Hunger-dependent predator inspection and foraging behaviours in the threespine stickleback (Gasterosteus aculeatus) under predation risk

Individual fish commonly leave the relative safety of the shoal to approach potential predators at a distance. Not all members of a shoal are equally likely to initiate such predator inspection visits. Here, we show for the first time that the current hunger state of individual fish strongly influences their predator inspection behaviour, as well as their foraging rate, in the face of predation hazard. When all members of threespine stickleback (Gasterosteus aculeatus) test shoals were in a similar hunger state, they were equally likely to inspect a trout predator model alone and did not differ in the frequency of their inspection visits or foraging rate. However, when individual sticklebacks in a shoal differed in their hunger state, the food-deprived (i.e. hungrier) member of the shoal fed at a higher rate, was significantly more likely to initiate solitary predator inspection visits, and inspected the predator model significantly more often than its less hungry (i.e. well-fed) shoal mates. Individual fish which inspected the predator model more frequently also tended to have higher feeding rates. The results indicate that the hungrier fish in a shoal are more willing to take greater risks to inspect a potential threat at a distance, compared with their well-fed shoal mates, and suggest that they may gain a foraging benefit in doing so. If marked asymmetries in hunger state exist among members of fish shoals, then mutual cooperation during predator inspection visits may be difficult to achieve because well-fed individuals are not as likely to initiate or participate in inspection visits as are hungry individuals.Correspondence to: J.-G.J. Godin     

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.     

Effects of stream hydraulic conditions on foraging strategies of false dace, Pseudorasbora parva, in the lentic ecosystem

The effects of current velocity on the foraging behavior of false dace, Pseudorasbora parva, were examined in a zero velocity (stagnant) condition, and at four flow rates (5, 7, 11 and 16 cm per second). In stagnant water, the fish displayed a cruise-searching pattern, but they used a drift-feeding foraging tactic in flowing water. The shape of the transverse field of reaction field was elliptical in the stagnant condition, whereas their downward regions were restricted under the flowing conditions. The fish had a blind spot oriented directly in front of their reaction field. Although the relative swimming speed (with considering the against current velocity) increased with increasing flow velocity, the absolute search speed (ignore the against current velocity) showed about 1.2 fish body length per second at stagnant water and low flow velocity. The results of feeding rates showed stop-and wait (driff-feeding) foraging strategy is more efficient in flowing water because prey drift directly towards the fish and prey easily detected.     

Prey ecology and behaviour affect foraging strategies in the Great Cormorant

The fine link between a particular dive pattern and a specific prey item represents a challenging task in the analysis of marine predator–prey relationships. There is growing evidence that prey type affects diving seabirds’ foraging strategies, dive shapes and underwater activity costs. This study investigates whether a generalist diver, the Great Cormorant Phalacrocorax carbo, modifies the time budget allocated to prey-capture behaviour and breathing strategies (reactive vs. anticipatory) with respect to the prey type (pelagic vs. benthic). Video recordings of 91 Great Cormorants show how the ecology and behaviour of their main prey, Mullets (Mugilidae) and Flounders Platichthys flesus, affect dive/surface durations and the diving pattern. The demersal habit and the low mobility of Flounders leads to an easy access to prey with an anticipatory strategy. Moreover, the patchy distribution of this fish species increases prey-capture rates. Conversely, Mullets exploit the whole water column and are highly mobile, and this is reflected in the need of performing two sequential dives to capture a prey, both longer and likely more expensive, with a consequent switch of strategy from reactive in the searching phase to anticipatory breathing during prey-capture events. This study provides evidence that a generalist diver may switch between different foraging strategies, and it shows how each of them may be optimal under particular ecological conditions. These constraints influence the dynamics that operate within the marine food chains and have relevant implications in managing lagoon areas, including fish ponds.     

