon previous experience (activity on previous days, the time at which foraging was initiated the day(s) before, and, during the day, the success of the last foraging flights) and mediated through direct interaction with the food source (load size harvested and time to collect a load). External information provided by returning foragers advanced the start of foraging of experienced bees. Most inexperienced bees initiated their foraging day after successful foragers had returned to the hive. The start of foraging by other inexperienced bees was stimulated by high waste-removal activity of nest mates. By experimentally controlling the entries of foragers (hence external information input) it was shown that very low levels of external information input had large effect on the departure of experienced foragers. After the return of a single successful forager, or five foragers together, the rate of forager exits increased dramatically for 15 min. Only the first and second entry events had large effect; later entries influenced forager exit patterns only slightly. The results show that Melipona foragers make decisions based upon their own experience and that communication stimulates these foragers if it concerns the previously visited source. We discuss the organisation of individual foraging in Melipona and Apis mellifera and are led to the conclusion that these species behave very similarly and that an information-integration model (derived from Fig. 1) could be a starting point for future research on social insect foraging. Received: 16 April 1997 / Accepted after revision: 30 August 1997     

Female behaviour mediates male courtship under predation risk in the guppy (Poecilia reticulata)

Previous work has shown that under elevated predation risk, male guppies (Poecilia reticulata) switch from courtship to less conspicuous coercive mating attempts. This behavioural transition is traditionally interpreted as a 'risk-sensitive' response that makes males less conspicuous to predators. However, predation risk leads to behavioural changes (such as schooling and predator inspection) in females that may result in coercive mating attempts being more profitable in high-risk situations. Here, we tested the hypothesis that the switch to coercive mating by male guppies in high-risk situations is mediated by adjustments in female behaviour, rather than directly by the predator. We used replicate models resembling a known guppy predator to simulate predation risk in wild-caught guppies from a high-predation population in Trinidad. Our results revealed that males performed proportionately more coercive mating attempts when presented with a female that had been exposed previously to a model predator compared to when males were paired with non-exposed females. Total mating activity (combined rates of courtship and forced mating attempts) did not differ significantly among the two treatment groups, indicating that overall mating activity is unaffected by predation risk. Importantly, when we subsequently presented both sexes concurrently with a predator model, total mating activity and the proportion of forced mating attempts remained unchanged in the high-risk treatment. Taken together, these results indicate that the transition from courtship to forced mating attempts under elevated predation risk is mediated by changes in female behaviour, which we suggest may favour the use of coercive mating under high predation risk.     

Shifting foraging strategies in colonies of the social wasp Polybia occidentalis (Hymenoptera, Vespidae)

Social insect colonies can be expected to forage at rates that maximize colony fitness. Foraging at higher rates would increase the rate of worker production, but decrease adult survival. This trade-off has particular significance during the founding stage, when adults lost are not replaced. Prior work has shown that independent-founding wasps rear the first workers rapidly by foraging at high rates. Foraging rates decrease after those individuals pupate, presumably reducing the risk of foundress death. In the swarm-founding wasps, colony-founding units have many workers, making colony death by forager attrition less likely. Do swarm-founding wasps show similar shifts in foraging rates during the founding stage? We measured foraging rates of the swarm-founding wasp, Polybia occidentalis at four stages of colony development. At each stage, foraging rates correlated with the number of larvae present, which, in the founding stages, correlated with the number of cells in the new nest. Thus, foraging rates appear to be demand-driven, with the level of demand in the founding stage set by the size of nest that is constructed. During the founding stage, foraging rates per larva were high initially, suggesting that colonies minimize the development times of larvae early in the founding stage. Later in the stage, foraging rates decreased, which would reduce worker mortality until new workers eclose. This pattern is similar to that shown for independent-founding wasps and likely results from conflicting pressures to maximize colony growth and minimize the risk of colony death by forager attrition.     

The behavioural basis of a species replacement: differential aggresssion and predation between the introduced Gammarus pulex and the native G. duebeni celticus (Amphipoda)

Previous studies have shown that differential predation by males on moulted female congenerics may be largely responsible for the elimination and replacement of the native Irish freshwater amphipod Gammarus duebeni celticus by the introduced G. pulex. Predation of moulted females occurs both shortly after their release from precopulatory mate-guarding and whilst they are being guarded by their mates. In the present study, two hypotheses concerning the underlying cause(s) of the differential predation pattern are tested. Firstly, female G. d. celticus may be more vulnerable to predation than female G. pulex due to the former being released from precopula guarding with the new exoskeleton in a less hardened state. Secondly, G. pulex may be an inherently more aggressive species than G. d. celticus during predatory interactions over guarded females. The first experiment indicated that differential predation was not mediated by species differences in the state of the female exoskeleton at the time of release from precopula by guarding males. The second experiment, however, showed that male G. pulex were significantly more aggressive than male G. d. celticus in attacking both guarding male congenerics and guarded moulted female congenerics. In addition, in defence against predatory attacks, paired male and female G. pulex were significantly more aggressive than paired male and female G. d. celticus. These differences in aggressive behaviour led to a significantly higher frequency of predation on G. d. celticus females than on G. pulex females, and also explains this finding in previous studies. It is concluded that differential predation due to differences in aggressive behaviour may explain the pattern of replacement between these species.     

Social cohesion and foraging decrease with group size in fallow deer (Dama dama)

We studied the impact of group size on foraging behaviour and level of movement synchronisation among female herdmates of a fallow deer population in Central Italy. Both proportion of foraging events and movement synchronisation decreased with increasing group size. The proportion of foraging events was higher for animals on the edge of the group than for deer in the centre of the group; hence, there appears to be a trade-off between protection against predators and foraging interference, both of which decrease from the centre to the periphery of the group. This is the first time this type of behaviour has been recorded for wild ungulates. As expected, we also found that the movement of peripheral animals was less synchronised than that of central animals. Consequently, peripheral animals may lose contact with their herdmates and split off the group. We conclude that social inequalities may lead to conflicting requirements among group members and instability of large groups. Movement synchronisation (as a function of group size) appears to interact with habitat openness to produce variations of group size (which appear to be adaptive for individuals) as an emergent property of these aggregations.     

Threat-sensitive feeding strategy of immature sticklebacks (Gasterosteus aculeatus) in response to recent experimental infection with the cestode Schistocephalus solidus

Threat-sensitive decision-making might be changed in response to a parasitic infection that impairs future reproduction. Infected animals should take more risk to gain energy to speed up their growth to achieve early reproduction and/or to strengthen their immune response. To avoid correlational evidence, we experimentally infected and sham-infected randomly selected immature three-spined sticklebacks with the cestode Schistocephalus solidus. For 7 weeks we determined the threat-sensitive foraging decisions and growth of individual sticklebacks in the presence of a live pike (Esox lucius). The experimenters were blind with respect to the infection status of the fish. In contrast to previous studies, our recently infected fish should have been almost unconstrained by the parasite and thus have been able to adopt an appropriate life history strategy. We found a strong predator effect for both infected and uninfected fish: the sticklebacks’ risk-sensitive foraging strategy resulted in significantly reduced growth under predation risk. Infected fish did not grow significantly faster under predation risk than uninfected fish. Since infected fish consumed much less prey in the presence of the predator than did infected fish in its absence, they obviously did not use the opportunity to maximize their growth rate to reach reproduction before the parasite impairs it. Received: 21 June 1999 / Revised: 27 November 1999 / Accepted: 5 September 2000