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Concept: Foraging

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Animals are primarily limited by their capacity to acquire food, yet digestive performance also conditions energy acquisition, and ultimately fitness. Optimal foraging theory predicts that organisms feeding on patchy resources should maximize their food loads within each patch, and should digest these loads quickly to minimize travelling costs between food patches. We tested the prediction of high digestive performance in wandering albatrosses, which can ingest prey of up to 3 kg, and feed on highly dispersed food resources across the southern ocean. GPS-tracking of 40 wandering albatrosses from the Crozet archipelago during the incubation phase confirmed foraging movements of between 475-4705 km, which give birds access to a variety of prey, including fishery wastes. Moreover, using miniaturized, autonomous data recorders placed in the stomach of three birds, we performed the first-ever measurements of gastric pH and temperature in procellariformes. These revealed surprisingly low pH levels (average 1.50±0.13), markedly lower than in other seabirds, and comparable to those of vultures feeding on carrion. Such low stomach pH gives wandering albatrosses a strategic advantage since it allows them a rapid chemical breakdown of ingested food and therefore a rapid digestion. This is useful for feeding on patchy, natural prey, but also on fishery wastes, which might be an important additional food resource for wandering albatrosses.

Concepts: Eating, Food, Stomach, PH, Digestion, Gastric acid, Optimal foraging theory, Foraging

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BACKGROUND: Optimal foraging theory predicts that animals will tend to maximize foraging success by optimizing search strategies. However, how organisms detect sparsely distributed food resources remains an open question. When targets are sparse and unpredictably distributed, a Lévy strategy should maximize foraging success. By contrast, when resources are abundant and regularly distributed, simple Brownian random movement should be sufficient. Although very different groups of organisms exhibit Lévy motion, the shift from a Lévy to a Brownian search strategy has been suggested to depend on internal and external factors such as sex, prey density, or environmental context. However, animal response at the individual level has received little attention. METHODOLOGY/PRINCIPAL FINDINGS: We used GPS satellite-telemetry data of Egyptian vultures Neophron percnopterus to examine movement patterns at the individual level during consecutive years, with particular interest in the variations in foraging search patterns during the different periods of the annual cycle (i.e. breeding vs. non-breeding). Our results show that vultures followed a Brownian search strategy in their wintering sojourn in Africa, whereas they exhibited a more complex foraging search pattern at breeding grounds in Europe, including Lévy motion. Interestingly, our results showed that individuals shifted between search strategies within the same period of the annual cycle in successive years. CONCLUSIONS/SIGNIFICANCE: Results could be primarily explained by the different environmental conditions in which foraging activities occur. However, the high degree of behavioural flexibility exhibited during the breeding period in contrast to the non-breeding period is challenging, suggesting that not only environmental conditions explain individuals' behaviour but also individuals' cognitive abilities (e.g., memory effects) could play an important role. Our results support the growing awareness about the role of behavioural flexibility at the individual level, adding new empirical evidence about how animals in general, and particularly scavengers, solve the problem of efficiently finding food resources.

Concepts: Psychology, Predation, Food, Menstrual cycle, Optimal foraging theory, Foraging, Behavioral ecology, Eating behaviors

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Feeding stations are commonly used to sustain conservation programs of scavengers but their impact on behaviour is still debated. They increase the temporal and spatial predictability of food resources while scavengers have supposedly evolved to search for unpredictable resources. In the Grands Causses (France), a reintroduced population of Griffon vultures Gyps fulvus can find carcasses at three types of sites: 1. “light feeding stations”, where farmers can drop carcasses at their farm (spatially predictable), 2. “heavy feeding stations”, where carcasses from nearby farms are concentrated (spatially and temporally predictable) and 3. open grasslands, where resources are randomly distributed (unpredictable). The impact of feeding stations on vulture’s foraging behaviour was investigated using 28 GPS-tracked vultures. The average home range size was maximal in spring (1272±752 km(2)) and minimal in winter (473±237 km(2)) and was highly variable among individuals. Analyses of home range characteristics and feeding habitat selection via compositional analysis showed that feeding stations were always preferred compared to the rest of the habitat where vultures can find unpredictable resources. Feeding stations were particularly used when resources were scarce (summer) or when flight conditions were poor (winter), limiting long-ranging movements. However, when flight conditions were optimal, home ranges also encompassed large areas of grassland where vultures could find unpredictable resources, suggesting that vultures did not lose their natural ability to forage on unpredictable resources, even when feeding stations were available. However during seasons when food abundance and flight conditions were not limited, vultures seemed to favour light over heavy feeding stations, probably because of the reduced intraspecific competition and a pattern closer to the natural dispersion of resources in the landscape. Light feeding stations are interesting tools for managing food resources, but don’t prevent vultures to feed at other places with possibly high risk of intoxication (poison).