Reward rate and forager activation in honeybees: recruiting mechanisms and temporal distribution of arrivals

We analyzed the foraging and recruitment activity of single foragers ( Apis mellifera), exploiting low reward rates of sucrose solution. Single employed foragers (test bees) were allowed to collect 2.0 m sucrose solution delivered by a rate-feeder located at 160 m from the hive for 2 h. Flow rates varied between 1.4 and 5.5 µl/min. The individual behavior of the test bees was registered both at the hive and the food source, and the social output was calculated as the number of incoming bees arriving at the feeder per hour (henceforth: arrival rate). Incoming bees were captured once they landed at the feeder and assigned to one of three categories according to their foraging experience and hive interactions with the test bee: inspector, reactivated, or inexperienced bees. Both the waggle-runs performed per hour of foraging by test bees and the social output attained, increased with the reward rate. Also the number of hive-stays and the trophallactic-offering contacts performed by test bees were positively correlated with the arrival rate. For the highest reward rates, the duration of Nasonov-gland exposure at the feeding place was higher, and the arrival of most of the incoming bees occurred shortly after the test bee landed at the feeding platform. Thus, in addition to hive-interactions, landing of incoming bees at the food source is promoted by olfactory and/or visual information provided by the test bees. The proportions of inspector, reactivated, and inexperienced bees changed depending on the reward rate offered. Therefore, not only the occurrence and intensity of the recruitment-related behaviors performed by the test bees, but also the stimulation required by each category of incoming bees, determined the social output observed.     

Female foraging and male vigilance in white-tailed ptarmigan (Lagopus leucurus): opportunism or behavioural coordination?

For several species of birds, high rates of male vigilance are correlated with high rates of female foraging. This relationship is thought to ultimately result in higher reproductive success for females paired with highly vigilant males. However, previous research has not examined the behavioural mechanism that produces the correlation between male vigilance and rates of female foraging. Foraging females may take advantage of vigilance that males are using for other purposes. Alternatively, the purpose of male vigilance may be to increase females' ability to forage. We examined these alternatives by testing whether vigilance preceded or followed bouts of female foraging more often than would occur by chance alone, using simultaneous behaviour observations of pre-incubation pairs of white-tailed ptarmigan (Lagopus leucurus). Our results indicate that each member of a pair may influence the behaviour of the other. Females were more likely to initiate foraging bouts after males became vigilant than if their mate remained non-vigilant. Moreover, non-vigilant males were more likely to become vigilant if their mate was foraging than if she was engaged in some other activity. Despite the possibility that a sexual conflict exists as each member of a pair attempts to maximize its fitness, both sexes behave as though a major role of male vigilance is to enhance female foraging opportunities. Received: 3 May 1999 / Received in revised form: 14 June 1999 / Accepted: 16 June 1999     

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     

Estimation of scavenger abundance and distance of attraction to bait

Patterns of arrival, times of first arrival on bait, and instantaneous numbers of animals on bait may be used to estimate abundance and distance of attraction for scavenging species of fish and invertebrates. A simple Gaussian odour plume model, which takes into account the rate of odour production by bait, chemosensory threshold of scavengers, swimming speed of scavengers relative to current velocity, and satiation time, was used. Scavengers are assumed to be stationary and randomly or evenly distributed prior to detecting odour, and presumably respond immediately to odour. Calculations with the model are made with new and published data for various fish and the parameters and assumptions which are critical to the model.     

Risk-prone hunting by chimpanzees (<Emphasis Type="Italic">Pan troglodytes schweinfurthii</Emphasis>) increases during periods of high diet quality

Most studies suggest that during times of nutritional stress, an animal faced with two foraging choices should follow a risk-prone strategy, choosing the option with highest payoff variance. This “scarcity/risk” hypothesis was developed to account for the foraging patterns of small animals with high metabolic rates susceptible to the threat of starvation. In this paper, we propose that animals should also be risk-prone when their diet quality is particularly high, far exceeding that which is needed to survive. Under these circumstances, the costs of experiencing a low or negative payoff can easily be recouped. We suggest that large-bodied omnivores are most likely to adopt this “abundance/risk” strategy. We investigate this question among wild chimpanzees (Pan troglodytes) that choose between a risk-averse strategy of feeding on plant material and a risk-prone strategy of hunting red colobus monkeys. Using 14 years of data on the Kanyawara chimpanzees of Kibale National Park, Uganda, we find strong evidence that chimpanzees follow the “abundance/risk” strategy. Both hunting rate (hunts/100 observation hours) and the probability of hunting upon encountering red colobus monkeys were positively correlated with seasonal consumption of ripe drupe fruits, a class of preferred food associated with elevated reproductive performance by females. Critically, these results remained statistically significant after controlling for the potentially confounding effects of male chimpanzee party size and the presence of sexually receptive females. These findings suggest that the relationship between risk-sensitive foraging and diet quality depends upon the daily probability of starvation, the number of alternative foraging strategies, and the degree to which diet quality satisfies an animal’s nutritional requirements.     

