Byron I. Katsoyannos

Sex differences in movement between natural feeding and mating sites and tradeoffs between food consumption, mating success and predator evasion in Mediterranean fruit flies (diptera : tephritidae)

SummarySystematic quantitative observations of the location and diel pattern of adult Mediterranean fruit fly, Ceratitis capitata (Wiedemann), activities were carried out in an orange grove and surroundings on the island of Chios in Greece. Natural fly foods were assessed for their contribution to fly longevity, fecundity and fertility. There were diel shifts in male and female location. Females required a substantial and varied diet to realize peak fecundity. This diet was acquired away from the primary host, orange. Foraging for food throughout most of the day on fig and non-host foliage (including feeding on bird droppings) as well as on fig fruit and grapes, females dispersed and fed more than males. A diet of grapes alone did not support any fecundity, contributing only to longevity. A diet of figs alone, on the other hand, sustained both longevity and egg production. Bird feces alone supported neither egg production nor longevity. However, when added to a diet of figs, bird feces significantly increased fly fecundity. Throughout most of the day, males aggregated in leks within the inner canopy of the primary host, orange. The arrival here during the warmest hours of the day of receptive females, followed by pair formation, reinforced the lek mating system on host foliage. In the afternoon, females shifted to orange fruit where they suffered from high predation mortality while ovipositing. Soon after, males also shifted to orange fruit, where they attempted matings with non-receptive ovipositing females. Male feeding on fig fruit occurred late in the day, a time when they were least likely to find a mate. Male survival did not differ between the natural diets. Tradeoffs between food consumption, mating success and predator evasion are discussed for each sex and related to fruit fly mating systems.

Effect of adult age, food, and time of day on sexual calling incidence of wild and mass-reared Ceratitis capitata males

The sexual calling incidence of wild and mass‐reared Mediterranean fruit fly males, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), was studied at 25 °C and a photophase of 14 h starting at 0600 h. Wild males fed on yeast hydrolysate and sugar attained sexual maturity earlier and exhibited higher calling activity than males fed on sugar alone. In both sugar and yeast hydrolysate‐fed wild males, calling levels were high during the first hours of the photophase, declined at 0900–1000 h, then increased again reaching high levels between 1200 and 1500 h, and finally declined and ceased after 1600 h. Food deprivation for 8 h or more caused a significantly lower frequency of calling. Irradiated (sterile) and unirradiated mass‐reared males fed on either sugar and yeast or sugar alone did not differ in the age of attaining sexual maturity (maximum levels of calling occurred about 8 days earlier than in the wild males). However, irradiated males fed on sugar called less frequently than males in the other treatments of mass‐reared males. The daily rhythm of calling in protein and sugar‐fed irradiated males differed somewhat from that of wild males. Calling was recorded at high levels from the beginning of the photophase until 1300 h without any decrease at 0900–1000 h. It then decreased to very low levels from 1500–1800 h and increased slightly at 1900 h. These findings are discussed in relation to the mating behavior of the fly and to the effectiveness of released sterile males in Sterile Insect Technique programs.

Odour-mediated foraging by yellowjacket wasps (Hymenoptera: Vespidae): predation on leks of pheromone-calling Mediterranean fruit fly males (Diptera: Tephritidae)

Predation is probably the most important male mortality factor in insect species with courtship displays that render males performing them conspicuous targets of predators. Sexually active Mediterranean fruit fly males, Ceratitis capitata (Wied.), aggregate in leks, where they participate in agonistic encounters and engage in visual, acoustic and pheromone-calling displays to attract receptive females. The objective of this study was to assess: a) whether sexually displaying C. capitata males in leks inside host and non-host foliage are subject to predation by the most prominent predators yellow-jacket wasps, Vespula germanica (F.), and if so, b) whether olfactory, visual or auditive stimuli are used by foraging wasps in locating male C. capitata prey. Studies were carried out in a citrus orchard and surroundings on the island of Chios, Greece. Observations were conducted using perforated containers hung within mulberry, fig or citrus foliage. Living C. capitata flies of different sex and either mature or immature were placed inside. Our results show that the yellowjacket wasps have learned to associate the presence of sexually active medfly males aggregated in leks with their preys pheromone (kairomone). Foraging wasps, flying through the crowns of host trees, responded to the odour source of C. capitata male pheromone by approaching from downwind. Even inside dense citrus tree foliage, wasps keyed in on aggregations of pheromone-calling males using olfactory stimuli. Stimuli of visual and acoustic male signalling were only used at close range, after having followed the pheromone plume close to its source. Visual cues played a greater role in directing wasp foraging under more open and exposed host foliage conditions. Odour-based foraging of wasps inside host foliage in the mid-morning hours, when medfly male lekking activities peak, shifted gradually to a more visual-based host fruit patrolling in the afternoons to capture ovipositing and feeding medfly females. On ripe fruit, particularly fig, V. germanica visual prey hunting also included the capture of feeding medfly males, other feeding Diptera, as well as medfly larvae extracted from wasp-made perforations in the fruit.

