Tool use behavior in three wild bonobo communities at Kokolopori

Comparative studies on tool technologies in extant primates, especially in our closest living relatives, offer a window into the evolutionary foundations of tool use in hominins. Whereas chimpanzee tool technology is well studied across populations, the scarcity of described tool technology in wild populations of our other closest living relative, the bonobo, is a mystery. Here we provide a first report of the tool use repertoire of the Kokolopori bonobos and describe in detail the use of leaf-umbrellas during rainfall, with the aim to improve our knowledge of bonobo tool use capacity in the wild. The tool use repertoire of the Kokolopori bonobos was most similar to that of the nearby population of Wamba and comprised eight behaviors, none in a foraging context. Further, over a 6-month period we documented 44 instances of leaf-umbrella use by 22 individuals from three communities, suggesting that this behavior is habitual. Most leaf-umbrella tool users were adult females, and we observed a nonadult using a leaf-umbrella on only a single occasion. While the study and theory of tool technologies is often based on the use of tools in foraging tasks, tool use in bonobos typically occurs in nonforaging contexts across populations. Therefore, incorporating both foraging and nonforaging contexts into our theoretical framework is essential if we wish to advance our understanding of the evolutionary trajectories of tool technology in humans.     

When to approach novel prey cues? Social learning strategies in frog-eating bats

Animals can use different sources of information when making decisions. Foraging animals often have access to both self-acquired and socially acquired information about prey. The fringe-lipped bat, Trachops cirrhosus, hunts frogs by approaching the calls that frogs produce to attract mates. We examined how the reliability of self-acquired prey cues affects social learning of novel prey cues. We trained bats to associate an artificial acoustic cue (mobile phone ringtone) with food rewards. Bats were assigned to treatments in which the trained cue was either an unreliable indicator of reward (rewarded 50% of the presentations) or a reliable indicator (rewarded 100% of the presentations), and they were exposed to a conspecific tutor foraging on a reliable (rewarded 100%) novel cue or to the novel cue with no tutor. Bats whose trained cue was unreliable and who had a tutor were significantly more likely to preferentially approach the novel cue when compared with bats whose trained cue was reliable, and to bats that had no tutor. Reliability of self-acquired prey cues therefore affects social learning of novel prey cues by frog-eating bats. Examining when animals use social information to learn about novel prey is key to understanding the social transmission of foraging innovations.     

Aggressive interactions for a decentralized regulation of foraging activity in the social wasp Polistes versicolor

Physical aggression among nestmates is commonly observed in animal societies like Polistes paper wasps, where it can be used to suppress worker reproduction. There is no consensus about how individuals use aggression in contexts other than reproduction. In order to clarify this topic, the regulation of worker-foraging behavior was studied in the Neotropical eusocial wasp Polistes versicolor. By experimentally manipulating food demand, we found evidence that aggression is used as a decentralized mechanism of regulating foraging, because after food supplementation: (1) aggression levels and foraging rates decreased and (2) aggression received and exhibited by foragers and non-foragers decreased. P. versicolor can use aggression in both reproductive and foraging contexts. The conclusion is drawn that this species is a good model for understanding how individuals differ from aggression related to reproduction and foraging, which would allow understanding of the evolutionary shift in the function of aggression from being the mechanism of reproductive control to being co-opted for the decentralized, self-organized regulation of worker-foraging.     

Foraging behavior and spatial use of a rock specialist: the southern vizcacha (Lagidium viscacia), and the exotic European hare (Lepus europaeus) in rocky outcrops of northwestern Patagonia, Argentina

The southern vizcacha (Lagidium viscacia) and the exotic European hare (Lepus europaeus) are two medium-sized herbivores that inhabit rocky outcrops in Patagonian steppe. These species overlap in diet and spatial use at medium distances from rocky outcrops in summer. We evaluated the spatial use through feces distribution in winter and determined seasonal foraging intensity in relation to the distances from rocky outcrops in order to elucidate how these herbivores use food and spatial resources in food scarcity periods. The vizcacha utilized the habitat close to rocky outcrops (<40 m) independent of season, while the hare exploited the space more widely, especially distances >40 m. However, in winter, at medium distances from rocky outcrops, there was partial spatial overlap because hares' activities were closer to rocky outcrops. Foraging intensity increased significantly in areas used by the vizcacha closer to rocky outcrops when food availability decreased, and the grasses Stipa speciosa, Poa sp., and Festuca pallescens were strongly foraged. In contrast, foraging intensity showed no changes in further distances to rocky outcrops and more use by the hare. The spatial and feeding behavior of the vizcacha, restricted to vicinity of rocky outcrops, showed high vulnerability to food availability changes. In resource scarcity situations, the spatial opportunistic behavior of the hare and the overlap in diet with the vizcacha constitutes a threat to this native herbivore. It is necessary to monitor populations of hare, since high densities could lead to food competition, impacting the small colonies of the southern vizcacha.     