Geographical variation in the behaviour of a central place forager: Antarctic fur seals foraging in contrasting environments

Foragers show adaptive responses to changes within their environment, and such behavioural plasticity can be a significant driving force in speciation. We investigated how lactating Antarctic fur seals, Arctocephalus gazella, adapt their foraging within two contrasting ecosystems. Location and diving data were collected concurrently, between December 2003 and February 2004, from 43 seals at Bird Island, where krill, Euphausia superba, are the main prey, and 39 at Heard Island, where mostly fish are consumed. Seals at Heard Island were shorter and lighter than those at Bird Island and they spent longer at sea, dived more frequently and spent more time in the bottom phase of dives. Generalized additive mixed effects models showed that diving behaviours differed between the islands. Both populations exploited diel vertically migrating prey species but, on average, Heard Island seals dived deeper and exceeded their estimated aerobic dive limits. We propose that the recovery of the Heard Island population may be limited by the relative inaccessibility and scarcity of food, whereas at Bird Island, the presence of abundant krill resources helps sustain extremely high numbers of seals, even with increased intra- and inter-specific competition. Both populations of fur seals appear to be constrained by their physiological limits, in terms of their optimal diving behaviour. However, there does appear to be some flexibility in strategy at the level of trip with animals adjusting their time at sea and foraging effort, in order to maximize the rate of delivery of energy to their pups.     

Behavioural inertia places a top marine predator at risk from environmental change in the Benguela upwelling system

In variable environments, organisms are bound to track environmental changes if they are to survive. Most marine mammals and seabirds are colonial, central-place foragers with long-term breeding-site fidelity. When confronted with environmental change, such species are potentially constrained in their ability to respond to these changes. For example, if environmental conditions deteriorate within their limited foraging range, long-lived species favour adult survival and abandon their current breeding effort, which ultimately influences population dynamics. Should poor conditions persist over several seasons, breeding-site fidelity may force animals to continue breeding in low-quality habitats instead of emigrating towards more profitable grounds. We assessed the behavioural response of a site-faithful central-place forager, the Cape gannet Morus capensis, endemic to the Benguela upwelling system, to a rapid shift in the distribution and abundance of its preferred prey, small pelagic shoaling fish. We studied the distribution and the abundance of prey species, and the diet, foraging distribution, foraging effort, energy requirements, and breeding success of gannets at Malgas Island (South Africa) over four consecutive breeding seasons. Facing a rapid depletion of preferred food within their foraging range, Cape gannets initially increased their foraging effort in search of their natural prey. However, as pelagic fish became progressively scarcer, breeding birds resorted to scavenging readily available discards from a nearby demersal fishery. Their chicks cannot survive on such a diet, and during our 4-year study, numbers of breeding birds at the colony decreased by 40% and breeding success of the remaining birds was very low. Such behavioural inflexibility caused numbers of Cape gannets breeding in Namibia to crash by 95% following over-fishing of pelagic fish in the 1970s. In the context of rapid environmental changes, breeding-site fidelity of long-lived species may increase the risk of local or even global extinction, rendering these species particularly vulnerable to global change.     

Shoal composition, body size and foraging in sticklebacks

Individuals which deviate from the majority in groups are likely to be most vulnerable to predation. This oddity effect, by definition, is frequency dependent, eventually fading at equal frequencies of the phenotypes in a group. It has been hypothesized that the increased predation risk of odd individuals may play an important role in the formation of phenotypically uniform shoals of fish. However, recent work has indicated that individuals may experience, or value, their predation hazard differently depending on their own size in relation to that of other group members: single large fish, but not small ones, appear concerned about their oddity in a shoal. Here I show that the apparent wariness of large fish is also expressed in a frequency-dependent manner, closely conforming to what is predicted if the oddity effect is responsible for their behavior. Using foraging activity of individuals as a means to evaluate their predation risk, I demonstrate with shoals comprising 12 threespine sticklebacks (Gasterosteus aculeatus) that large fish forage least actively when in a shoal consisting of 2 large and 10 small fish. An increase in the number of large fish to 4 among 8 small individuals clearly results in an increase in their foraging activity. However, having reached an equal frequency with small fish in a shoal, large fish do not seem to change their foraging activity much even when their number in a shoal increases further. In contrast, foraging activity of small sticklebacks remains fairly constant throughout the entire range of tested shoal compositions, providing further evidence that small and large fish respond to their oddity differently. Received: 12 February 1998 / Accepted after revision: 7 May 1998     

