The geometry of search movements of insects in plant canopies

The aim of this study was to provide a framework for describingand understanding the geometry of movement of insects foragingwithin complex plant canopies where the insect is exposed tovarying stimuli. We used the apple maggot fly, Rhagoletis pomonella(Walsh) (Diptera: Tephritidae), foraging in apple trees devoidof fruit as our model system. The framework provides the nullhypothesis required for inferring the influence of externalstimuli, such as fruit color and odor, on the paths of foragingflies. We mapped trees into cells, released preconditioned fliesin caged trees, and recorded their behavior and location. Fliesmoved mainly to the nearest neighbor cells, but displacementwithin a wide range of distances was observed. The model closestto observations is a random walk with a position-dependent biasin the vertical component of movement. Four other models werebuilt, spanning a range of simplifications in the rules determiningthe vertical component of movement We used the concept of avoidanceof self-crossing in a searching path for defining efficiencyof movement Flies were quite efficient at visiting almost asmany different cells as possible. Comparisons of assumptionsand predictions of the five models revealed that this efficiencyis due to the small number of steps, the location of the startingcell, and a strong tendency to move upward in its vicinity.We discuss the selection pressures on movement rules: pressurefrom predators may explain the short hops, while the sensoryecology of fruit finding and the avoidance of sites alreadyvisited by other flies or by the same fly may explain the position-dependentupward bias. Strong similarities between the rules for the verticalcomponent of movement of one simplified model and the observationslead us to believe that canopy architecture influences insectmovement not only by defining the set of locations that theinsect can visit using predefined rules for movement but alsoby defining the rules of movement     

Habitat architecture and trophic interaction strength in a river: riffle-scale effects

Invertebrate algal grazer densities were manipulated in a temperate river to discover the impact of differences in riffle-scale architectural complexity on the strength of the trophic interaction between grazers and epilithic algae. Animal densities were manipulated by manual removal in architecturally complex boulder-cobble riffles and simpler bedrock riffles, with the complexity of smaller-scale architecture held constant. Responses in algal density were recorded before and after a month of manipulations, together with grazer colonization rate and body sizes. The experiment was carried out in winter and again in summer. The interaction between grazers and algae differed between habitats and seasons. In winter, when algae were growing, the more complex rifflescale architecture in the boulder-cobble riffles created a refuge from grazing for algae. This was probably the result of the movement abilities of the grazers interacting with habitat architecture, and potentially also due to the control of predatory fish densities by habitat architecture resulting in greater predation pressure on grazers in boulder-cobble riffles. Therefore the impact of highly complex riffle-scale architecture was to weaken the strength of the trophic interaction between algae and their grazers by reducing grazer densities, while potentially strengthening the trophic interaction between grazers and their fish predators.     

Resting sites,edge effects and dispersion of a polyphagous Bactrocera fruit fly within crops of different architecture

The spot or strip application of poisoned protein bait is a lure‐and‐kill technique used for the management of fruit flies. Knowledge of where flies occur in the crop environment is an important part of maximizing the efficacy of this tool. Bactrocera tryoni is a polyphagous pest of horticulture for which very little is known about its distribution within crops. With particular reference to edge effects, we monitored the abundance of B. tryoni in two crops of different architecture; strawberry and apple. In strawberries, we found more flies on the crop edge early in the fruiting season, which lessened gradually and eventually disappeared as the season progressed. In apple orchards, no such edge effect was observed and flies were found equally throughout the orchard. We postulated these differences may be due to differences in crop height (high vs. short) and/or crop canopy architecture (opened and branched in apple, dense and closed in strawberry). In a field cage trial, we tested these predictions using artificial plants of different height and canopy condition. Height and canopy structure type had no significant effects on fly oviposition and protein feeding, but the ‘apple’ type canopy significantly influenced resting. We thus postulate that there was an edge effect in strawberry because the crop was not providing resting sites and flies were doing so in vegetation around the field margins. The finding that B. tryoni shows different resting site preferences based on plant architecture offers the potential for strategic manipulation of the fly through specific border or inter‐row plantings.     