DNA diet profiles with high‐resolution animal tracking data reveal levels of prey selection relative to habitat choice in a crepuscular insectivorous bird

Given the global decline of many invertebrate food resources, it is fundamental to understand the dietary requirements of insectivores. We give new insights into the functional relationship between the spatial habitat use, food availability, and diet of a crepuscular aerial insectivore, the European Nightjar (Caprimulgus europaeus) by relating spatial use data with high‐throughput sequencing (HTS) combined with DNA metabarcoding. Our study supports the predictions that nightjars collect a substantial part of their daily nourishment from foraging locations, sometimes at considerable distance from nesting sites. Lepidopterans comprise 65% of nightjars'' food source. Nightjars tend to select larger species of Lepidoptera (>19 mm) which suggests that nightjars optimize the efficiency of foraging trips by selecting the most energetically favorable—larger—prey items. We anticipate that our findings may shed additional light on the interactions between invertebrate communities and higher trophic levels, which is required to understand the repercussions of changing food resources on individual‐ and population‐level processes.     

Activity profiles and hook-tool use of New Caledonian crows recorded by bird-borne video cameras

New Caledonian crows are renowned for their unusually sophisticated tool behaviour. Despite decades of fieldwork, however, very little is known about how they make and use their foraging tools in the wild, which is largely owing to the difficulties in observing these shy forest birds. To obtain first estimates of activity budgets, as well as close-up observations of tool-assisted foraging, we equipped 19 wild crows with self-developed miniature video cameras, yielding more than 10 h of analysable video footage for 10 subjects. While only four crows used tools during recording sessions, they did so extensively: across all 10 birds, we conservatively estimate that tool-related behaviour occurred in 3% of total observation time, and accounted for 19% of all foraging behaviour. Our video-loggers provided first footage of crows manufacturing, and using, one of their most complex tool types—hooked stick tools—under completely natural foraging conditions. We recorded manufacture from live branches of paperbark (Melaleuca sp.) and another tree species (thought to be Acacia spirorbis), and deployment of tools in a range of contexts, including on the forest floor. Taken together, our video recordings reveal an ‘expanded’ foraging niche for hooked stick tools, and highlight more generally how crows routinely switch between tool- and bill-assisted foraging.     

Cultural transmission of tool use by Indo-Pacific bottlenose dolphins (Tursiops sp.) provides access to a novel foraging niche

Culturally transmitted tool use has important ecological and evolutionary consequences and has been proposed as a significant driver of human evolution. Such evidence is still scarce in other animals. In cetaceans, tool use has been inferred using indirect evidence in one population of Indo-Pacific bottlenose dolphins (Tursiops sp.), where particular dolphins (‘spongers’) use marine sponges during foraging. To date, evidence of whether this foraging tactic actually provides access to novel food items is lacking. We used fatty acid (FA) signature analysis to identify dietary differences between spongers and non-spongers, analysing data from 11 spongers and 27 non-spongers from two different study sites. Both univariate and multivariate analyses revealed significant differences in FA profiles between spongers and non-spongers between and within study sites. Moreover, FA profiles differed significantly between spongers and non-spongers foraging within the same deep channel habitat, whereas the profiles of non-spongers from deep channel and shallow habitats at this site could not be distinguished. Our results indicate that sponge use by bottlenose dolphins is linked to significant differences in diet. It appears that cultural transmission of tool use in dolphins, as in humans, allows the exploitation of an otherwise unused niche.     

Seasonal variation in feeding habits and diet selection by wild boars in a semi-arid environment of Argentina

The wild boar, Sus scrofa, was first introduced for hunting purposes in Argentina in 1906 and presently occupies a wide range of habitats. Understanding the food habits of invasive species is important for predicting the effects of animal food consumption on the environment and on human activities, such as farming. The wild boar is an omnivorous, opportunistic species whose diet is determined by the relative abundance of different types of foods. In general, the wild boar’s diet has been widely studied in the world, both as a native and invasive species, but little is known regarding food resource selection in the Monte Desert biome. Our study assessed the seasonal variation in the diet of wild boars, as well as the nutritional quality of consumed items. Further, we determined the diet selection of this species. Diet analyses were based on faecal samples collected over two seasons (wet and dry) in 1 year. Herbs were the most frequently consumed food item, with wild boars showing a selection for them in both seasons. The wild boar uses food resources according to seasonal availability (larger trophic niche breadth under higher plant diversity, as in the wet season). In turn, within each season, it selects items of high forage quality and high carbohydrate contents. In conclusion, this foraging strategy enables wild boar to maximize energy budget through food selection in order to survive in a semi-arid environment such as the Monte Desert.     