Chinstrap penguins alter foraging and diving behavior in response to the size of their principle prey, Antarctic krill

Penguins may exhibit plasticity in their diving and foraging behaviors in response to changes in prey availability. Chinstrap penguins are dependent predators of Antarctic krill in the Scotia Sea region, but krill populations have fluctuated in recent years. We examined the diet of chinstrap penguins at Livingston Island, South Shetland Islands, in relation to their diving and foraging behavior using time-depth recorders over six breeding seasons: 2002–2007. When krill were smaller, more chinstrap penguins consumed fish. In these years, chinstrap penguins often exhibited a shift to deep dives after sundown, and then resumed a shallower pattern at sunrise. These night dives were unexpectedly deep (up to 110 m) and mean night dive depths sometimes exceeded those from the daytime. The average size of krill in each year was negatively correlated to mean night dive depths and the proportion of foraging trips taken overnight. Based on these patterns, we suggest that when krill were small, penguins increasingly targeted myctophid fish. The average krill size was negatively correlated to the time chinstrap penguins spent foraging which suggests that foraging on smaller krill and fish incurred a cost: more time was spent at sea foraging.     

Gulls and plovers: age-related differences in kleptoparasitism among black-headed gulls (Larus ridibundus)

Summary Kleptoparasitic attacks by adult and first winter (immature) black-headed gulls in flocks of lapwings (Vanellus vanellus) were compared. Attacks by immatures were less successful because they were more likely to be mistimed and detected by the target and immatures were apparently less selective in launching long distance attacks and choosing vantage points within flocks. As a result of their reduced success rate immature gulls tended to attack more often and were more likely to adopt other foraging techniques. There is some evidence that lapwings responded differentially to the arrival of adult and immature gulls. The success rate of attacks by immatures increased through the winter and immatures were correspondingly more likely to be encountered as kleptoparasites later in the season. Nevertheless success and intake rates among immatures did not increase to those among adults even by the end of the winter.     

Variations in mortality of a coral-reef fish: links with predator abundance

The mortality rates of a pomacentrid Acanthochromis polyacanthus were examined in relation to the abundance of large predatory fish (>200 mm total length, TL) at two spatial scales. Survivorship was negatively related to patterns of predator abundance at a large spatial scale (hundreds of metres) over 3 yr, but not at a small spatial scale (tens of metres) over 2 yr. On the large scale, mortality was consistently greater (14 to 30%) in locations where there were greater numbers of predators, and lower in locations where predators occurred in smaller numbers. Among these locations, spatial differences in rank abundance of surviving juveniles were primarily due to mortality, whereas temporal differences in rank abundance were primarily due to initial juvenile abundance. These data suggest that impacts of large predatory fish were likely to have been greater in space than time and at the large spatial scale than the small spatial scale.     

Intracolonial genetic diversity in honeybee (<Emphasis Type="Italic">Apis mellifera</Emphasis>) colonies increases pollen foraging efficiency

Multiple mating by honeybee queens results in colonies of genotypically diverse workers. Recent studies have demonstrated that increased genetic diversity within a honeybee colony increases the variation in the frequency of tasks performed by workers. We show that genotypically diverse colonies, each composed of 20 subfamilies, collect more pollen than do genotypically similar colonies, each composed of a single subfamily. However, genotypically similar colonies collect greater varieties of pollen than do genotypically diverse colonies. Further, the composition of collected pollen types is less similar among genotypically similar colonies than among genotypically diverse colonies. The response threshold model predicts that genotypic subsets of workers vary in their response to task stimuli. Consistent with this model, our findings suggest that genotypically diverse colonies likely send out fewer numbers of foragers that independently search for pollen sources (scouts) in response to protein demand by the colony, resulting in a lower variety of collected pollen types. The cooperative foraging strategy of honeybees involves a limited number of scouts monitoring the environment that then guide the majority of foragers to high quality food sources. The genetic composition of the colony appears to play an important role in the efficiency of this behavior.     

