Food selection in larval fruit flies: dynamics and effects on larval development

Selecting food items and attaining a nutritionally balanced diet is an important challenge for all animals including humans. We aimed to establish fruit fly larvae (Drosophila melanogaster) as a simple yet powerful model system for examining the mechanisms of specific hunger and diet selection. In two lab experiments with artificial diets, we found that larvae deprived of either sucrose or protein later selectively fed on a diet providing the missing nutrient. When allowed to freely move between two adjacent food patches, larvae surprisingly preferred to settle on one patch containing yeast and ignored the patch providing sucrose. Moreover, when allowed to move freely between three patches, which provided either yeast only, sucrose only or a balanced mixture of yeast and sucrose, the majority of larvae settled on the yeast-plus-sucrose patch and about one third chose to feed on the yeast only food. While protein (yeast) is essential for development, we also quantified larval success on diets with or without sucrose and show that larvae develop faster on diets containing sucrose. Our data suggest that fruit fly larvae can quickly assess major nutrients in food and seek a diet providing a missing nutrient. The larvae, however, probably prefer to quickly dig into a single food substrate for enhanced protection over achieving an optimal diet.     

Recruits of the stingless bee Scaptotrigona pectoralis learn food odors from the nest atmosphere

The ability to learn food odors inside the nest and to associate them with food sources in the field is of essential importance for the recruitment of nestmates in social bees. We investigated odor learning by workers within the hive and the influence of these odors on their food choice in the field in the stingless bee Scaptotrigona pectoralis. During the experiments, recruited bees had to choose between two feeders, one with an odor that was present inside the nest during the recruitment process, and one with an unknown odor. In all experiments with different odor combinations (linalool/phenylacetaldehyde, geraniol/eugenol) a significant majority of bees visited the feeder with the odor they had experienced in their nest (χ ²-tests; p?<?0.05). By contrast, the bees showed no preference for one of two feeders when they were either baited with the same odor (linalool) or contained no odor. Our results clearly show that naïve workers of S. pectoralis can learn the odor of a food source during the recruitment process from the nest atmosphere and that their subsequent food search in the field is influenced by the learned odor.     

Foraging scent marks of bumblebees: footprint cues rather than pheromone signals

In their natural habitat foraging bumblebees refuse to land on and probe flowers that have been recently visited (and depleted) by themselves, conspecifics or other bees, which increases their overall rate of nectar intake. This avoidance is often based on recognition of scent marks deposited by previous visitors. While the term 'scent mark' implies active labelling, it is an open question whether the repellent chemicals are pheromones actively and specifically released during flower visits, or mere footprints deposited unspecifically wherever bees walk. To distinguish between the two possibilities, we presented worker bumblebees (Bombus terrestris) with three types of feeders in a laboratory experiment: unvisited control feeders, passive feeders with a corolla that the bee had walked over on its way from the nest (with unspecific footprints), and active feeders, which the bee had just visited and depleted, but which were immediately refilled with sugar-water (potentially with specific scent marks). Bumblebees rejected both active and passive feeders more frequently than unvisited controls. The rate of rejection of passive feeders was only slightly lower than that of active feeders, and this difference vanished completely when passive corollas were walked over repeatedly on the way from the nest. Thus, mere footprints were sufficient to emulate the repellent effect of an actual feeder visit. In confirmation, glass slides on which bumblebees had walked on near the nest entrance accumulated hydrocarbons (alkanes and alkenes, C23 to C31), which had previously been shown to elicit repellency in flower choice experiments. We conclude that repellent scent marks are mere footprints, which foraging bees avoid when they encounter them in a foraging context.     

