Social Environment Influences Performance in a Cognitive Task in Natural Variants of the Foraging Gene

In Drosophila melanogaster, natural genetic variation in the foraging gene affects the foraging behaviour of larval and adult flies, larval reward learning, adult visual learning, and adult aversive training tasks. Sitters (for ^s) are more sedentary and aggregate within food patches whereas rovers (for^R) have greater movement within and between food patches, suggesting that these natural variants are likely to experience different social environments. We hypothesized that social context would differentially influence rover and sitter behaviour in a cognitive task. We measured adult rover and sitter performance in a classical olfactory training test in groups and alone. All flies were reared in groups, but fly training and testing were done alone and in groups. Sitters trained and tested in a group had significantly higher learning performances compared to sitters trained and tested alone. Rovers performed similarly when trained and tested alone and in a group. In other words, rovers learning ability is independent of group training and testing. This suggests that sitters may be more sensitive to the social context than rovers. These differences in learning performance can be altered by pharmacological manipulations of PKG activity levels, the foraging (for) gene''s gene product. Learning and memory is also affected by the type of social interaction (being in a group of the same strain or in a group of a different strain) in rovers, but not in sitters. These results suggest that for mediates social learning and memory in D. melanogaster.     

Rover/sitterDrosophila melanogaster larval foraging polymorphism as a function of larval development,food-patch quality,and starvation

The genetically based rover/sitter behavioral difference in Drosophila melanogasterlarval foraging is expressed throughout most of the larval instars when larvae forage on food patches of differing food quality. The amount of locomotor behavior decreases when third-instar larvae of both rover and sitter strains are starved just prior to the behavioral test. Such strain differences in locomotor behavior are maintained despite the starvation-induced decrease in locomotion found in both strains. Measurements of larval body length and width, taken at 24, 48, 72, and 96 h posthatching, reveal that rover and sitter larval growth rates do not differ. The finding that rover/sitter differences are expressed in a variety of environments and throughout the majority of the larval instars should aid in attempts to uncover selection pressures which may differentially affect the two morphs in environmentally heterogeneous natural populations.     

Natural selection in the laboratory for a change in resistance byDrosophila melanogaster to the parasitoid waspAsobara tabida

The selection response of the polymorphic hostD. melanogaster (Meigen) to the braconid waspA. tabida (Nees) is addressed. Cages of flies with and without wasps were initiated with a population ofD. melanogaster that exhibited variation both in larval foraging behavior and in encapsulation ability. Encapsulation ability was measured as the proportion of parasitized larvae that produce a hardened capsule which encapsulates the wasp egg and ultimately kills the wasp larva. We determined whether the host population changed its encapsulation ability and/or its foraging behavior in response to the wasp. Both species were collected from a local orchard whereA. tabida is the only wasp known to parasitizeD. melanogaster larvae. The naturally occurring genetic polymorphism for rover and sitter larval foraging behavior inD. melanogaster is also found in this field population.A. tabida's vibrotactic search behavior enables it to detect rover more frequently than sitter larvae. Rover larvae move significantly more while feeding than do sitter larvae. In this field population, rover larvae also show higher encapsulation abilities than do sitter larvae. Six cage populations, three without wasps and three with wasps, each containing an equal mixture of rover and sitter flies, were established in the laboratory and maintained for 19 fly generations. Selection pressure in the laboratory was similar to that found in the field population from which the flies and wasps were derived. We found that larvae from cages with wasps developed a significantly higher frequency of encapsulation than those reared without wasps. We were, however, unable to detect a change in larval movement (rover or sitter behavior) in larvae from cages subject to selection from wasps compared to larvae from cages containing no wasps. This may have resulted from a balance between two selective forces, selection against rovers by the wasps' use of vibrotaxis, and selection for rovers resulting from their increased encapsulation abilities     

Foraging behaviour in Drosophila larvae: mushroom body ablation

Drosophila larvae and adults exhibit a naturally occurring genetically based behavioural polymorphism in locomotor activity while foraging. Larvae of the rover morph exhibit longer foraging trails than sitters and forage between food patches, while sitters have shorter foraging trails and forage within patches. This behaviour is influenced by levels of cGMP-dependent protein kinase (PGK) encoded by the foraging (for) gene. Rover larvae have higher expression levels and higher PGK activities than do sitters. Here we discuss the importance of the for gene for studies of the mechanistic and evolutionary significance of individual differences in behaviour. We also show how structure-function analysis can be used to investigate a role for mushroom bodies in larval behaviour both in the presence and in the absence of food. Hydroxyurea fed to newly hatched larvae prevents the development of all post-embryonically derived mushroom body (MB) neuropil. This method was used to ablate MBs in rover and sitter genetic variants of foraging to test whether these structures mediate expression of the foraging behavioural polymorphism. We found that locomotor activity levels during foraging of both the rover and sitter larval morphs were not significantly influenced by MB ablation. Alternative hypotheses that may explain how variation in foraging behaviour is generated are discussed.     