Antagonist effects of non-host fruit volatiles on discrimination of host fruit by Rhagoletis flies infesting apple (Malus pumila), hawthorn (Crataegus spp.), and flowering dogwood (Cornus florida)

In previous flight‐tunnel tests Rhagoletis pomonella (Walsh) (Diptera: Tephritidae) flies originating from domestic apple (Malus pumila), hawthorn (Crataegus spp.), and flowering dogwood (Cornus florida), displayed greater numbers of upwind flights to blends of volatiles identified from their natal fruit compared to non‐natal fruit. Here, we show that when certain non‐host volatiles were added to the host blend, significantly fewer apple, hawthorn, and dogwood flies exhibited sustained upwind flight to the source. Specifically, the upwind flight of apple flies to the apple blend was significantly antagonized by the addition of the hawthorn or dogwood blends, the addition of 3‐methylbutan‐1‐ol alone (a key volatile for hawthorn and dogwood flies), or the combination of 3‐methylbutan‐1‐ol and another key dogwood volatile, 1‐octen‐3‐ol. Similarly, the upwind flight of dogwood and hawthorn flies to their respective natal blends was antagonized by the addition of the apple blend or the key apple volatile butyl hexanoate. Experiments were also conducted to determine whether non‐natal fruit volatiles could disrupt the close‐range flight response of flies to the visual stimulus of fruit alone, represented by an odorless red sphere. Tests with apple‐origin flies showed that when the hawthorn blend, the dogwood blend, or the key antagonist volatiles from each (3‐methylbutan‐1‐ol and 1‐octen‐3‐ol) were added to a red sphere fruit mimic, significantly lower proportions of flies were captured, compared with captures when no odor was present. Our results support the hypothesis that agonist and antagonist properties of fruit volatiles can play an important role in host recognition/discrimination by Rhagoletis flies.     

Prior experience influences the fruit residence of male apple maggot flies,Rhagoletis pomonella

Male apple maggot flies spend considerable time residing on individual host fruit as territories on which they force-copulate arriving females in search of oviposition sites. Here, we present evidence from investigations in nature and the laboratory that shows the propensity of males to reside on a hawthorn or apple fruit as a territory is significantly modifiable through prior experience with fruit and, hence, involves learning. Previous studies revealed that after a female apple maggot fly, Rhagoletis pomonella, arrived on a host hawthorn or apple fruit, its propensity to accept or reject that fruit for egg-laying was similarly modifiable through prior fruit-exposure experience and also involved learning. We discuss how host fruit learning in males and females, in concert with genetic-based differences in host fruit residence and acceptance behavior between populations of flies originating from hawthorn and apple, could give rise to a reduction in gene flow between populations of flies on these two host types.     

Discrepancy in laboratory and field attraction of apple fruit moth Argyresthia conjugella to host plant volatiles

Abstract.  Apple fruit moth Argyresthia conjugella is a specialist seed predator of rowan Sorbus aucuparia . Large-scale synchronous fluctuation of seed production in rowan (i.e. named masting) drives the apple fruit moth to seek alternative host plants such as apple, during years when rowan berries are not available for oviposition. The role of plant volatile compounds in the attraction of gravid apple fruit moth females is studied in a laboratory wind tunnel. Volatiles from rowan branches with green berries stimulate female moths to fly upwind and to land at the odour source. By contrast, females are not attracted to rowan branches without green berries, and they are not attracted to apple, demonstrating that the chemical stimulus from rowan berries is required for attraction. Attraction to synthetic compounds identified from rowan, anethole and 2-phenyl ethanol confirms the role of plant volatiles in host finding. These two compounds, however, show a discrepant behavioural effect in wind tunnel and field tests. Field traps baited with 2-phenyl ethanol capture female moths but anethole does not produce significant captures. Wind tunnel tests produce the opposite results: moths fly upwind towards the anethole lure, whereas 2-phenyl ethanol is not attractive at all. Wind tunnel attraction to 2-phenyl ethanol is achieved by adding odour from a rowan branch without berries, which is not attractive on its own. This finding demonstrates that interaction with the background odour contributes to the behavioural effect of plant volatile stimuli in the field.     

