Female Mediterranean Fruit Flies Research Articles

A mortality cost of virginity at older ages in female Mediterranean fruit flies

Mortality rates were measured over the lifetime of 65,000 female Mediterranean fruit flies, Ceratitis capitata, maintained in either all-female (virgin) cages or cages with equal initial numbers of males, to determine the effect of sexual activity and mating on the mortality trajectory of females at older ages. Although a greater fraction of females maintained in all-female (virgin) cages survived to older ages, the life expectancy of the surviving virgins was less than the life expectancy of surviving non-virgins at older ages. This was due to a mortality crossover where virgin flies experience lower mortality than mated flies from eclosion to Day 20 but higher mortality thereafter. These results suggest that there are two consequences of mating—a short-term mortality increase (cost) and a longer term mortality decrease (benefit).

Reproductive potential predicts longevity of female Mediterranean fruitflies.

Reproduction exacts a price in terms of decreased survival. Our analysis of the interplay between age patterns of fecundity and mortality for individual female medflies (Ceratitis capitata) revealed that individual mortality is associated with the time-dynamics of the egg-laying trajectory. In a sample of 531 medflies, we found that each individual has a characteristic rate of decline in egg laying with age. This defines an individual's rate of reproductive exhaustion. This rate was shown to predict subsequent mortality The larger the remaining reproductive potential, the lower the subsequent mortality An increased mortality risk was seen in flies for which egg production declined rapidly early on, irrespective of the level of egg production. Thus, reproductive potential and lifetime are coupled in such a way that those flies which are able to profit most from an extended life span in terms of increased egg output are indeed likely to live longer.

Local enhancement of arrivals of Ceratitis capitata females on fruit mimics

Mature female Mediterranean fruit flies, Ceratitis capitata (Wiedemann), isolated from conspecifics for 7 days prior to testing in laboratory cages, were attracted to yellow plastic fruit-mimicking hemispheres or spheres in significantly greater numbers when groups of conspecific females were present than absent on fruit mimics. Attraction of females to conspecifics occurred for females deprived of protein or continuously provided with protein since eclosion, for fruit mimics that were unbaited or baited with odor of food or fruit, and under single-choice as well as multiple-choice test conditions. Attraction proved just as great to fruit mimics having dead conspecifics as to mimics having live conspecifics, was evident also when fruit mimics were orange or white, and occurred also in response to presence of live Bactrocera dorsalis (Hendel) females on fruit mimics. We discuss our findings in relation to local enhancement, a form of social facilitation in insects and other animals.

Evaluation of synthetic food‐based attractants for female Mediterranean fruit flies (Dipt., Tephritidae) in McPhail type traps

During summer 1997 field experiments were conducted on the island of Chios, Greece, to compare captures of female Mediterranean fruit flies (medflies), Ceratitis capitata (Wiedemann), in traps baited with either synthetic female‐targeted lures or a standard protein bait (NuLure and borax). The synthetic lures contained ammonium acetate,1,4 diaminobutane (putrescine), and trimethylamine. Two trap types (International Pheromone’s McPhail Trap (IPMT) and the Tephri trap) were tested as either wet or dry. Wet IPMT traps baited with the synthetic attractants were the most attractive of all trap combinations tested and captured 2.1 times more female medflies and 1.8 times more total medflies than traps baited with NuLure and borax. Traps containing the synthetic attractant captured approximately 4.6 times fewer nontarget insects than NuLure baited traps. Vapona used in IPMT traps was repellent to medflies and dry traps with lower concentrations of Vapona were approximately 1.5 times less attractive to female medflies than traps containing water. Even with a decrease in attractiveness, the dry traps were significantly more effective for females and more practical for mass trapping and monitoring than the currently used traps baited with protein solutions.