Social learning about egg-laying substrates in fruitflies

Social learning, defined as learning from other individuals, has had dramatic effects on some species, including humans, in whom it has generated a rich culture. As a first step in examining the evolution of and mechanisms underlying social learning in insects, we tested for social learning in fruitflies (Drosophila melanogaster). Focal females (observers) that experienced novel food together with mated females (models), who had laid eggs on that food, subsequently exhibited a stronger preference for laying eggs on that food over another novel food compared with focal females that experienced the food alone. We observed no social learning, however, when observers experienced food with potentially more ambiguous social information provided by the presence of either virgin models or aggregation pheromone. This first documentation of social learning about egg-laying substrates in fruitflies builds on recent data indicating intricate use of social information by fruitflies and opens up exciting avenues for research on the evolution and neurogenetics of social learning using biology''s major model system.     

Flexible feeding on cultivated underground storage organs by rainforest-dwelling chimpanzees at Bossou, West Africa

It has been proposed that exploitation of underground storage organs (USOs) played an important role in the evolution of the genus Homo, these items serving as ‘fallback foods’ during periods of low food availability. The use of USOs as food by wild chimpanzees is infrequent and seen mostly in populations inhabiting relatively arid environments, such as the savanna. Here, we specifically test the hypothesis that chimpanzees (Pan troglodytes verus) inhabiting tropical wet forest at Bossou (Republic of Guinea, West Africa) exploit USOs as a fallback food during periods of fruit scarcity. Chimpanzees were never observed feeding on wild USOs, that is, those that were never cultivated, and rarely on other underground plant parts. However, direct observations revealed regular consumption of the USOs of cultivated cassava (Manihot esculenta), a spatially abundant and continuously available plant, although the chimpanzees did not use tools when acquiring and feeding on cassava. In agreement with the fallback foods hypothesis, our results show that chimpanzees exploited cassava USOs more frequently when both wild and cultivated fruits were scarce, and consumption patterns of cassava paralleled those of wild fallback foods. These seasonal extractive USO foraging strategies by chimpanzees can strengthen attempts to construct a clearer picture of the importance of USO feeding in hominoid evolution.     

Optimal Foraging and Hominid Evolution: Labor and Reciprocity

We argue that cooperative foraging incorporating information exchange may have preceded tool use during the course of hominid evolution. In moving to the savanna, early hominids must have faced increasingly dispersed but sometimes more profitable food sources. The problem is finding such foods. Search costs can be reduced for each individual if a number of foragers cooperate by ranging over different parts of the habitat and by exchanging information about encountered food items. Given the probability of encountering a given food item and the return per individual for that item, it is possible to specify the optimal group size. Thus, in the patchy savanna environment, selection would have favored increased gregariousness and cooperation on the part of early hominids, setting the stage for the emergence of reciprocal exchanges of information and resources. However, such a system of reciprocity is open to manipulation. Outside the foraging context, the tension between reciprocity and manipulation would shape other social interactions. Communication and information exchange may have been more critical than labor and technology in evolving hominids from hominoids. Human sociality may find its origins in a shift in primate foraging tactics.     

The fourth dimension of tool use: temporally enduring artefacts aid primates learning to use tools

All investigated cases of habitual tool use in wild chimpanzees and capuchin monkeys include youngsters encountering durable artefacts, most often in a supportive social context. We propose that enduring artefacts associated with tool use, such as previously used tools, partly processed food items and residual material from previous activity, aid non-human primates to learn to use tools, and to develop expertise in their use, thus contributing to traditional technologies in non-humans. Therefore, social contributions to tool use can be considered as situated in the three dimensions of Euclidean space, and in the fourth dimension of time. This notion expands the contribution of social context to learning a skill beyond the immediate presence of a model nearby. We provide examples supporting this hypothesis from wild bearded capuchin monkeys and chimpanzees, and suggest avenues for future research.     