Concepts: Intraspecific competition, Scarcity, Foraging, Winter, Vulture, Gyps, Griffon Vulture, Home range

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Most seabirds are very noisy at their breeding colonies, when aggregated in high densities. Calls are used for individual recognition and also emitted during agonistic interactions. When at sea, many seabirds aggregate over patchily distributed resources and may benefit from foraging in groups. Because these aggregations are so common, it raises the question of whether seabirds use acoustic communication when foraging at sea? We deployed video-cameras with built in microphones on 36 Cape gannets (Morus capensis) during the breeding season of 2010-2011 at Bird Island (Algoa Bay, South Africa) to study their foraging behaviour and vocal activity at sea. Group formation was derived from the camera footage. During ~42 h, calls were recorded on 72 occasions from 16 birds. Vocalization exclusively took place in the presence of conspecifics, and mostly in feeding aggregations (81% of the vocalizations). From the observation of the behaviours of birds associated with the emission of calls, we suggest that the calls were emitted to avoid collisions between birds. Our observations show that at least some seabirds use acoustic communication when foraging at sea. These findings open up new perspectives for research on seabirds foraging ecology and their interactions at sea.

Concepts: Bird, Albatross, Seabird, Sound, Foraging, Gannet, Gannets, Sulidae

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Insect pollinators such as bumblebees play a vital role in many ecosystems, so it is important to understand their foraging movements on a landscape scale. We used harmonic radar to record the natural foraging behaviour of Bombus terrestris audax workers over their entire foraging career. Every flight ever made outside the nest by four foragers was recorded. Our data reveal where the bees flew and how their behaviour changed with experience, at an unprecedented level of detail. We identified how each bee’s flights fit into two categories-which we named exploration and exploitation flights-examining the differences between the two types of flight and how their occurrence changed over the course of the bees' foraging careers. Exploitation of learned resources takes place during efficient, straight trips, usually to a single foraging location, and is seldom combined with exploration of other areas. Exploration of the landscape typically occurs in the first few flights made by each bee, but our data show that further exploration flights can be made throughout the bee’s foraging career. Bees showed striking levels of variation in how they explored their environment, their fidelity to particular patches, ratio of exploration to exploitation, duration and frequency of their foraging bouts. One bee developed a straight route to a forage patch within four flights and followed this route exclusively for six days before abandoning it entirely for a closer location; this second location had not been visited since her first exploratory flight nine days prior. Another bee made only rare exploitation flights and continued to explore widely throughout its life; two other bees showed more frequent switches between exploration and exploitation. Our data shed light on the way bumblebees balance exploration of the environment with exploitation of resources and reveal extreme levels of variation between individuals.

Concepts: Honey bee, Pollinator decline, Bee, Bumblebee, Pollinator, Apidae, Pollinators, Foraging

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Social relationships are fundamental to animals living in complex societies [1-3]. The extent to which individuals base their decisions around their key social relationships, and the consequences this has on their behavior and broader population level processes, remains unknown. Using a novel experiment that controlled where individual wild birds (great tits, Parus major) could access food, we restricted mated pairs from being allowed to forage at the same locations. This introduced a conflict for pair members between maintaining social relationships and accessing resources. We show that individuals reduce their own access to food in order to sustain their relationships and that individual foraging activity was strongly influenced by their key social counterparts. By affecting where individuals go, social relationships determined which conspecifics they encountered and consequently shaped their other social associations. Hence, while resource distribution can determine individuals' spatial and social environment [4-8], we illustrate how key social relationships themselves can govern broader social structure. Finally, social relationships also influenced the development of social foraging strategies. In response to forgoing access to resources, maintaining pair bonds led individuals to develop a flexible “scrounging” strategy, particularly by scrounging from their pair mate. This suggests that behavioral plasticity can develop to ameliorate conflicts between social relationships and other demands. Together, these results illustrate the importance of considering social relationships for explaining behavioral variation due to their significant impact on individual behavior and demonstrate the consequences of key relationships for wider processes.

Concepts: Sociology, Behavior, Social relation, Great Tit, Parus, Foraging, Forage

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Many dynamical networks, such as the ones that produce the collective behavior of social insects, operate without any central control, instead arising from local interactions among individuals. A well-studied example is the formation of recruitment trails in ant colonies, but many ant species do not use pheromone trails. We present a model of the regulation of foraging by harvester ant (Pogonomyrmex barbatus) colonies. This species forages for scattered seeds that one ant can retrieve on its own, so there is no need for spatial information such as pheromone trails that lead ants to specific locations. Previous work shows that colony foraging activity, the rate at which ants go out to search individually for seeds, is regulated in response to current food availability throughout the colony’s foraging area. Ants use the rate of brief antennal contacts inside the nest between foragers returning with food and outgoing foragers available to leave the nest on the next foraging trip. Here we present a feedback-based algorithm that captures the main features of data from field experiments in which the rate of returning foragers was manipulated. The algorithm draws on our finding that the distribution of intervals between successive ants returning to the nest is a Poisson process. We fitted the parameter that estimates the effect of each returning forager on the rate at which outgoing foragers leave the nest. We found that correlations between observed rates of returning foragers and simulated rates of outgoing foragers, using our model, were similar to those in the data. Our simple stochastic model shows how the regulation of ant colony foraging can operate without spatial information, describing a process at the level of individual ants that predicts the overall foraging activity of the colony.