Effects of energy requirements and worker mortality on colony growth and foraging in the honey bee

Summary A model of colony growth and foraging in the honey bee (Apis mellifera L.) is presented. It is assumed that summer workers choose a foraging strategy that maximizes colony population by the end of the season subject to the constraint that enough nectar has been stored to sustain the adult population overwinter. The optimal foraging strategy is derived with respect to the number of flowers visited during one foraging trip. A forager that visits many flowers collects a substantial amount of nectar but the probability that the worker returns alive from the excursion decreases accordingly. Using dynamic modelling, I explore the effects on colony growth of colony population, colony energy requirements and mortality rate while foraging. The model shows that when the expected rate of increase in nectar reserves is low, for instance in small colonies or when mortality rate rises rapidly with foraging intensity, workers collect more nectar during each foraging trip. The increase in foraging activity is realized at the expense of colony growth. The main finding is that depending on colony status the foraging strategy that maximizes worker population implies visits to almost any number of flowers. This is in sharp contrast to predictions from traditional foraging models where foraging intensity is assumed to cluster around values that maximize net rate or efficiency. The model suggests that strategies that cluster around rate and efficiency maximization should be viewed as particular solutions to a more general problem.     

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     

Evidence of a maternal foraging cycle resembling that of otariid seals in a small phocid,the harbor seal

Summary Lactation strategies in the two largest families of seals have been characterized as a phylogenetic dichotomy, with sea lions and fur seals (Otariidae) exhibiting foraging cycles and true seals (Phocidae) a strategy of fasting. We show that a lactating phocid, the harbor seal, Phoca vitulina, has a foraging cycle similar to that of otariids. Time-depth recorders attached to lactating harbor seal mothers revealed that 9 of 11 females began bouts of diving, averaging 12–40 m, by mid-lactation (12 days). During the remainder of lactation, females made an average of seven diving trips, lasting about 7 h. They returned to the rookery during the interval between successive bouts to nurse their pups. Diving was more frequent during daylight than at night and diving bouts increased in duration as lactation progressed. The diving behavior of females that had weaned their pups and previously collected data from stomach lavage, suggest that the bouts of diving represent successful foraging. We propose that the lactation strategy of the harbor seal is intermediate to that of the otariids and other phocids studied. The harbor seal has a foraging cycle like the otariids, but typically resembles other phocids in length of lactation, rate of mass gain in pups, and in milk fat content. As harbor seals are among the smallest phocids, and only slightly larger than most otariids, it seems likely that maternal size constrains the amount of stored energy harbor seal females can bring to the rookery, forcing them to start feeding during the lactation period.Correspondence to: D.J. Boness     

Interactions between fangblennies (Plagiotremus rhinorhynchus) and their potential victims: fooling the model rather than the client?

Lepidophagous (scale-eating) blue-striped fangblennies (Plagiotremus rhinorhynchus Bleeker 1852) are often found sympatrically with the bluestreak cleaner wrasse (Labroides dimidiatus Valenciennes 1839). They have some resemblance to the juvenile L. dimidiatus and have previously been reported as aggressive cleaner wrasse mimics. We observed 14 P. rhinorhynchus on a small area in the barrier reef near Hoga Island, Indonesia to assess the effects of client size on the behaviour and attack success of fangblennies: our results suggest that fangblennies are selective with regard to victim size; fish avoided by the fangblennies are significantly larger than those not avoided and attack success is significantly higher at intermediate victim size classes. The behaviour of the victims also has a significant direct effect on the foraging success of the fangblennies; where the potential victim posed, 63.6% were ignored by the fangblenny and only 7.4% of attacks were successful on posing fish as opposed to a surprise attack success rate of 71.6%. Overall, victims which exhibited the pose behaviour were significantly smaller in size. It appears likely that the predatory strategy of these fangblennies varies with victim size and that mimicry plays a minor role in attracting potential victims. We suggest that in common with other mimetic fish the resemblance of fangblennies to juvenile bluestreak cleaner wrasse allows them to actively hunt in areas where adult cleaners are common thus, indirectly improving their feeding opportunities.