High precision during food recruitment of experienced (reactivated) foragers in the stingless bee<Emphasis Type="Italic"> Scaptotrigona mexicana</Emphasis> (Apidae,Meliponini)

Several studies have examined the existence of recruitment communication mechanisms in stingless bees. However, the spatial accuracy of location-specific recruitment has not been examined. Moreover, the location-specific recruitment of reactivated foragers, i.e., foragers that have previously experienced the same food source at a different location and time, has not been explicitly examined. However, such foragers may also play a significant role in colony foraging, particularly in small colonies. Here we report that reactivated Scaptotrigona mexicana foragers can recruit with high precision to a specific food location. The recruitment precision of reactivated foragers was evaluated by placing control feeders to the left and the right of the training feeder (direction-precision tests) and between the nest and the training feeder and beyond it (distance-precision tests). Reactivated foragers arrived at the correct location with high precision: 98.44% arrived at the training feeder in the direction trials (five-feeder fan-shaped array, accuracy of at least ±6° of azimuth at 50 m from the nest), and 88.62% arrived at the training feeder in the distance trials (five-feeder linear array, accuracy of at least ±5 m or ±10% at 50 m from the nest). Thus, S. mexicana reactivated foragers can find the indicated food source at a specific distance and direction with high precision, higher than that shown by honeybees, Apis mellifera, which do not communicate food location at such close distances to the nest.     

Yellowjackets use nest-based cues to differentially exploit higher-quality resources

While foraging, social insects encounter a dynamic array of food resources of varying quality and profitability. Because food acquisition influences colony growth and fitness, natural selection can be expected to favor colonies that allocate their overall foraging effort so as to maximize their intake of high-quality nutrients. Social wasps lack recruitment communication, but previous studies of vespine wasps have shown that olfactory cues influence foraging decisions. Odors associated with food brought into the nest by successful foragers prompt naive foragers to leave the nest and search for the source of those odors. Left unanswered, however, is the question of whether naive foragers take food quality into account in making their decisions about whether or not to search. In this study, two different concentrations of sucrose solutions, scented differently, were inserted directly into each of three Vespula germanica nests. At a feeder away from the nest, arriving foragers were given a choice between two 1.5 M sucrose solutions with the same scents as those in the nest. We show that wasps chose higher-quality resources in the field using information in the form of intranidal food-associated odor cues. By this simple mechanism, the colony can bias the allocation of its foraging effort toward higher-quality resources in the environment.     

The innate responses of bumble bees to flower patterns: separating the nectar guide from the nectary changes bee movements and search time

Nectar guides can enhance pollinator efficiency and plant fitness by allowing pollinators to more rapidly find and remember the location of floral nectar. We tested if a radiating nectar guide around a nectary would enhance the ability of naïve bumble bee foragers to find nectar. Most experiments that test nectar guide efficacy, specifically radiating linear guides, have used guides positioned around the center of a radially symmetric flower, where nectaries are often found. However, the flower center may be intrinsically attractive. We therefore used an off-center guide and nectary and compared “conjunct” feeders with a nectar guide surrounding the nectary to “disjunct” feeders with a nectar guide separated from the nectary. We focused on the innate response of novice bee foragers that had never previously visited such feeders. We hypothesized that a disjunct nectar guide would conflict with the visual information provided by the nectary and negatively affect foraging. Approximately, equal numbers of bumble bees (Bombus impatiens) found nectar on both feeder types. On disjunct feeders, however, unsuccessful foragers spent significantly more time (on average 1.6-fold longer) searching for nectar than any other forager group. Successful foragers on disjunct feeders approached these feeders from random directions unlike successful foragers on conjunct feeders, which preferentially approached the combined nectary and nectar guide. Thus, the nectary and a surrounding nectar guide can be considered a combination of two signals that attract naïve foragers even when not in the floral center.     

Tandem carrying,a new foraging strategy in ants: description,function, and adaptive significance relative to other described foraging strategies

An important aspect of social insect biology lies in the expression of collective foraging strategies developed to exploit food. In ants, four main types of foraging strategies are typically recognized based on the intensity of recruitment and the importance of chemical communication. Here, we describe a new type of foraging strategy, “tandem carrying”, which is also one of the most simple recruitment strategies, observed in the Ponerinae species Pachycondyla chinensis. Within this strategy, workers are directly carried individually and then released on the food resource by a successful scout. We demonstrate that this recruitment is context dependent and based on the type of food discovered and can be quickly adjusted as food quality changes. We did not detect trail marking by tandem-carrying workers. We conclude by discussing the importance of tandem carrying in an evolutionary context relative to other modes of recruitment in foraging and nest emigration.     