Mating-induced inhibition of remating in female Mediterranean fruit flies Ceratitis capitata

Mechanisms producing inhibition of remating in mated female Mediterranean fruit flies Ceratitis capitata, were investigated by matings with surgically altered males. Comparison of remating by females mated with either intact control males or males with a shortened penis, showed that ejaculate or a physical stimulus of penis insertion caused remating inhibition for at least 10 days after first mating. Remating frequency at two days after mating was significantly higher in females mated to castrated (spermless) males than in females mated to sham-operated control males. This difference disappeared by day four after mating, indicating that sperm cause a shorter-term inhibition of remating than does a normal first mating. Other factors in addition to sperm must therefore play a role in inhibition of remating.

Behavioural switch of female Mediterranean fruit fly, Ceratitis capitata: mating and oviposition activity in outdoor field cages in Hawaii

Abstract1 Laboratory‐reared normal, and wild female Mediterranean fruit flies, Ceratitis capitata (Wiedemann), were assayed in outdoor field cages to assess the impact of a mating‐induced behavioural switch on mating and subsequent oviposition activity.2 Virgin females preferred interactions with males leading to mating over attraction to, and oviposition in, artificial yellow spheres containing guava odour or green apples hung in a guava tree. Laboratory‐reared females previously mated with either laboratory‐reared normal males or laboratory‐reared irradiated (sterile) males showed little interest in remating with males and instead, were much more likely to be found arrested on artificial and real fruit and ovipositing. Oviposition on artificial fruit was five times greater by females that had mated with either normal or irradiated males than by virgin females. Wild females showed similar qualitative changes in the mating‐induced behavioural switch; however, oviposition activity was significantly less than for laboratory‐reared females.3 These results confirm that mating has a profound effect on the behaviour of female Mediterranean fruit flies and that irradiated males are functionally equal with normal males (lab‐reared or wild) in their ability to alter female behaviour. These results are discussed in the context of the sterile insect technique for control of Mediterranean fruit flies in the field.

Dual modes of aging in Mediterranean fruit fly females.

The life history of medflies is characterized by two physiological modes with different demographic schedules of fertility and survival: a waiting mode in which both mortality and reproduction are low and a reproductive mode in which mortality is very low at the onset of egg laying but accelerates as eggs are laid. Medflies stay in waiting mode when they are fed only sugar. When fed protein, a scarce resource in the wild, medflies switch to reproductive mode. Medflies that switch from waiting to reproductive mode survive longer than medflies kept in either mode exclusively. An understanding of the physiological shift that occurs between the waiting and reproductive modes may yield information about the fundamental processes that determine longevity.

Relationship of Age Patterns of Fecundity to Mortality, Longevity, and Lifetime Reproduction in a Large Cohort of Mediterranean Fruit Fly Females

Daily reproduction was monitored throughout the lives of 1000 individual female Mediterranean fruit flies (Ceratitis capitata). Inasmuch as the average female medfly lived 35.6 days and laid 740 eggs in her lifetime, the overall data set consisted of information on around 740,000 eggs distributed over 35,600 fly-days. Results described include the frequency distributions of eggs/day at young (< or =30 days), middle (31-60 days), and older (61-90 days) ages, the relationship between individual life span and lifetime reproduction, the distribution of deaths for non-egg layers versus egg layers, and density plots for daily egg production relative to both lifetime reproduction and life span. One of the more surprising results was the lack of correlation of the total number of eggs laid by females at younger ages (all ages under 30) and subsequent reproduction and life span. Technical and conceptual implications for analyses of reproductive data on other species and groups are briefly discussed.

A simple graphical technique for displaying individual fertility data and cohort survival: case study of 1000 Mediterranean Fruit Fly females

1.A graphic technique is presented in which data on age‐specific reproduction of individuals are portrayed using: (i) a horizontal life line, the length of which is proportional to individual longevity; (ii) colour‐coded segments depicting the level of reproduction at each age; and (iii) a cohort survival schedule created by rank‐ordering individual life lines from shortest‐ to longest‐lived.2.The resulting graphic, referred to as an event history diagram, portrays data at the individual level and thus allows visual comparisons of detailed life‐history patterns such as age of first reproduction, longevity, ages of high, medium, low and zero reproduction, and post‐reproductive period.3.Example graphs are shown for reproductive and longevity data gathered on 1000 medfly females. The average female lived 35·6 days and laid 759·3 eggs and therefore the graphs display information for 35 600 fly days and the age‐distribution of laying for 759 300 eggs.4.Because the graphics provide a means for visualizing large amounts of data precisely and efficiently, they reveal details and nuances in the data that are not apparent from conventional graphic methods.5.The advantages of longitudinal data gathered on individuals and reasons why visualizing individual‐level data is important are discussed.