Movement of Anastrepha fraterculus from native breeding sites into apple orchards in Southern Brazil

We report movements exhibited by adults of Anastrepha fraterculus (Wiedemann) (Diptera: Tephritidae) from patches of native forests into apple orchards in Southern Brazil. Two mark-release-recapture experiments were conducted using wild flies. Released flies behaved as wild unmarked flies, and periods of peak captures of marked adults coincided with those of unmarked ones. In the first experiment (December 94), out of 2154 released adults, 7.1% were recaptured from day 2 through day 20 after release. Captures peaked from day 7–9 after release. Most marked flies (94.7%) were trapped within 200 m of the release point but eight adults (seven females and one male) were captured in traps placed in an apple orchard, 400–800 m from the release point. The vegetation found between forest and orchard consisted of pastures and annual crops. In the second experiment (January 95), a total of 3284 flies was released in an area where native host plants were abundant and located at ca. 900 m from an apple orchard. In all, 37.1% of marked flies were captured, 99.0% of them at a distance of less than 200 m from the release point. Four adults were captured in an apple orchard, 7 to 24 days after release. They may have reached the orchard through a large and continuous area of native forest. Our results unequivocally demonstrate that A. fraterculus adults are able to disperse from native forests where they originate and invade apple orchards, probably foraging for food and oviposition sites.     

Visually mediated motor planning in the escape response of Drosophila

A key feature of reactive behaviors is the ability to spatially localize a salient stimulus and act accordingly. Such sensory-motor transformations must be particularly fast and well tuned in escape behaviors, in which both the speed and accuracy of the evasive response determine whether an animal successfully avoids predation [1]. We studied the escape behavior of the fruit fly, Drosophila, and found that flies can use visual information to plan a jump directly away from a looming threat. This is surprising, given the architecture of the pathway thought to mediate escape [2, 3]. Using high-speed videography, we found that approximately 200 ms before takeoff, flies begin a series of postural adjustments that determine the direction of their escape. These movements position their center of mass so that leg extension will push them away from the expanding visual stimulus. These preflight movements are not the result of a simple feed-forward motor program because their magnitude and direction depend on the flies' initial postural state. Furthermore, flies plan a takeoff direction even in instances when they choose not to jump. This sophisticated motor program is evidence for a form of rapid, visually mediated motor planning in a genetically accessible model organism.     

Functional diversity of avian communities increases with canopy height: From individual behavior to continental‐scale patterns

Vegetation complexity is an important predictor of animal species diversity. Specifically, taller vegetation should provide more potential ecological niches and thus harbor communities with higher species richness and functional diversity (FD). Resource use behavior is an especially important functional trait because it links species to their resource base with direct relevance to niche partitioning. However, it is unclear how exactly the diversity of resource use behavior changes with vegetation complexity. To address this question, we studied avian FD in relation to vegetation complexity along a continental‐scale vegetation gradient. We quantified foraging behavior of passerine birds in terms of foraging method and substrate use at 21 sites (63 transects) spanning 3,000 km of woodlands and forests in Australia. We also quantified vegetation structure on 630 sampling points at the same sites. Additionally, we measured morphological traits for all 111 observed species in museum collections. We calculated individual‐based, abundance‐weighted FD in morphology and foraging behavior and related it to species richness and vegetation complexity (indexed by canopy height) using structural equation modeling, rarefaction analyses, and distance‐based metrics. FD of morphology and foraging methods was best predicted by species richness. However, FD of substrate use was best predicted by canopy height (ranging 10–30 m), but only when substrates were categorized with fine resolution (17 categories), not when categorized coarsely (8 categories). These results suggest that, first, FD might increase with vegetation complexity independently of species richness, but whether it does so depends on the studied functional trait. Second, patterns found might be shaped by how finely we categorize functional traits. More complex vegetation provided larger "ecological space" with more resources, allowing the coexistence of more species with disproportionately more diverse foraging substrate use. We suggest that the latter pattern was driven by nonrandom accumulation of functionally distinct species with increasing canopy height.     