Distribution and dietary regulation of an associated facultative Rhizobiales-related bacterium in the omnivorous giant tropical ant,Paraponera clavata

We document a facultative Bartonella-like Rhizobiales bacterium in the giant tropical ant, Paraponera clavata. In a lowland tropical rainforest in Costa Rica, 59 colonies were assayed for the prevalence of the Bartonella-like bacterium (BLB), 14 of which were positive. We addressed three questions: First, how does the prevalence of BLB within colonies vary with environmental conditions? Second, how does diet affect the prevalence of BLB in P. clavata? Third, how does the distribution of BLB among colonies reflect ambient differences in food resources and foraging habits? A variety of environmental variables that may be predictive of the presence of BLB were measured, and diet manipulations were conducted to test whether the prevalence of BLB responded to supplemental carbohydrate or prey. The ambient frequency of BLB is much higher in young secondary forests, but is nearly absent from older secondary forests. The prevalence of BLB inside field colonies increased over the duration of a 2-week carbohydrate supplementation; however, water and prey supplementation did not alter the prevalence of BLB. The diets of the colonies located in young secondary forest, compared to other habitats, have a diet richer in carbohydrates and lower in prey. The abundance of carbohydrate, or the relative lack of N, in a colony’s diet influences the occurrence of the BLB microbe in P. clavata. As experimental diet manipulations can affect the facultative presence of an N-cycling microbe, a consistent diet shift in diet may facilitate the emergence of tighter symbioses.     

Floral odor learning within the hive affects honeybees’ foraging decisions

Honeybees learn odor cues quickly and efficiently when visiting rewarding flowers. Memorization of these cues facilitates the localization and recognition of food sources during foraging flights. Bees can also use information gained inside the hive during social interactions with successful foragers. An important information cue that can be learned during these interactions is food odor. However, little is known about how floral odors learned in the hive affect later decisions of foragers in the field. We studied the effect of food scent on foraging preferences when this learning is acquired directly inside the hive. By using in-hive feeders that were removed 24 h before the test, we showed that foragers use the odor information acquired during a 3-day stimulation period with a scented solution during a food-choice situation outside the nest. This bias in food preference is maintained even 24 h after the replacement of all the hive combs. Thus, without being previously collected outside by foragers, food odors learned within the hive can be used during short-range foraging flights. Moreover, correct landings at a dual-choice device after replacing the storing combs suggests that long-term memories formed within the colony can be retrieved while bees search for food in the field.     

Sexual differences in food preferences in the white stork: an experimental study

Sex differences in the foraging ecology of monomorphic species are poorly understood, due to problems with gender identification in field studies. In the current study, we used experimental conditions to investigate the food preferences of the white stork Ciconia ciconia, an opportunistic species in terms of food, but characterised by a low level of sexual dimorphism. During a 10-day experiment, 29 individuals (20 females and 9 males) were studied by means of a ‘cafeteria test’ in which the storks’ diet consisted of mammals, birds, fish, amphibians, insects and earthworms. The storks preferred food characterised by high calorific and protein values such as mammals, birds and fish. Sexes differed strongly in their preferences; males preferred mammals, whereas females preferred birds. Moreover, females consumed insects and earthworms less often than males. Interestingly, males spent significantly less time foraging than females. We have demonstrated that the white stork exhibits clear sexual differences in food preferences which are mostly attributable to differences in parental duties, physiology and anatomy.     

Experience,but not distance,influences the recruitment precision in the stingless bee <Emphasis Type="Italic">Scaptotrigona mexicana</Emphasis>

Recruitment precision, i.e. the proportion of recruits that reach an advertised food source, is a crucial adaptation of social bees to their environment. Studies with honeybees showed that recruitment precision is not a fixed feature, but it may be enhanced by factors like experience and distance. However, little is known regarding the recruitment precision of stingless bees. Hence, in this study, we examined the effects of experience and spatial distance on the precision of the food communication system of the stingless bee Scaptotrigona mexicana. We conducted the experiments by training bees to a three-dimensional artificial patch at several distances from the colony. We recorded the choices of individual recruited foragers, either being newcomers (foragers without experience with the advertised food source) or experienced (foragers that had previously visited the feeder). We found that the average precision of newcomers (95.6 ± 2.61%) was significantly higher than that of experienced bees (80.2 ± 1.12%). While this might seem counter-intuitive on first sight, this “loss” of precision can be explained by the tendency of experienced recruits to explore nearby areas to find new rewarding food sources after they had initially learned the exact location of the food source. Increasing the distance from the colony had no significant effect on the precision of the foraging bees. Thus, our data show that experience, but not the distance of the food source, affected the patch precision of S. mexicana foragers.     