Extractive foraging and tool-aided behaviors in the wild Nicobar long-tailed macaque (<Emphasis Type="Italic">Macaca fascicularis umbrosus</Emphasis>)

Macaques possess a repertoire of extractive foraging techniques that range from complex manipulation to tool-aided behaviors, to access food items that increase their foraging efficiency substantially. However, the complexity and composition of such techniques vary considerably between species and even between populations. In the present study, we report seven such complex manipulative behaviors that include six extractive foraging behaviors, and teeth flossing, in a population of Nicobar long-tailed macaques. The apparent purpose of these behaviors was an extraction of encased food, processing food, foraging hidden invertebrates, and dental flossing. Among these behaviors, three behaviors viz. wrapping, wiping, and teeth-flossing were tool-aided behaviors, where macaques used both natural and synthetic materials as tools. Occasionally macaques also modified those tools prior to their use. The substrate use patterns of leaf rubbing and teeth flossing were similar to that observed in other macaques. The spontaneous tool modification to perform wrapping was a first time observation. These observations suggest that Nicobar long-tailed macaques have a high level of sensorimotor intelligence which helps to evolve such innovative foraging solutions.     

Feeding Strategies of Brown Howler Monkeys in Response to Variations in Food Availability

Primates display varying degrees of behavioral flexibility that allow them to adjust their diet to temporal changes in food availability. This trait might be critical for the survival of folivorous-frugivorous species inhabiting small forest fragments, where the availability of food resources tends to be lower than in large fragments and continuous forests. However, the scarcity of studies addressing this issue hampers our understanding of the adaptive behaviors that favor the survival of these primates in low-quality habitats. We conducted a 36-mo study testing the hypothesis that brown howler monkeys (Alouatta guariba clamitans) are able to adjust their diet in response to local and seasonal changes in resource availability. We compared the diet of six free-ranging groups inhabiting three small (<10 ha) and three large (>90 ha) Atlantic forest fragments in southern Brazil and estimated the temporal availability of their top food species (i.e., those species that together contribute ≥80% of total feeding records). We found that brown howlers exploited similarly rich diets in small (45, 54, and 57 plant species) and large (48, 51, and 56 species) fragments. However, intermonth diet similarity was higher for groups in small fragments, where howlers also fed on plant items from nine alien species. Fruits and leaves were the most consumed plant items in both small (42% and 49% of feeding records, respectively) and large (51% and 41%, respectively) fragments. The consumption of young leaves was higher in small than in large fragments, whereas the consumption of other plant items did not show a pattern related to fragment size. Regarding the contribution of growth forms as food sources, only the exploitation of palms showed a pattern related to fragment size. Palms contributed more to the diet of groups inhabiting large fragments. The availability of seasonal food items–ripe fruits and young leaves–influenced their consumption in both habitat types. Therefore, brown howlers cope with local and seasonal fluctuations in food availability by opportunistically exploiting resources. We believe that this feeding flexibility is a key component of the phenotypic plasticity that enables howlers to thrive in disturbed habitat patches, where periods of scarcity of preferred foods shall be more common.     

Honey bee (Apis mellifera) preference towards micronutrients and their impact on bee colonies

Honey bees are important pollinators and take micronutrients from different natural floral resources and turbid water to adequately meet their nutritional requirements. But the role of micronutrients for honey bee health is not well understood. Here, the present study was conducted to determine honey bees' micronutrients preference in summer and winter seasons. Also, the impact of micronutrients on foraging behaviour and brood increase was studied in different honey bee colonies. The results elucidated that honey bees exhibited a strong preference for a salt solution compared to deionized water during the summer and winter seasons. However, there was a notable switch in salt preference between seasons. Overall, honey bees showed significantly more foraging activity, more pollen collection, and increased brood area after sodium consumption compared to other minerals in the summer season. Further, pollen collection and brood area were significantly higher after the use of potassium in the winter season. Thus, the food preference of honey bees is strongly linked with the seasons and the availability of the floral resources. Our data suggested that honey bees may seek specific nutrients during variation of the seasonal conditions.     

Social networks predict patch discovery in a wild population of songbirds

Animals use social information in a wide variety of contexts. Its extensive use by individuals to locate food patches has been documented in a number of species, and various mechanisms of discovery have been identified. However, less is known about whether individuals differ in their access to, and use of, social information to find food. We measured the social network of a wild population of three sympatric tit species (family Paridae) and then recorded individual discovery of novel food patches. By using recently developed methods for network-based diffusion analysis, we show that order of arrival at new food patches was predicted by social associations. Models based only on group searching did not explain this relationship. Furthermore, network position was correlated with likelihood of patch discovery, with central individuals more likely to locate and use novel foraging patches than those with limited social connections. These results demonstrate the utility of social network analysis as a method to investigate social information use, and suggest that the greater probability of receiving social information about new foraging patches confers a benefit on more socially connected individuals.     