Prey protein influences growth and decoration building in the orb web spider Argiope keyserlingi

Abstract. 1. Protein is important for a foraging animal to consume, as it promotes growth and enhances survival, particularly in web‐building spiders, which need to invest considerable protein into web building and may trade‐off growth for web investment. 2. The influence of dietary protein uptake on growth and web investment was tested in the orb web spider Argiope keyserlingi, by feeding them flies reared on three different media: (1) high protein, (2) low protein, and (3) standard (control) media. There was a negative correlation between protein and energy content of the flies across treatments; flies reared on the high protein media had the highest protein, but lowest energy, while flies reared on the low protein media had the lowest protein but highest energy. 3. It was found that silk investment and web architecture in A. keyserlingi was not affected by diet. Growth and decoration building were both enhanced when spiders were fed a high protein diet. 4. It was concluded that protein intake, rather than energy, influenced both growth and decoration building because: (1) protein intake enhances growth in other animals, (2) protein is essential for silk synthesis, especially aciniform silk, and (3) protein is a limiting factor actively sought by foraging animals in natural environments.     

Effects of recent experience on foraging in tephritid fruit flies

In field-cage studies, we investigated how the foraging behavior of tephritid fruit flies is modified by experience immediately prior to release on host plants. We observed females of a relatively monophagous species,Rhagoletis mendax (blueberry maggot fly), an oligophagous species,Rhagoletis pomomella (apple maggot fly), and a polyphagous species,Ceratitis capitata (Mediterranean fruit fly). Just prior to release on a host plant, the following kinds of stimuli were supplied: (1) single oviposition in a host fruit, (2) contact with 20% sucrose, (3) contact with a mixture of protein food (bird feces and sucrose), (4) contact with water, and (5) a walk over a host-plant leaf. When flies foraged on host plants without resources, search was most intensive (as measured by number of leaves visited) following a single oviposition in fruit, but residence time generally was the same following exposure to sugar, protein, and fruit stimuli.Rhagoletis mendax andC. capitata females visited the fewest leaves following exposure to water or host leaves, whereasR. pomonella foraged equally intensively following exposure to food stimuli, water, or leaves. On host plants containing resources (fruit and protein food), a single oviposition dramatically increased the number of females of all three species that found fruit compared to females that received experience with food, water or foliar stimuli. We found no significant effect of recent brief experience with any of the stimuli on subsequent attraction to protein food. Overall,C. capitata exhibited a higher propensity to abandon host plants than eitherR. mendax orR. pomonella. We suggest that this may reflect adaptations to differences in distribution of host plants in nature, strategies of dispersal, and host range.     

On the scent of standing variation for speciation: behavioral evidence for native sympatric host races of rhagoletis pomonella (Diptera: tephritidae) in the southern United States

Standing variation can be critical for speciation. Here, we investigate the origins of fruit odor discrimination for Rhagoletis pomonella underlying the fly's sympatric shift in the northeastern United States from downy hawthorn (Crataegus mollis) to apple (Malus domestica). Because R. pomonella mate on host fruit, preferences for natal fruit volatiles generate prezygotic isolation. Apples emit volatiles that appear to be missing from gas chromatography/electroantennographic detection profiles for flies infesting downy hawthorns, raising the question of how R. pomonella evolved a preference for apple. In the southern United States, R. pomonella attacks several native hawthorns. Behaviorally active volatile blends for R. pomonella infesting southern hawthorns contain the missing apple volatiles, potentially explaining why downy hawthorn flies could have evolved to be sensitive to a blend of apple volatiles. Flight tunnel assays imply that southern hawthorn populations were not the antecedent of a preassembled apple race, as southern flies were not attracted to the apple volatile blend. Instead, behavioral evidence was found for southern host races on native hawthorns, complementing the story of the historical sympatric shift to introduced apple in the North and illustrating how R. pomonella may evolve novel combinations of agonist and antagonist responses to volatiles to use new fruit resources.     