Procurement of exogenous ammonia by the swallowtail butterfly, Papilio polytes, for protein biosynthesis and sperm production

How to acquire sufficient quantity of nitrogen is a pivotal issue for herbivores, particularly for lepidopterans (butterflies and moths) of which diet quality greatly differs among their life stages. Male Lepidoptera often feed from mud puddles, dung, and carrion, a behavior known as puddling, which is thought to be supplementary feeding targeted chiefly at sodium. During copulation, males transfer a spermatophore to females that contains, besides sperm, nutrients (nuptial gifts) rich in sodium, proteins, and amino acids. However, it is still poorly understood how adults, mostly nectarivores, extract nitrogen from the environment. We examined the availability of two ubiquitous inorganic nitrogenous ions in nature, viz. ammonium (or ammonia) and nitrate ions, as nutrients in a butterfly, and show that exogenous ammonia ingested by adult males of the swallowtail, Papilio polytes, can serve as a resource for protein biosynthesis. Feeding experiments with ¹⁵N-labeled ammonium chloride revealed that nitrogen was incorporated into eupyrene spermatozoa, seminal protein, and thoracic muscle. Ammonia uptake by males significantly increased the number of eupyrene sperms in the reproductive tract tissues. The females also had the capacity to assimilate ammonia into egg protein. Consequently, it is evident that acquired ammonia is utilized for the replenishment of proteins allocable for reproduction and somatic maintenance. The active exploitation of exogenous ammonia as a nutrient by a butterfly would foster better understanding of the foraging and reproductive strategies in insects.     

The cues have it; nest-based, cue-mediated recruitment to carbohydrate resources in a swarm-founding social wasp

This study explores whether or not foragers of the Neotropical swarm-founding wasp Polybia occidentalis use nest-based recruitment to direct colony mates to carbohydrate resources. Recruitment allows social insect colonies to rapidly exploit ephemeral resources, an ability especially advantageous to species such as P. occidentalis, which store nectar and prey in their nests. Although recruitment is often defined as being strictly signal mediated, it can also occur via cue-mediated information transfer. Previous studies indicated that P. occidentalis employs local enhancement, a type of cue-mediated recruitment in which the presence of conspecifics at a site attracts foragers. This recruitment is resource-based, and as such, is a blunt recruitment tool, which does not exclude non-colony mates. We therefore investigated whether P. occidentalis also employs a form of nest-based recruitment. A scented sucrose solution was applied directly to the nest. This mimicked a scented carbohydrate resource brought back by employed foragers, but, as foragers were not allowed to return to the nest with the resource, there was no possibility for on-nest recruitment behavior. Foragers were offered two dishes—one containing the test scent and the other an alternate scent. Foragers chose the test scent more often, signifying that its presence in the nest induces naïve foragers to search for it off-nest. P. occidentalis, therefore, employs a form of nest-based recruitment to carbohydrate resources that is mediated by a cue, the presence of a scented resource in the nest.     

Chemical compounds of the foraging recruitment pheromone in bumblebees

When the frenzied and irregular food-recruitment dances of bumblebees were first discovered, it was thought that they might represent an evolutionary prototype to the honeybee waggle dance. It later emerged that the primary function of the bumblebee dance was the distribution of an alerting pheromone. Here, we identify the chemical compounds of the bumblebee recruitment pheromone and their behaviour effects. The presence of two monoterpenes and one sesquiterpene (eucalyptol, ocimene and farnesol) in the nest airspace and in the tergal glands increases strongly during foraging. Of these, eucalyptol has the strongest recruitment effect when a bee nest is experimentally exposed to it. Since honeybees use terpenes for marking food sources rather than recruiting foragers inside the nest, this suggests independent evolutionary roots of food recruitment in these two groups of bees.     

