Thierry Brévault

Relationships between temperature, development and survival of different life stages of the tomato fruit fly, Neoceratitis cyanescens

The development and survival of female Neoceratitis cyanescens (Bezzi) (Diptera: Tephritidae) from egg to complete ovarian maturation were studied in the laboratory at five different constant temperatures: 15, 20, 25, 30, and 35 °C. The aim of this study was to get information on the influence of temperature on pre‐mature stages, as a prerequisite to optimise rearing procedures and to understand temporal and geographical patterns of fruit fly occurrence. The developmental rate of the different life stages increased linearly with increasing temperatures up to 30 °C. The fastest development of pre‐mature stages was recorded at 30 °C (22±1 days) and the slowest at 15 °C (98±3 days). The day‐degrees requirements (K) to complete total development were 432.6 day‐degrees. Lower temperature thresholds were 11.4, 11.9, 10.0, and 11.1 °C for egg, larval, pupal stages and ovarian maturation, respectively. The number of adults obtained from an initial batch of 100 eggs reached a maximum (64) at 25 °C. At 35 °C, no adults emerged. Larval developmental time was significantly shorter in green tomato fruits than in potato tubers at 15, 20, and 25 °C. Mortality rate of larvae was higher in green tomato fruits than in potato tubers at 25 and 30 °C.

Factors affecting behavioural responses to visual stimuli in the tomato fruit fly, #Neoceratitis cyanescens#

Responses of Neoceratitis cyanescens (Bezzi) (Diptera: Tephritidae) females to visual stimuli were studied in a laboratory flight chamber. A bright orange sphere was used to investigate the effects of age, mating status and time of day on their responses. In no‐choice assays, four parameters were considered: mean time before leaving the release vial, percentage of flies that visited the sphere, mean number of flights and mean time before landing on the sphere. Naive mated females first became strongly responsive to the orange sphere 6u2003days post‐adult emergence (>u200340%). The percentage of females that visited the sphere increased significantly with egg load. There were no significant differences in behavioural responses between virgin and mated mature females. In a choice situation between a yellow and an orange sphere, starved females displayed a greater propensity than well‐fed females to land on the yellow sphere. Mature females were more responsive to the orange sphere when tested in the afternoon than earlier in the day. In a no‐choice situation, females visited the yellow sphere as often as the orange sphere. However, the mean delay before landing was significantly greater for the yellow sphere. The results emphasize the importance of physiological condition on responses of N. cyanescens females to host‐simulating visual stimuli.

Influence of habitat pattern on orientation during host fruit location in the tomato fruit fly, Neoceratitis cyanescens

Fruit flies have evolved mechanisms using olfactory and visual signals to find and recognize suitable host plants. The objective of the present study was to determine how habitat patterns may assist fruit flies in locating host plants and fruit. The tomato fruit fly, Neoceratitis cyanescens (Bezzi), was chosen as an example of a specialized fruit fly, attacking plants of the Solanaceae family. A series of experiments was conducted in an outdoor field cage wherein flies were released and captured on sticky orange and yellow spheres displayed in pairs within or above potted host or non-host plants. Bright orange spheres mimicking host fruit were significantly more attractive than yellow spheres only when placed within the canopy of host plants and not when either within non-host plants or above both types of plants. Additional experiments combining sets of host and non-host plants in the same cage, or spraying leaf extract of host plant (bug weed) on non-host plants showed that volatile cues emitted by the foliage of host plants may influence the visual response of flies in attracting mature females engaged in a searching behaviour for a laying site and in assisting them to find the host fruit. Moreover, the response was specific to mature females with a high oviposition drive because starved mature females, immature females and males showed no significant preference for orange spheres. Olfactory signals emitted by the host foliage could be an indicator of an appropriate habitat, leading flies to engage in searching for a visual image.