Socially facilitated egglaying behavior in Mediterranean fruit flies

We examined the behavior of individual mature female Mediterranean fruit flies (medflies), Ceratitis capitata (Wiedemann), transferred from a holding cage without fruit to a clean host kumquat fruit already occupied by another medfly female engaged in ovipositional behavior. A significantly greater proportion of transferred (=test) ovipositionally naive females initiated ovipositor boring into a fruit in the presence than in the absence of an occupying medfly. Moreover, test females commenced boring significantly sooner in the presence than in the absence of another medfly. Interestingly, similar results occurred when a test medfly was transferred to a kumquat occupied by an ovipositing female oriental fruit fly, Bactrocera dorsalis Hendel. In contrast, there was no enhancement of propensity to bore when a test medfly was transferred to a kumquat occupied by a female Biosteres arisanus (Sonan), a parasitoid attacking medfly eggs. The principal proximate stimulus giving rise to the higher tendency to oviposit of a test medfly in the presence of an occupying medfly or oriental fruit fly appeared to be wing-waving by the occupant during an encounter. We consider our findings to be good evidence of socially facilitated ovipositional behavior in ovipositionally naive medflies, and suggest that such females may benefit from acquisition of a cue demonstrating the acceptability of a host for oviposition.

Statistical tools for the analysis of nutrition effects on the survival of cohorts.

We discuss various methods which can be employed for the comparative analysis of samples of response curves. In the application discussed here, these curves are hazard functions, each generated by the survival data obtained for a cohort of experimental subjects which are fed a specific diet. It is demonstrated how comparisons of the effects of different diets on survival can be carried out by employing statistical techniques for inference on samples of curves. The methods are illustrated with data on the survival of large cohorts of male and female Mediterranean fruit flies under full diet and under protein deprivation. These statistical methods allow one to investigate differences between the samples of hazard functions generated by the four groups defined by combinations of sex and diet.

Asymmetries in Physiological State as a Possible Cause of Resident Advantage in Contests

Abstract As is common in defense of resources in many animals, contests on host fruit between female Mediterranean fruit flies (Ceratitis capitata) are generally resolved in favour of the resident individual. Here we offer an interpretation of resident advantage in this species which is derived from a dynamical state-variable perspective on behaviour. We first demonstrated the occurrence of residence advantage. In field-cage assays of freely-foraging and freely-interacting females within a tree bearing host coffee berries, the occurrence of two females on a berry almost always resulted in contests. Approximately half of the contests among females on berries resulted in clear winners; resident females won an overwhelming majority of such contests. Contests tended to occur while the resident fly was currently engaged in egg-laying, either boring into the berry with their ovipositor or marking the berry after laying eggs. Non-residents, by contrast, were uniformly engaged in searching behaviour. We next tested the hypothesis that degree of resident advantage is a function of the degree to which a resident is engaged in egg-laying behaviour just prior to the contest. In experimental manipulations of resident status, which female won depended strongly on what residents were doing at the time contests were initiated. If residents were resting and grooming, non-residents (who were uniformly searching) usually won. If residents were laying eggs or marking the fruit after laying eggs, residents usually won. Only when both residents and non-residents were engaged in searching behaviour did the outcome of a contest not depend on resident status. Finally, we tested the hypothesis that contest outcome is related to the dynamical state of the contestants in terms of their relative age. We staged contests between host-deprived females that differed in age by two weeks, manipulating age independently of resident status. Older females won virtually all contests with younger ones regardless of resident status. In a field-cage assay of freely-foraging flies, older females also engaged in significantly more egg-laying activity. Taken together, these results indicate that older females value a fruit more highly than do younger ones, invest more in defense of that resource and therefore win more contests.