Social familiarity modulates group living and foraging behaviour of juvenile predatory mites

Environmental stressors during early life may have persistent consequences for phenotypic development and fitness. In group-living species, an important stressor during juvenile development is the presence and familiarity status of conspecific individuals. To alleviate intraspecific conflicts during juvenile development, many animals evolved the ability to discriminate familiar and unfamiliar individuals based on prior association and use this ability to preferentially associate with familiar individuals. Assuming that familiar neighbours require less attention than unfamiliar ones, as predicted by limited attention theory, assorting with familiar individuals should increase the efficiency in other tasks. We assessed the influence of social familiarity on within-group association behaviour, development and foraging of juvenile life stages of the group-living, plant-inhabiting predatory mite Phytoseiulus persimilis. The observed groups consisted either of mixed-age familiar and unfamiliar juvenile mites or of age-synchronized familiar or unfamiliar juvenile mites or of pairs of familiar or unfamiliar larvae. Overall, familiar mites preferentially grouped together and foraged more efficiently, i.e. needed less prey at similar developmental speed and body size at maturity, than unfamiliar mites. Preferential association of familiar mites was also apparent in the inter-exuviae distances. Social familiarity was established by imprinting in the larval stage, was not cancelled or overridden by later conspecific contacts and persisted into adulthood. Life stage had an effect on grouping with larvae being closer together than nymphal stages. Ultimately, optimized foraging during the developmental phase may relax within-group competition, enhance current and future food supply needed for optimal development and optimize patch exploitation and leaving under limited food.     

Nesting habits shape feeding preferences and predatory behavior in an ant genus

We tested if nesting habits influence ant feeding preferences and predatory behavior in the monophyletic genus Pseudomyrmex (Pseudomyrmecinae) which comprises terrestrial and arboreal species, and, among the latter, plant-ants which are obligate inhabitants of myrmecophytes (i.e., plants sheltering so-called plant-ants in hollow structures). A cafeteria experiment revealed that the diet of ground-nesting Pseudomyrmex consists mostly of prey and that of arboreal species consists mostly of sugary substances, whereas the plant-ants discarded all the food we provided. Workers forage solitarily, detecting prey from a distance thanks to their hypertrophied eyes. Approach is followed by antennal contact, seizure, and the manipulation of the prey to sting it under its thorax (next to the ventral nerve cord). Arboreal species were not more efficient at capturing prey than were ground-nesting species. A large worker size favors prey capture. Workers from ground- and arboreal-nesting species show several uncommon behavioral traits, each known in different ant genera from different subfamilies: leaping abilities, the use of surface tension strengths to transport liquids, short-range recruitment followed by conflicts between nestmates, the consumption of the prey’s hemolymph, and the retrieval of entire prey or pieces of prey after having cut it up. Yet, we never noted group ambushing. We also confirmed that Pseudomyrmex plant-ants live in a kind of food autarky as they feed only on rewards produced by their host myrmecophyte, or on honeydew produced by the hemipterans they attend and possibly on the fungi they cultivate.     

How floral odours are learned inside the bumblebee (Bombus terrestris) nest

Recruitment in social insects often involves not only inducing nestmates to leave the nest, but also communicating crucial information about finding profitable food sources. Although bumblebees transmit chemosensory information (floral scent), the transmission mechanism is unknown as mouth-to-mouth fluid transfer (as in honeybees) does not occur. Because recruiting bumblebees release a pheromone in the nest that triggers foraging in previously inactive workers, we tested whether this pheromone helps workers learn currently rewarding floral odours, as found in food social learning in rats. We exposed colonies to artificial recruitment pheromone, paired with anise scent. The pheromone did not facilitate learning of floral scent. However, we found that releasing floral scent in the air of the colony was sufficient to trigger learning and that learning performance was improved when the chemosensory cue was provided in the nectar in honeypots; probably because it guarantees a tighter link between scent and reward, and possibly because gustatory cues are involved in addition to olfaction. Scent learning was maximal when anise-scented nectar was brought into the nest by demonstrator foragers, suggesting that previously unidentified cues provided by successful foragers play an important role in nestmates learning new floral odours.     