Interaction Between Visual and Olfactory Cues During Host Finding in the Tomato Fruit Fly Neoceratitis cyanescens

Herbivorous insects searching for a host plant need to integrate a sequence of multimodal sensory inputs. We conducted a series of no-choice experiments in a laboratory wind tunnel to examine the behavioral response of the specialist fruit fly, Neoceratitis cyanescens (Diptera: Tephritidae), to host visual and olfactory stimuli presented singly or in combination (e.g., colored fruit model with or without host fruit odor). We also studied the influence of wind flow, age, and sex on the response of flies. In two-choice experiments, we evaluated the ability of mature females to discriminate between two fruit models emitting host vs. non-host fruit odor or clean air. Neoceratitis cyanescens mature females can use independently or interactively olfactory and visual stimuli to locate their host, whereas immature females and males respond primarily to host fruit odor. In the absence of wind, mature females mainly use visual information to locate the host fruit. In wind, host fruit odor significantly increases the probability and speed of locating the host fruit. In a two-choice situation between two bright orange spheres, flies accurately detected the sphere emitting host fruit odor vs. non-host fruit odor or odorless air. Nevertheless, they preferred to land on the bright orange sphere when the sphere emitting host fruit odor was blue. Furthermore, when odor source and fruit model were spatially decoupled (90 or 180°), >50% flies that landed on the fruit model initially performed an oriented flight toward the odor source, then turned back to the fruit model while in flight or after one landing, thus suggesting visual information to be the ultimate indicator of host fruit.

Visual response of the tomato fruit fly, Neoceratitis cyanescens, to colored fruit models

To determine how mature females of the tomato fruit fly, Neoceratitis cyanescens (Bezzi) (Diptera: Tephritidae), detect host fruit after arriving in their host plant habitat, behavioral responses to colored models were observed in a laboratory flight chamber. Host‐seeking females oriented themselves preferentially towards bright orange spheres (3.7 cm in diameter), irrespective of their natal host fruit: tomato, bug weed, or black nightshade. Females oriented themselves preferentially towards the orange sphere when placed against a fluorescent yellow background as opposed to a black background, but the distribution of responses to the set of colored spheres did not vary significantly with background color. In a choice situation between bright orange spheres of various sizes (1.9, 3.7, and 7.5 cm in diameter), females landed preferentially on the bigger sphere. However, they preferred a yellow color when the latter was associated with two‐dimensional models, probably mimicking leaves. The attractiveness of orange spheres depended more on the proportion of reflected light in the spectral region around 610 nm than brightness of color in itself. Low light intensity significantly influenced the activity of the flies but not their visual preference. The strong response of females to bright orange spheres confirmed the importance of visual characteristics in short‐range mechanisms of host‐plant location in specialist insects. Responses to fruit visual stimuli are discussed relative to other Tephritidae, host‐finding strategy, and pest management.

Diel patterns of reproductive activities in the tomato fruit fly, Neoceratitis cyanescens

We describe the diurnal temporal and spatial patterns of reproductive activities (mating and ovipositing) of adult tomato fruit flies, Neoceratitis cyanescens (Bezzi) (Diptera: Tephritidae), under laboratory, field‐cage and field conditions. The distribution pattern of flies in the different habitats (host and non‐host plants) showed temporal, physiological and sexual differences. Mature females were observed to frequent host plants preferentially, particularly in the late afternoon. By contrast, immature females preferred to rest on non‐host plants throughout the day. Males frequented mainly non‐host plants but some were observed on host fruits in the morning. Mating activity took place preferentially on non‐host plants, in the morning. In laboratory cages, females showed a strong daily propensity to engage in mating behaviour; the mean percentage of mating females was 88u2003±u20035%. Time allotted to this activity (4u2003h 52u2003minu2003±u20031u2003h 23u2003min in laboratory cages and at least 3u2003h for the mating pairs observed in the field) appeared considerable compared to the time required to satisfy feeding or oviposition activities. Except for a few ovipositing females observed in the morning, oviposition activities occurred mainly in the late afternoon.