Chaser (Csr), a New Gene Affecting Larval Foraging Behavior in Drosophila Melanogaster

Chaser (Csr) was uncovered in a gamma mutagenesis screen to identify genes that modify the larval foraging behavior of sitters to rovers. Rover larvae have significantly longer path lenghts than sitters while foraging on a yeast and water paste. This difference is influenced by one major gene, foraging (for), which has two naturally occurring alleles, for(R) (rover) and for(s) (sitter). In a mutagenesis screen for modifiers of for, we identified three lines with viable mutations on chromosome 3 that alter foraging behavior. Each of these mutations increased larval path lengths in for(s)/for(s) larvae in a dominant fashion, and were not separable by recombination. These mutations are therefore probably allelic and define a new gene that we have called Csr. Csr was genetically localized using the lethal-tagging technique. This technique resulted in seven lines with a significant decrease in larval path-length and recessive lethal mutations on chromosome 3. We refer to these as reverted Csr (Csr(rv)) lines. Deficiencies that uncovered cytologically visible chromosome rearrangements in three of the seven reverted lines were used in a complementation analysis. In this way we mapped the lethal mutations in the Csr(rv) lines to cytological region 95F7-96A1 on the right arm of chromosome 3.     

Interactions between searching strategies ofDrosophila parasitoids and the polymorphic behavior of their hosts

Two strains of Drosophila melanogaster, rover and sitter, differing in locomotion while foraging were simultaneously exposed to females of either Leptopilina boulardi or Ganaspis xanthopoda (parasitic Hymenoptera). These two parasitoids show different modes of host-searching behavior, ovipositor searching, or vibrotaxis, respectively. L. boulardi parasitized the sitter host strain significantly more than the rover. In contrast, G. xanthopoda parasitized the rover strain more than the sitter. In one case, L. boulardi selected far more sitters than rovers in population cage experiments. We also describe the frequencies of rovers and sitters in three natural populations where the local parasitoid community may have partially contributed to the differences in rover and sitter frequencies.     

Foraging for solitarily and gregariously feeding caterpillars: A comparison of two related parasitoid species (Hymenoptera: Braconidae)

In the present study we apply a comparative approach, in combination with experimentation, to study behavior of two parasitoid species that attack caterpillar hosts with different feeding strategies (gregarious or solitary). In a semifield setup, consisting of clean cabbage plants and plants infested with one of two host species, the foraging behavior of the specialistCotesia rubecula, on obligate parasitoid of solitarily feedingPieris rapae larvae, was compared to that of the generalistCotesia glomerata, a polyphagous parasitoid of several Pieridae species (mainly the gregariously feedingPieris brassicae).Cotesia glomerata displayed equal propensity to search for and parasitize larvae of both host species. AlthoughC. glomerata exhibited a relatively plastic foraging behavior in that it searched differently under different host distribution conditions, its behavior seems more adapted to search for gregariously feeding hosts. Females exhibited a clear area-restricted search pattern and were more successful in finding the gregariously feeding caterpillars.Cotesia rubecula showed a higher propensity to search forP. rapae than forP. brassicae, i.e., females left the foraging setup significantly earlier when their natural hostP. rapae was not present.C. rubecula showed a more fixed foraging behavior, which seems adapted to foraging for solitarily feeding host larvae. In a setup with onlyP. rapae larvae, the foraging strategies of the two parasitoid species were quite similar. In a choice situationC. glomerata did not show a preference for one of the host species, whileCotesia rubecula showed a clear preference for its natural host species. The latter was shown by several behavioral parameters such as the number of first landings, allocation of search time, and percentage parasitization.     