Mating-Induced Changes in Olfactory-Mediated Behavior of Laboratory-Reared Normal, Sterile, and Wild Female Mediterranean Fruit Flies (Diptera: Tephritidae) Mated to Conspecific Males

Laboratory-reared normal, sterile, and wild female Mediterranean fruit flies, Ceratitis capitata (Wiedemann), were mated with laboratory-reared normal, sterile, and wild male flies to assess the ability of males to alter olfactory-mediated behavioral responses of females to male-produced pheromone or host fruit odor. Virgin females of all 3 types showed a preferential attraction and arrestment on yellow spheres emitting male-produced pheromone in a laboratory flight tunnel. Laboratory-reared normal and wild females mated to laboratory reared normal, sterile, or wild males switched their behavior showing strong preferential attraction to, arrestment on, and egg-laying in (for laboratory-reared females) yellow spheres emitting host fruit odor (guava) over male-produced pheromone. Sterile females did not show a significant switch in behavior except when mated to sterile males. The olfactory-mediated behavioral switch was most evident in the laboratory-reared normal female × laboratory-reared normal male mating. These findings suggest that irradiation of males inducing gamete sterility does not affect the factor(s) from the male accessory gland associated with altering female olfactory behavior. The ability of sterile males to alter adequately olfactory-mediated behavior of wild females is discussed in the context of the sterile insect technique for control of Mediterranean fruit flies in the field.

Attraction of Mature Ceratitis capitata Females to 2-Heptanone, A Component of Coffee Fruit Odor

In indoor laboratory-cage and outdoor field-cage assays, we evaluated the attraction of released, protein-fed, mature Mediterranean fruit fly females to six volatile compounds emitted by attractive crushed ripe coffee fruit: 3-methyl-1-butanal, decanal, 3-methyl-1-butanol, 2-(Z)-pentenol, 2-(E)-hexenol, and 2-heptanone. Previous tests in a wind tunnel indicated that each of these six compounds was more attractive than clean air to females. In laboratory cage assays, none of the compounds elicited a response significantly greater than that to water. In field-cage assays, 2 or 4 μl of 2-heptanone in 5 ml of water (but none of the other compounds at 2 or 4 μl in 5 ml of water) consistently attracted protein-fed medflies at significant levels that averaged about five times greater than attraction to water alone, although about 40% less than attraction to odor of coffee fruit extract. All types of mature protein-fed females tested (laboratory-cultured virgin, laboratory-cultured mated, wild mated) in field-cage assays responded similarly to 2-heptanone, whereas same-age (9- to 11-day-old) protein-deprived females did not respond significantly to 2-heptanone. Response of protein-fed females to 2-heptanone increased progressively with increasing dose (1, 2, 4, or 8 μl in 5 ml of water). Addition of 2 μl of 2-heptanone or 2 μl of any of the other compounds tested to 5 ml of water extract of coffee fruit did not enhance attractiveness of the extract. Relative to response to water, protein-fed females consistently exhibited a significant positive response to odor of coffee fruit extract but no significant response to odor of Nulure (a proteinaceous food attractant). Together, our findings suggest that mature protein-fed females were responding to 2-heptanone as though it were an oviposition-site stimulus rather than a feeding-site stimulus.

Volatile, Potential Attractants from Ripe Coffee Fruit for Female Mediterranean Fruit Fly

Twenty-eight volatile compounds from freshly crushed, ripe, dark red coffee fruit, Coffea arabica, were identified by dynamic headspace analysis techniques. Identifications were made on the basis of a comparison of Kovats indices and GC-MS spectra for unknowns and authentic samples. Of the compounds identified, 10 were alcohols, nine were aldehydes, five were ketones, and four were monoterpenes. The five most abundant volatiles in decreasing order were hexanal (21%), 2-(E)-hexenal (11%), 3-methyl-1-butanol (9.0%), 3-methyl-1-butanal (8.5%), and 1-hexanol (8.4%). The five least abundant volatiles of the 28 identified, in increasing order, were decanal (0.19%), methyl hexanoate (0.33%), pulegone (0.44%), α-isomenthone (0.45%), and 2-nonanone (0.55%). In preliminary tests, many of the identified volatiles attracted more female Mediterranean fruit flies than the control.