Microsatellite analysis reveals remating by wild Mediterranean fruit fly females, Ceratitis capitata

Accurate estimates of remating in wild female insects are required for an understanding of the causes of variation in remating between individuals, populations and species. Such estimates are also of profound importance for major economic fruit pests such as the Mediterranean fruit fly (Ceratitis capitata). A major method for the suppression of this pest is the sterile insect technique (SIT), which relies on matings between mass‐reared, sterilized males and wild females. Remating by wild females will thus impact negatively on the success of SIT. We used microsatellite markers to determine the level of remating in wild (field‐collected) Mediterranean fruit fly females from the Greek Island of Chios. We compared the four locus microsatellite genotypes of these females and their offspring. Our data showed 7.1% of wild females remated. Skewed paternity among progeny arrays provided further evidence for double matings. Our lowest estimate of remating was 3.8% and the highest was 21%.

Seasonal and Annual Occurrence of the Mediterranean Fruit Fly (Diptera: Tephritidae) in Northern Greece

Abstract The phenology and population dynamics of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), were studied from 1991 to 1995 using Jackson traps baited with trimedlure and periodic fruit sampling in two orchards in Thessaloniki northern Greece (40.3° north latitude, 22.5° longitude). This area is located within the northernmost zone of establishment of the fly in Europe. No adults were captured from December to the end of June. The first captures were recorded from the end of June to August, depending on the year and orchard, and captures rates peaked in the autumn of each year. Significant differences were observed in adult population density and in the initiation of fly activity between two neighboring orchards (≈500 m apart) that differed in host fruit abundance and availability. The results of fruit sampling showed that apricots were the first fruits infested every year in the area of Thessaloniki. Though infested at low rates, they were very important for breeding the first summer generation, and also for the increase in C. capitata population later in the summer. Peaches and figs were important hosts for breeding the late summer and early autumn generations. Apples and other pome fruits were important hosts later in autumn (October–November), and also served as overwintering refuges for the larvae. Among 17 fruit species collected in the area 11 were found infested. Pecan [ Carya illinoensis (Wang) k. Koch] and Malus floribunda Sieb. (an ornamental tree) are reported here for the first time as hosts of C. capitata. Our findings suggest that C. capitata completes four to five generations per year in the area of Thessaloniki. Practical and theoretical implications concerning the population dynamics and the control of this fly are discussed.

Effect of orange peel substances on mating competitiveness of male Ceratitis capitata

The response of wild Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) males to orange peel chemicals and their effect in mating competitiveness of males exposed to these chemicals was studied in the laboratory (25±2 °C, 65±5%, r.h.). Males were attracted, landed, and arrested on ripe oranges that were superficially wounded in the flavedo region of the peel, and fed on the wounds. Exposure to wounded oranges conferred to males a mating advantage over unexposed males. In flies of 1 to 10 days of age, this advantage was independent of the age of the flies during exposure and lasted at least 10 days following exposure. Twenty‐four hours of exposure ensured this effect. Exposure to intact oranges, or to wounded oranges covered with a wire‐screen, which allowed olfactory response and landing on the screen but not direct contact with the fruit, did not confer any mating advantage. Apparently, males required direct contact with wounded oranges in order to increase their mating competitiveness. It is suggested that the acquisition of certain substances of the flavedo, most probably through their ingestion, is responsible for the observed phenomenon. Our findings are discussed in relation to the sexual behaviour of this fly. Implications of these findings for the enhancement of the mating competitiveness of released sterile males and of the effectiveness of the Sterile Insect Technique programs are discussed as well.