Evaluating the sustainability of diets–combining environmental and nutritional aspects

This study examined two methods for jointly considering the environmental impact and nutritional quality of diets, which is necessary when designing policy instruments promoting sustainable food systems. Both methods included energy content and 18 macro- and micronutrients in the diet, the climate impact, land use and biodiversity damage potential. In Method 1, the content of different nutrients in the diet was normalised based on recommended intake or upper levels for average daily intake and presented together with the environmental impacts, which were normalised according to estimated sustainable levels. In Method 2, the nutritional quality of different diets was considered by calculating their nutrient density score, and the environmental impact was then expressed per nutrient density score. Three diets were assessed; a diet corresponding to Nordic recommendations, the current average Swedish diet and a lifestyle Low Carbohydrate-High Fat (LCHF) diet. Method 1 clearly showed that the climate impact was far beyond the sustainable level for all diets, while land use was within the sustainability limit for the recommended diet, but not the other two. Comparisons based on nutrient density scores depended on the score used, but the current and LCHF diets had more impact than the recommended diet (less livestock products) for all but one score. Over- and under-consumption of nutrients were clearly shown by Method 1 but not possible to distinguish with Method 2, as normalisation was not possible, making it difficult to evaluate the absolute scale of the impacts when nutrient density scores were used. For quantitative information on the environmental and nutritional impacts of diets as support in decision-making processes, it is important that data presentation is transparent. There is limited value in reducing results to a low number of indicators that are easy to read, but difficult to interpret, e.g. nutrient density score. Method 1 allows combined assessment of diets regarding environmental impact and nutritional intake and could be useful in dietary planning and in development of dietary recommendations and other policy instruments to achieve more sustainable food systems.     

Influence of interspecific competition on the recruitment behavior and liquid food transport in the tramp ant species Pheidole megacephala

This study was conducted on the reactions of Pheidole megacephala scouts when finding liquid food sources situated on territories marked by competing dominant ant species or on unmarked, control areas to see if the number of recruited nestmates is affected and if soldiers behave in ways adapted to the situation. We show that scouts recruit more nestmates, particularly soldiers, on marked rather than on unmarked areas. This recruitment allows P. megacephala to organize the defence and rapid depletion of these food sources prior to any contact with competitors. Soldiers can carry liquid foods both (1) in their crops like other Myrmicinae and (2), in a new finding concerning myrmicine ants, under their heads and thoraxes like certain poneromorph genera because the droplets adhere through surface tension strengths. Later, the liquids stored in the crop are distributed to nestmates through regurgitations during trophallaxis and the external droplets are distributed through social buckets, or the mode of liquid food transfer common in poneromorphs. Their flexibility to use or not use the latter technique, based on the situation, corroborates other reports that Pheidole soldiers have a relatively large behavioral repertoire.     

Microbial degradation of usnic acid in the reindeer rumen

Reindeer (Rangifer tarandus) eat and utilize lichens as an important source of energy and nutrients in winter. Lichens synthesize and accumulate a wide variety of phenolic secondary compounds, such as usnic acid, as a defense against herbivores and to protect against damage by UV-light in solar radiation. We have examined where and to what extent these phenolic compounds are degraded in the digestive tract of the reindeer, with particular focus on usnic acid. Three male reindeer were given ad libitum access to a control diet containing no usnic acid for three weeks and then fed lichens ad libitum (primarily Cladonia stellaris) containing 9.1 mg/g DM usnic acid for 4 weeks. Usnic acid intake in reindeer on the lichen diet was 91–117 mg/kg BM/day. In spite of this, no trace of usnic acid or conjugates of usnic acid was found either in fresh rumen fluid, urine, or feces. This suggests that usnic acid is rapidly degraded by rumen microbes, and that it consequently is not absorbed by the animal. This apparent ability to detoxify lichen phenolic compounds may gain increased importance with future enhanced UV-B radiation expected to cause increased protective usnic acid/phenol production in lichens.