Concepts: Time, Insect, Ant, Foraging, Pheromone, Forage, Termite, Ant colony

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Since 1994, more than €41 billion has been spent in the European Union on agri-environment schemes (AESs), which aim to mitigate the effects of anthropomorphic landscape changes via financial incentives for land managers to encourage environmentally friendly practices [1-6]. Surprisingly, given the substantial price tag and mandatory EU member participation [2], there is either a lack of [1] or mixed [1, 2, 7] evidence-based support for the schemes. One novel source of data to evaluate AESs may be provided by an organism that itself may benefit from them. Honeybees (Apis mellifera), important pollinators for crops and wildflowers [8, 9], are declining in parts of the world from many factors, including loss of available forage from agricultural intensification [10-13]. We analyzed landscape-level honeybee foraging ecology patterns over two years by decoding 5,484 waggle dances from bees located in the center of a mixed, urban-rural 94 km(2) area, including lands under government-funded AESs. The waggle dance, a unique behavior performed by successful foragers, communicates to nestmates the most profitable foraging locations [14-16]. After correcting for distance, dances demonstrate that honeybees possess a significant preference for rural land managed under UK Higher Level AESs and a significant preference against rural land under UK Organic Entry Level AESs. Additionally, the two most visited areas contained a National and Local Nature Reserve, respectively. Our study demonstrates that honeybees, with their great foraging range and sensitive response to forage quality, can be used as bioindicators to monitor large areas and provide information relevant to better environmental management. VIDEO ABSTRACT:

Concepts: European Union, European honey bee, Honey bee, Beekeeping, Bumblebee, Pollinators, Foraging, Waggle dance

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Even as demand for their services increases, honey bees (Apis mellifera) and other pollinating insects continue to decline in Europe and North America. Honey bees face many challenges, including an issue generally affecting wildlife: landscape changes have reduced flower-rich areas. One way to help is therefore to supplement with flowers, but when would this be most beneficial? We use the waggle dance, a unique behaviour in which a successful forager communicates to nestmates the location of visited flowers, to make a 2-year survey of food availability. We “eavesdropped” on 5097 dances to track seasonal changes in foraging, as indicated by the distance to which the bees as economic foragers will recruit, over a representative rural-urban landscape. In year 3, we determined nectar sugar concentration. We found that mean foraging distance/area significantly increase from springs (493 m, 0.8 km2) to summers (2156 m, 15.2 km2), even though nectar is not better quality, before decreasing in autumns (1275 m, 5.1 km2). As bees will not forage at long distances unnecessarily, this suggests summer is the most challenging season, with bees utilizing an area 22 and 6 times greater than spring or autumn. Our study demonstrates that dancing bees as indicators can provide information relevant to helping them, and, in particular, can show the months when additional forage would be most valuable.

Concepts: Insect, Honey bee, Beekeeping, Season, Flower, Honey, Dance, Foraging

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Identifying characteristics of foraging activity is fundamental to understanding an animals' lifestyle and foraging ecology. Despite its importance, monitoring the foraging activities of marine animals is difficult because direct observation is rarely possible. In this study, we use an animal-borne imaging system and three-dimensional data logger simultaneously to observe the foraging behaviour of large juvenile and adult sized loggerhead turtles (Caretta caretta) in their natural environment. Video recordings showed that the turtles foraged on gelatinous prey while swimming in mid-water (i.e., defined as epipelagic water column deeper than 1 m in this study). By linking video and 3D data, we found that mid-water foraging events share the common feature of a marked deceleration phase associated with the capture and handling of the sluggish prey. Analysis of high-resolution 3D movements during mid-water foraging events, including presumptive events extracted from 3D data using deceleration in swim speed as a proxy for foraging (detection rate = 0.67), showed that turtles swam straight toward prey in 171 events (i.e., turning point absent) but made a single turn toward the prey an average of 5.7±6.0 m before reaching the prey in 229 events (i.e., turning point present). Foraging events with a turning point tended to occur during the daytime, suggesting that turtles primarily used visual cues to locate prey. In addition, an incident of a turtle encountering a plastic bag while swimming in mid-water was recorded. The fact that the turtle’s movements while approaching the plastic bag were analogous to those of a true foraging event, having a turning point and deceleration phase, also support the use of vision in mid-water foraging. Our study shows that integrated video and high-resolution 3D data analysis provides unique opportunities to understand foraging behaviours in the context of the sensory ecology involved in prey location.

Concepts: Ecology, Observation, Foraging, Loggerhead Sea Turtle, The Turtles, Mark Volman