Foraging behavior and encapsulation ability ofDrosophila melanogaster larvae: Correlated polymorphisms? (Diptera: Drosophilidae)

Larvae ofDrosophila melanogaster are polymorphic with respect to their foraging behavior. Rovers move around, while sitters stay more in one place. This difference in movements while foraging may result in differences in the rate at which these larvae are attacked by hymenopteran parasitoids, especially by those that locate their hosts by reacting to the vibrations they make. From previous work it is known thatD. melanogaster larvae show intra- and interpopulation variation in their ability to destroy parasitoid eggs by encapsulation. If rovers have a higher probability to be attacked by a parasitoid, they may have a higher developed encapsulation system as compensation for this higher attack probability. Experiments show that rovers are indeed more often attacked byAsobara tabida, a vibrotactic (=reacting to vibrations) parasitoid, than sitters. However, foraging behavior and encapsulation ability appear to be independent of each other inD. melanogaster. This shows that the large variation between populations in encapsulation ability is not a reflection of the relative proportion of rovers and sitters in the populations. It also shows that parasitoids can be an important factor in the maintenance of the foraging behavior polymorphism, because a higher encapsulation ability is not a compensation for a higher attack probability.     

Alleles underlying larval foraging behaviour influence adult dispersal in nature

The dispersal and migration of organisms have resulted in the colonisation of nearly every possible habitat and ultimately the extraordinary diversity of life. Animal dispersal tendencies are commonly heterogeneous (e.g. long vs. short) and non‐random suggesting that phenotypic and genotypic variability between individuals can contribute to population‐level heterogeneity in dispersal. Using laboratory and field experiments, we demonstrate that natural allelic variation in a gene underlying a foraging polymorphism in larval fruit flies (for), also influences their dispersal tendencies as adults. Rover flies (for^R; higher foraging activity) have consistently greater dispersal tendencies and are more likely to disperse longer distances than sitter flies (for^s; lower foraging activity). Increasing for expression in the brain and nervous system increases dispersal in sitter flies. Our study supports the notion that variation in dispersal can be driven by intrinsic variation in food‐dependent search behaviours and confirms that single gene pleiotropic effects can contribute to population‐level heterogeneity in dispersal.     

Search orientation in adultDrosophila melanogaster: Responses of rovers and sitters to resource dispersion in a food patch

Drosophila melanogasteradults were employed in single resource patches of varying density and size and in a multiple-patch array to determine the degree to which resource dispersion influences searching success. Individuals from rover and sitter selected lines, with extreme genotypes for local search duration, are not as successful as control-line (wild-type) flies in locating sucrose drops in single patches varying in size and density. The number of new drops located differed significantly between fly lines in all patch types, except in a high-density patch, and within each fly line over the different patch sizes and densities. The similarities in number of drops found by rovers and sitters in all patch types are not reflected in the time periods spent searching. In the multiple-patch array sitters never left the central patch, whereas most rovers and con-trol-line flies found additional patches. The proximate explanations for the success or failure of the three fly lines in different patch sizes and densities relate to the looping locomotor pattern characterizing local search in D. melanogaster.The reactivation of searching each time a drop is ingested or revisited keeps an individual in the immediate vicinity of the last encountered resource. Flies from the selected lines, each exhibiting extreme types of locomotor patterns, leave patches relatively unexploited because local search consists either of rapid, nearly linear movement away from a drop in rovers or of relatively long bouts of local search in sitters, which promotes revisiting rather than locating new drops. Control-line flies locate more drops than either rovers or sitters and in less time than sitters, suggesting that their intermediate phenotype for search behavior allows for more flexibility in searching in various patch sizes and resource densities. The results are discussed with reference to environmental and physiological factors that may modify searching behavior and, possibly, enhance the survival of individuals with extreme genotypes.     

Abundance,size, and feeding success of larval shortnose suckers and Lost River suckers from different habitats of the littoral zone of Upper Klamath Lake

We examined near-shore habitat use by larval shortnose and Lost River suckers in the lower Williamson River and Upper Klamath Lake of south-central Oregon. Emergent macrophytes Scirpus, Sparganium and Polygonum supported significantly more, larger, and better-fed larvae than submergent macrophytes, woody vegetation, or open water. Abundance, size, and gut fullness were similar for sucker larvae collected from different emergent macropytes. During the larval period, there was no evidence of density dependant effects or habitat shifts. Ranked catch per unit effort data indicated potential predators also were more likely to use emergent macrophytes, but ordination indicated larvae and potential predators were differentially distributed along a vegetation structure-water depth gradient with larvae in shallow vegetated areas. Between-habitat differences appeared to be due to larval sucker selection for, or better survival in, emergent macrophytes, rather than differential access or exclusion from other habitats. The importance of emergent macrophytes appears to be related to increased foraging success and reduced predation. Because larvae in emergent macrophytes have a size and gut fullness advantage, the amount of emergent habitat could affect early survival. However, interannual differences in recruitment to the adult population may or may not be dependent on larval dynamics. Our results suggest larval sucker access to emergent macrophytes may be necessary, but perhaps not sufficient, for promoting good year class formation.     