Oviposition preference in the oligophagous tomato fruit fly, Neoceratitis cyanescens

We assessed the role of visual and olfactory cues on oviposition preference in the oligophagous tomato fruit fly, Neoceratitis cyanescens (Bezzi) (Diptera: Tephritidae). In a field survey, we evaluated the stage of susceptibility of field‐grown tomatoes by monitoring N. cyanescens infestations from fruit‐setting up to harvest, in relation to post‐flowering time, size, and visual properties of fruit. In two‐choice laboratory experiments, we tested the degree to which females use visual and olfactory cues to select their host plant for oviposition. In addition, we investigated the ability of flies to avoid fruit already infested by conspecific eggs or larvae, and the influence of natal host fruit on oviposition preference. Neoceratitis cyanescens females preferentially lay their eggs in small yellow‐green unripe fruit (2–3.5u2003cm diameter, 10–21u2003days post‐flowering). Damage to fruit was significantly affected by brightness and size properties. In laboratory experiments, females chose to lay their eggs in bright orange rather than yellow domes. On the sole basis of olfactory stimuli, females showed a significant preference for unripe vs. ripe host fruit, for unripe fruit vs. flowers or leaves, and for host vs. non‐host fruit (or control). However, colour interacted with odour as females dispatched their eggs equally between the yellow dome and the bright orange dome when unripe fruit of tomato was placed under the yellow dome vs. ripe fruit under the bright orange dome. When offered real ripe and unripe tomatoes, females preferred unripe tomatoes. Females significantly chose to lay eggs in non‐infested fruit when they were given the choice between these or fruit infested with larvae. In contrast, recent stings containing eggs did not deter females from laying eggs. Rather, they could have an attractive effect when deposited within <1u2003h. Regardless of their natal host plant, tomato or bugweed, N. cyanescens females laid significantly more eggs in a dome containing bugweed fruit. However, 15% of females originating from tomato laid eggs exclusively in the dome with tomato, against 3% of females originating from bugweed.

Flower and fruit volatiles assist host-plant location in the Tomato fruit fly Neoceratitis cyanescens

Mature females of the tomato fruit fly Neoceratitis cyanescens can detect host fruit at a short distance using only visual stimuli, but little is known about the role of airborne volatile cues in the host searching strategy. A series of experiments is conducted in a laboratory wind tunnel, in which the behavioural responses of individual flies to volatiles from Solanaceae host plants (including tomato Lycopersicum esculentum Mill., bug weed Solanum mauritianum Scop. and Turkey berry Solanum torvum Sw.) are observed, according to some environmental (air speed) and physiological (age and mating status of females, time of day) factors. Mature females respond primarily to specific olfactory cues from blends of flowers or host fruit, preferentially unripe fruit for bug weed, as opposed to ripe fruit for Turkey berry or tomato. Males are also highly attracted by the odour of unripe fruit of bug weed. Wind plays a key role, as shown by the proportion of flies that reach the upwind section of the tunnel in the presence of both fruit odour and air flow (66.7%) and in the absence of either fruit odour (13.3%) or wind (36.7%). In response to fruit volatiles carried by wind, flies embark in a ‘plume tracking’ or ‘aim and shoot flight, consistent with odour‐conditioned anemotaxis. Females respond to host fruit odour regardless of their age, egg load or mating status, and also more consistently in the afternoon, which is their preferential time of day for egg‐laying. Searching behaviour and response to host volatiles in N. cyanescens are discussed in the light of host‐finding and an adaptive strategy.

Sexual Attraction, Male Courtship and Female Remating in the Tomato Fruit Fly, Neoceratitis cyanescens

Sexual attraction in the tomato fruit fly, Neoceratitis cyanescens (Bezzi) (Diptera: Tephritidae) was tested in an olfactometer while major behavioral traits during courtship at a short range were described by video recording. In addition, 30 pairs of flies were monitored for mating activity in individual cages, during a 38-day study following adult emergence. Virgin females of N. cyanescens showed a significant attraction when males were placed in the upwind section of the olfactometer. Males adopted a typical calling behavior characterized by immobility, wings perpendicular to the body axis, swollen abdominal pleura and presence of a small transparent droplet at the tip of the abdomen. In addition, a specific odor was clearly perceptible by the observer. In individual cages, the first mating of N. cyanescens females took place on the second day after emergence. Females showed a high mating propensity, with 73u2009±u200918% females mated daily. Sexual conflicts due to mating system and applications to pest management strategies are discussed.