Attraction of Mexican Fruit Flies (Diptera: Tephritidae) to Grapefruit: Enhancement by Mechanical Wounding of and Experience with Grapefruit

Wild strain, mated, female Mexican fruit flies, Anastrepha ludens (Loew), with no prior experience with fruit (naive), were not attracted to grapefruit, a preferred cultivated host, in wind tunnel experiments. Naive, mated laboratory strain females were attracted. Prior experience with grapefruit increased attraction of both laboratory and wild strains. More females were attracted to fruit with peel damage than to undamaged fruit, indicating that fruit odor mediated attraction. More naive than experienced females attempted to oviposit on the sides of the wind tunnel. Experienced laboratory males, but not wild males or naive males, were attracted to grapefruit. Attraction and oviposition behavior of laboratory flies was greater than that of wild flies.     

Motor planning: insects do it on the hop

Planning a motor action in advance of its possible execution doesn't require cortical complexity: a recent paper demonstrates that even fruit flies prepare for movement some time before they decide whether or not to take action.     

The genetic basis for fruit odor discrimination in Rhagoletis flies and its significance for sympatric host shifts

Rhagoletis pomonella (Diptera: Tephritidae) use volatile compounds emitted from the surface of ripening fruit as important chemosensory cues for recognizing and distinguishing among alternative host plants. Host choice is of evolutionary significance in Rhagoletis because these flies mate on or near the fruit of their respective host plants. Differences in host choice based on fruit odor discrimination therefore result in differential mate choice and prezygotic reproductive isolation, facilitating sympatric speciation in the absence of geographic isolation. We test for a genetic basis for host fruit odor discrimination through an analysis of F2 and backcross hybrids constructed between apple-, hawthorn-, and flowering dogwood-infesting Rhagoletis flies. We recovered a significant proportion (30-65%) of parental apple, hawthorn, and dogwood fly response phenotypes in F2 hybrids, despite the general failure of F1 hybrids to reach odor source spheres. Segregation patterns in F2 and backcross hybrids suggest that only a modest number of allelic differences at a few loci may underlie host fruit odor discrimination. In addition, a strong bias was observed for F2 and backcross flies to orient to the natal fruit blend of their maternal grandmother, implying the existence of cytonuclear gene interactions. We explore the implications of our findings for the evolutionary dynamics of sympatric host race formation and speciation.     

Behavioral evidence for host races in Rhagoletis pomonella flies

Summary One of the most controversial putative cases of host race formation in insects is that of the apple maggot fly, Rhagoletis pomonella (Diptera: Tephritidae). A principal cause of the controversy is lack of relevant data. In laboratory and field enclosure experiments, we compared the host acceptance behavior of sympatric populations of flies originating from naturally infested hawthorn (the native host) and apple (an introduced host) in Amherst, Massachusetts or East Lansing, Michigan. In general, hawthorn fruit were accepted for ovipositional attempts nearly equally by apple and hawthorn origin females, whereas apples were accepted much more often by apple than hawthorn origin females. Similarly, males of apple and hawthorn origin exhibited about equal duration of residence on hawthorn fruits as sites at which to acquire potential mates, while males of apple origin tended to reside substantially longer than males of hawthorn origin on apples. Irrespective of fly origin, both sexes always responded more positively to hawthorn fruit than to apples. Because all flies assayed were naive (ruling out effects of prior host experience of adults) and because tests revealed no influence of pre-imaginal fruit exposure on pattern of host fruit acceptance by females, the combined evidence suggests the phenotypic differences we observed in host response pattern between hawthorn and apple origin flies may have an underlying genetic basis. Further tests showed that while larval progeny of flies of each origin survived better in naturally growing hawthorn fruit than in naturally growing apples, there was no differential effect of fly origin on larval survival ability in either host. We discuss our findings in relation to restriction in gene flow between sympatric populations of R. pomonella and in relation to current models of host shifts in insects.     