Rover/sitter foraging behavior inDrosophila melanogaster: Genetic localization to chromosome2L using compound autosomes

Genetic control of the rover/sitter behavioral polymorphism in Drosophila melanogasterlarvae was localized to the left arm of chromosome 2.Ten independent left and right compound second chromosomes were generated in isogenic rover and sitter strains by gamma irradiation and substituted into 25 different lines. Comparisons were made between lines to determine the chromosome arm contributions to rover/sitter phenotype expression.     

Evolution of foraging behaviour in response to chronic malnutrition in Drosophila melanogaster

Chronic exposure to food of low quality may exert conflicting selection pressures on foraging behaviour. On the one hand, more active search behaviour may allow the animal to find patches with slightly better, or more, food; on the other hand, such active foraging is energetically costly, and thus may be opposed by selection for energetic efficiency. Here, we test these alternative hypotheses in Drosophila larvae. We show that populations which experimentally evolved improved tolerance to larval chronic malnutrition have shorter foraging path length than unselected control populations. A behavioural polymorphism in foraging path length (the rover-sitter polymorphism) exists in nature and is attributed to the foraging locus (for). We show that a sitter strain (for(s2)) survives better on the poor food than the rover strain (for(R)), confirming that the sitter foraging strategy is advantageous under malnutrition. Larvae of the selected and control populations did not differ in global for expression. However, a quantitative complementation test suggests that the for locus may have contributed to the adaptation to poor food in one of the selected populations, either through a change in for allele frequencies, or by interacting epistatically with alleles at other loci. Irrespective of its genetic basis, our results provide two independent lines of evidence that sitter-like foraging behaviour is favoured under chronic larval malnutrition.     

Patch Time Allocation by the Parasitoid Diadegma semiclausum (Hymenoptera: Ichneumonidae). I. Effect of Interpatch Distance

We observed the foraging behavior of Diadegma semiclausum (Hymenoptera:Ichneumonidae), a larval parasitoid of the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae), in a wind tunnel to determine how interpatch distance affects patch time allocation. Individual female wasps were released onto an experimental patch infested with host larvae and were allowed freely to leave for an identically extrapatch placed upwind of the experimental patch with varying interpatch distances. The effects of interpatch distance and within-patch foraging experience on the patch-leaving tendency of the parasitoid were analyzed bymeans of the proportional hazards model. Increasing interpatch distance andunsuccessful host encounter as a result of host defense decreased the patch-leaving tendency, while successful oviposition and unsuccessful search time since last oviposition increased the patch-leaving tendency. Asa result, both patch residence time and number of ovipositions by D. semiclausum increased with increasing interpatch distance, which appears to agree with the general predictions of the marginal value theorem that a parasitoid should stay longer and parasitize more hosts with increasing interpatch distance.     

Host–parasitoid interaction as affected by interkingdom competition

Although still underrepresented in ecological research, competitive interactions between distantly related organisms (so-called “interkingdom competition”) are expected to be widespread in various ecosystems, with yet unknown consequences for, e.g. trophic interactions. In the model host–parasitoid system Drosophila melanogaster–Asobara tabida, toxic filamentous fungi have been shown to be serious competitors that critically affect the density-dependent survival of host Drosophila larvae. This study investigates the extent to which the competing mould Aspergillus niger affects key properties of the well-studied Drosophila–parasitoid system and how the host–parasitoid interaction influences the microbial competitor. In contrast to slightly positive density-dependent host mortality under mould-free conditions, competing A. niger mediated a strong Allee effect for parasitised larvae, i.e. mortality decreased with increasing larval density. It was found that the common toxic fungal metabolite kojic acid is not responsible for higher death rates in parasitised larvae. Single parasitised Drosophila larvae were less harmful to fungal reproduction than unparasitised larvae, but this effect vanished with an increase in larval density. As predicted from the negative effect of fungi on host survival and thus on parasitoid fitness at low larval densities, A. tabida females spent less time foraging in fungus-infested patches. Interestingly, even though high host larval densities increased host survival, parasitoids still reduced their search efforts in fungus-infested patches, indicating a benefit for host larvae from feeding in the presence of noxious mould. Thus, this experimental study provides evidence of the potentially important role of interkingdom competition in determining trophic interactions in saprophagous animal communities and the dynamics of both host–parasitoid and microbial populations.     