Use of fruit wounds in oviposition by Mediterranean fruit flies

Casual observations suggested that female Mediterranean fruit flies (Ceratitis capitata Wiedemann) exploit fruit wounds (including pre‐existing oviposition punctures) as oviposition sites. This behaviour was quantified under field conditions in a citrus grove on the Greek island of Chios. Fruit wounds influenced oviposition behaviour in three ways. First, females were more likely to land on oranges (Citrus sinensis) that were artificially wounded than into unwounded control oranges. Second, having landed, females were more likely to attempt oviposition into a wounded orange than into control oranges. Third, females that attempted oviposition into wounded oranges usually did so directly into or very near the wound. The diameter and depth of the wound significantly influenced the tendency for female flies to land on a fruit but not their propensity, having landed, to attempt oviposition in or near the wound. The significance of this behavior in nature and implications for management of the Mediterranean fruit fly are discussed.

Spatial Autocorrelation Analysis of a Ceratitis capitata (Diptera: Tephritidae) Adult Population in a Mixed Deciduous Fruit Orchard in Northern Greece

Abstract We studied the spatio-temporal dispersion patterns of Mediterranean fruit fly, Ceratitis capitata (Wiedemann), in a mixed, deciduous, fruit orchard in Thessaloniki (northern Greece), using spatial autocorrelation methods to analyze adult trapping data. Each trapping station consisted of a Jackson trap (baited with trimedlure) and a McPhail trap (baited with ammonium acetate, putrescine, and trimethylamine). More males than females were captured throughout the season. Males and females exhibited different spatial dispersion patterns. Females were first detected during the summer (June–July) in apricot and peach trees bearing ripe fruits and significantly aggregated there toward the end of July. In the autumn, females significantly aggregated in apple orchards bearing mature fruits. Early aggregations of males were first detected in August in cherries and plums. In September, males significantly clustered in pears at the edges of the orchard, and by October, after an increase in population density, their spatial dispersion pattern became random (no significant spatial autocorrelation). At the end of the season (November), the dispersion of both sexes became random. Our results show that spatial autocorrelation statistics can provide an important tool in studying the spatial dynamics of this fly even in small orchards. Results also suggest that the incorporation of knowledge on spatial patterns into area-wide control projects may improve monitoring efforts and reduce program costs.

Age-specific and lifetime behavior patterns in Drosophila melanogaster and the Mediterranean fruit fly, Ceratitis capitata.

Patterns of behavior were recorded every 10 min during a 2-h period each day from eclosion to death for individual Drosophila melanogaster (both sexes) and Ceratitis capitata (males-only) including walking, preening, feeding, flying, and resting for the former species, and walking, calling (signaling), supine (upside-down), and resting in the latter. Results reveal that, with the exception of preening in D. melanogaster, behavioral patterns are age-specific and the frequency of several behaviors (e.g. supine in medfly; walking and resting in D. melanogaster) are correlated with time-to-death. This is the first set of studies to report the age patterns over a range of behavioral categories throughout the lives of individuals and thus the first that systematically documents the behavior of individuals at advanced ages. We suggest that the new and unique behaviors (e.g. supine) that emerge from the aging process be referred to as degenerative behaviors, not only to distinguish them from the conventional behavioral classifications (innate, learned), but also to reflect their emergent nature.

Remating in wild females of the Mediterranean fruit fly, Ceratitis capitata

Female remating is widespread among animal taxa, and shows high interspecific diversity in frequency. While there is no consensus on general explanations for why females mate multiply, it is clear that remating rate has important implications for many evolutionary processes such as sperm competition, cryptic female choice and sexual conflict. We investigated the refractory period and the effect of sex ratio on remating in wild-derived individuals of the Mediterranean fruit fly (medfly) Ceratitis capitata (Wiedemann) (Diptera, Tephritidae), an insect pest species of major worldwide economic importance. In addition, we determined the remating rates of wild females throughout the flying season. Experiments with medflies that were the offspring of wild flies showed that remating was frequent and was observed in 3.3–13.3% of females on each of the 4 days after the first mating. Many matings thus induce only a short refractory period. Again using the offspring of wild flies, we found that female remating increased significantly under a highly male-biased sex ratio. Microsatellite analysis of offspring from wild-collected females showed that remating is common (4–28% of offspring arrays showed multiple paternity) and occurred throughout the flying season of these insects. These results have important implications for insect pest management using the sterile insect technique.