Nutritional status and the foraging behaviour of Bactrocera tryoni with particular reference to protein bait spray

Poisoned protein baits comprise a recognized method for controlling tephritid fruit flies in the form of a ‘lure‐and‐kill’ technique. However, little is known about how a fly's internal protein and carbohydrate levels (i.e. nutritional status) might influence the efficacy of this control. In the present study, the relationships between the internal levels of protein (as measured by total body nitrogen) and carbohydrate (as measured by total body carbon) of the fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) are investigated, as well as its foraging behaviours in response to protein, fruit and cue‐lure (a male‐specific attractant) baits. Small cage behavioural experiments are conducted using flies from cultures of different nutritional status and wild flies sampled from the field during the fruiting cycle of a guava crop. For female flies, increasing total body nitrogen is correlated with decreased protein foraging and increased oviposition activity; increasing total body carbon levels generate the same behavioural changes except that the oviposition response is not significant. For males, there are no significant correlations between changes in total body nitrogen and total body carbon and protein or cue‐lure foraging. For wild flies from the guava orchard, almost all of them are sexually mature when entering the crop and, over the entire season, total body nitrogen and total body carbon levels are such that protein hunger is unlikely for most flies. The results infer strongly that the requirements of wild, sexually mature flies for protein are minimal and that flies can readily gain sufficient nutrients from wild sources for their physiological needs. The results offer a mechanistic explanation for the poor response of male and mature female fruit flies to protein bait spray.     

The Effect of Animal Movement on Line Transect Estimates of Abundance

Line transect sampling is a distance sampling method for estimating the abundance of wild animal populations. One key assumption of this method is that all animals are detected at their initial location. Animal movement independent of the transect and observer can thus cause substantial bias. We present an analytic expression for this bias when detection within the transect is certain (strip transect sampling) and use simulation to quantify bias when detection falls off with distance from the line (line transect sampling). We also explore the non-linear relationship between bias, detection, and animal movement by varying detectability and movement type. We consider animals that move in randomly orientated straight lines, which provides an upper bound on bias, and animals that are constrained to a home range of random radius. We find that bias is reduced when animal movement is constrained, and bias is considerably smaller in line transect sampling than strip transect sampling provided that mean animal speed is less than observer speed. By contrast, when mean animal speed exceeds observer speed the bias in line transect sampling becomes comparable with, and may exceed, that of strip transect sampling. Bias from independent animal movement is reduced by the observer searching further perpendicular to the transect, searching a shorter distance ahead and by ignoring animals that may overtake the observer from behind. However, when animals move in response to the observer, the standard practice of searching further ahead should continue as the bias from responsive movement is often greater than that from independent movement.     

Connectivity counts: disentangling effects of vegetation structure elements on the searching movement of a parasitoid

1. A heterogeneous habitat structure can have a profound impact on foraging carnivorous arthropods. In the present study, we examined which elements of complex vegetation structure influence the searching movement of a parasitoid model organism. 2. Previous field work showed that tall and dense vegetation reduces the parasitism success of the eulophid egg parasitoid Oomyzus galerucivorus while the probability of host egg deposition increased close to plant tips. 3. In laboratory bioassays, dried grass stems were arranged according to the natural situation in different setups. The wasps' walking time on stems increased with increasing stem height and density. High stem density decreased the walking time of the parasitoids on the ground and an increased stem height reduced the propensity to fly to the ground. Connectivity had a minor positive effect on the number of stem contacts, but considerably reduced the number of wasps reaching the upper part of grass stems by two‐thirds. 4. Thus, although enhanced vegetation complexity enhances walking activity of the parasitoids in the vegetation, laying eggs at the tip of long grass stems in dense vegetation can be an adaptive strategy for the host, as it maximises the number of connections between plant parts to cross by parasitoids before reaching the host. The connection points disorient the wasps, which lose time, reverse their direction or fly away.