Larval Sociality in Three Species of Central-place Foraging Lappet Moths (Lepidoptera: Lasiocampidae): A Comparative Survey

We studied three species of Lasiocampidae with social, tent-building caterpillars in Northern Bavaria, viz. Eriogaster lanestris, Eriogaster catax, and Malacosoma neustria. We used key life-history data (number of larval instars, sizes and weights of eggs, caterpillars, and moths, size of egg clutches) as well as behavioral data (activity patterns, tent-building behavior, trail following behavior) for a comparative study. Although larvae of all three species are active only in spring, show overlapping habitat requirements, and use the same major host-plant (Prunus spinosa) with only minor differences in phenology, they show markedly different life-history and behavioral strategies.E. catax lays comparatively few but large eggs while E. lanestris lays more but smaller eggs. M. neustria lays the smallest eggs but large clusters. E. lanestris caterpillars build a large tent with an accessible interior while those of E. catax build a small tent that is only used as a resting and molting platform. M. neustria shows a flexible behavior, may abandon the primary tent and build a new one several times. M. neustria colonies also subdivide and reunite regularly while Eriogaster colonies stay together until larvae become solitary. In E. lanestris all tentmates of a colony are highly synchronized while foraging or resting. Instead, in E. catax small subgroups leave the tent for foraging while at every time the majority rests on the tent. M. neustria caterpillars forage more or less individually and only synchronize by night. Results are discussed in relation to other species of the genera Eriogaster and Malacosoma and with regard to the evolution and diversification of caterpillar sociality.     

The Effects of Water,Season, and Colony Composition on Foraging Preferences of <Emphasis Type="Italic">Pheidole ceres</Emphasis> [Hymenoptera: Formicidae]

Field colonies of the ant Pheidole ceres were presented with a choice between a protein source and a carbohydrate source, under wet and dry conditions, at three different times in the year. These time periods corresponded with different reproductive (the production of sexuals) and growth (the production of workers) stages of the colony. Moisture had no effect on the forging behavior of P. ceres but the colonies did change their foraging preferences during different times of the year. This behavior correlated with the amount of larvae in the colony. However, lab experiments demonstrated that larvae did not directly influence the foraging decisions of the workers but that adult reproductives did.     

The Importance of Behavioral Plasticity for Maximizing Foraging Efficiency in Frugivorous Lepidopteran Larvae

In this study, we present evidence that the larvae of Acrobasis vaccinii (Lepidoptera: Pyralidae), a species that feeds on cranberry fruit, are able to take into account at least three cues (fruit size, fruit color, and the distance between fruits) when searching for food. In laboratory experiments, the relative impact of each cue depended on which cues were presented in a given bioassay. Fruit color was the dominant cue in some contexts (e.g., larvae showed a significant perference for green fruit over red ones regardless of fruit size when fruits were equidistant from the larvae) but not in others (e.g., when given a choice between a large red fruit placed close to the larvae and a small green fruit placed farther away, a significantly higher proportion of larvae chose the former). This plasticity in foraging behavior allows larvae to maximize foraging efficiency under conditions of differing fruit and larval densities, which this species experiences in nature.     

Tomato-aphid-hoverfly: a tritrophic interaction incompatible for pest management

Trichome-based tomato resistance offers the potential to reduce pesticide use, but its compatibility with biological control remains poorly understood. We evaluated Episyrphus balteatus De Geer (Diptera, Syrphidae), an efficient aphidophagous predator, as a potential biological control agent of Myzus persicae Sulzer (Hemiptera, Aphididae) on trichome-bearing tomato cultivars. Episyrphus balteatus’ foraging and oviposition behavior, as well as larval mobility and aphid accessibility, were compared between two tomato cultivars (Lycopersicon esculentum Mill. ‘Moneymaker’ and ‘Roma’) and two other crop plants; broad bean (Vicia faba L.) and potato (Solanum tuberosum L.). Hoverfly adults landed and laid more eggs on broad beans than on three species of Solanaceae. Hoverfly larval movement was drastically reduced on tomato, and a high proportion of hoverfly larvae fell from the plant before reaching aphid prey. After quantifying trichome abundance on each of these four plants, we suggest that proprieties of the plant surface, specifically trichomes, are a key factor contributing to reduced efficacy of E. balteatus as a biological agent for aphid control on tomatoes. Handling editor: Stanislaw Gorb