Ecological Risk Aversion and Foraging Behaviors of Juvenile Squirrel Monkeys (Saimiri sciureus)

The ‘ecological risk aversion hypothesis’ [C.H. Janson and C.P. van Schaik, Juvenile Primates, Oxford Univ. Press, New York (1993), pp. 57–74] proposes that the pattern of slow growth characteristic of juvenile primates is a response to ecological risks (predation and starvation) experienced by juveniles. Juveniles are thought to avoid predation risk by positioning themselves near conspecifics, therefore experiencing high levels of feeding competition with older individuals, reduced access to resources and, consequently, high starvation risks during periods of food scarcity. The present study compared the foraging behaviors of juvenile and adult squirrel monkeys, a small neotropical primate characterized by a long juvenile period, to determine how predation and starvation risks affected juvenile behaviors. The study was conducted in Eastern Amazonia, in a seasonal environment. Due to their slow development, small body size and large group sizes, it was expected that juveniles in this species would behave in a manner consistent with the risk aversion hypothesis. However, age differences in foraging efficiency and foraging success were smaller than predicted. There was also no evidence that juveniles sacrificed access to food for predator protection. Adults did not have preferential access to fruit patches and direct competition was rare. Feeding competition for prey, the most common resource in the troop's diet, was negligible. Therefore, the slow growth and long juvenile period of squirrel monkeys do not correspond with evidence of predation or starvation risk, as predicted by the risk aversion hypothesis.     

Social Behavior and the Ontogeny of Foraging in the Kea (Nestor notabilis)

Kea are omnivorous parrots endemic to the high mountains of the South Island of New Zealand. Over a two-year period, we recorded quantitative behavioral data from 38 banded male kea foraging at a refuse dump outside Arthur's Pass National Park and analyzed the effects of social factors on the ontogeny of foraging. Members of the four distinguishable age classes — fledglings, juveniles, subadults, and adults — displayed characteristic differences in foraging ability and in the social behavior used to obtain access to resources. Adults performed most of the excavation that uncovered new food resources. Fledglings explored and manipulated objects almost continuously, but they discovered little food on their own and were commonly fed directly by adults. Juveniles obtained the highest foraging yields for the amount of time spent searching of any age class, aided by appeasement behavior that gave them preferential access to foods discovered by adults. Kleptoparasitism served as a primary foraging strategy for subadults, who were otherwise poor at discovering and retaining food resources. Social factors influence the acquisition of foraging expertise in the Kea in different ways at different stages of development.     

Tandem running by foraging Pachycondyla striata workers in field conditions vary in response to food type,food distance,and environmental conditions

Ants show collective and individual behavioral flexibility in their response to immediate context, choosing for example between different foraging strategies. In Pachycondyla striata, workers can forage solitarily or recruit and guide nestmates to larger food sources through tandem running. Although considered more ancestral and less efficient than pheromone trail-laying, this strategy is common especially in species with small colony size. What is not known is how the decision to recruit or follow varies according to the immediate context. That is, how fine adjustments in information transfer affect immediate foraging decisions at the colony level. Here, we studied individually marked workers and evaluated their foraging decisions when food items varied in nature (protein versus carbohydrate), size, and distance from the nest at different temperatures and humidity levels. Our results show that tandem run leaders and potential followers adjust their behavior according to a combination of external factors. While 84.2% of trips were solitary, most ants (81%) performed at least 1 tandem run. However, tandem runs were more frequent for nearby resources and at higher relative humidity. Interestingly, when food items were located far away, tandem runs were more successful when heading to protein sources (75%) compared with carbohydrate sources (42%). Our results suggest that the social information transfer between leaders and followers conveys more information than previously thought, and also relies on their experience and motivation.     

Reef fishes foraging facilitation behavior: increasing the access to a food resource

Fishes associated in schools acquire adaptive advantages by grouping together, e.g., access to a larger variety of food resources, foraging sites, and protection against potential predators. This work presents the first record of a feeding association between the bucktooth parrotfish, Sparisoma radians and the sailor’s grunt Haemulon parra, on Tamandaré reefs, Southwestern Atlantic. Through this association, S. radians gained access to otherwise unavailable food resources to be found inside territorial damselfish domain, thus characterizing an event of foraging facilitation.