Circadian Patterns of Feeding and Reproductive Activities of Mediterranean Fruit Flies (Diptera: Tephritidae) on Various Hosts in Israel

We determined how male and female Mediterranean fruit flies, ceratitis capitata (Wiedemann), allocate time between feeding and reproductive activities in 2 agricultural habitats in coastal Israel. We determined diurnal temporal distribution patterns between and within various hosts, established when and where feeding and reproductive activities take place, and identified the primary sources of nutrition in the field. The synchronized behavior of the population indicates a daily periodic movement between copulatory, oviposition, feeding, and resting sites. Male activities were regimented and discrete with a clear separation between feeding and reproductive activities, whereas females engaged in different behaviors throughout the day. Males congregated in leks on pitanga trees, Eugenia uniflora, from midmorning to early afternoon, and rarely engaged in other activities during this period. Fruit guarding, an alternative tactic, occurred mainly in the late afternoon. Feeding was observed primarily in the evening on ripe and rotten fruit, leaf surfaces, and fresh bird feces. We postulate that although food itself is not a limited resource, time to consume it without the threat of predation limits and regulates feeding behavior of these flies.

Potential for host range expansion in Ceratitis capitata flies: impact of proximity of adult food to egg‐laying sites

Abstract. In field cage and field tests, female Mediterranean fruit flies, Ceratitis capitata (Wiedemann), in trees alighted in significantly greater numbers upon sticky‐coated (non‐odour‐emitting) kumquats, Fortunella japonica, that were in the vicinity of odorous natural proteinaceous food (bird faeces) or synthetic food odour than on similar kumquats distant from bird faeces or synthetic food odour. In field cage tests, oviposition in non‐sticky kumquats nearby bird faeces was significantly greater than in non‐sticky kumquats distant from bird faeces. In field tests, medflies laid significantly more eggs in host kumquat and non‐host hawthorn, Crataegus mollis, fruit adjacent to bird faeces and synthetic food odour than in fruit of these types distant from food‐type stimuli. These findings suggest that odour of natural food of medflies could lure flies to plants whose fruit emit little or no attractive odour and are not permanent hosts but which are nonetheless susceptible to egg‐laying and larval development, resulting in temporary expansion of host range.

Functional shifts in the use of parasitized hosts by a tephritid fly: the role of host quality

Superparasitism, a phenomenon in which parasitic insects lay eggs in already-exploited hosts, provides a useful context in which to examine the dynamics of parental investment. This study explored conditions under which female Mediterranean fruit flies (Ceratitis capitata) shift from avoiding superparasitism of host fruit to preferring it, even placing eggs direcdy into existing egglaying cavities. An a priori hypothesis of costs and benefits was used to predict how use and avoidance of parasitized fruit would change in -response to changes in fruit size and ripeness. We predicted that avoidance would decrease with increasing fruit size, while use would increase with decreasing ripeness. Using a field-cage assay, ripeness was held constant and the size of host coffee berries manipulated. Avoidance of parasitized berries was significandy less pronounced on large berries than on small ones. In a second experiment, size was held constant and ripeness manipulated. On unripe berries, females deposited the majority of clutches direcdy into existing egg-laying cavities. On ripe berries, by contrast, die same females deposited most clutches in previously unparasitized fruit. Parallel patterns in the frequency of female-female contests were observed, supporting die nodon diat a fruit's value is determined by an interaction between fruit size or ripeness, on one hand, and die prior occurrence of eggs, on die odier. Laboratory assays suggested that use of existing sites had advantages in terms of time savings; female behavior thus constitutes a relatively uncommon example of adaptive superparasitism in which parasitized hosts are actually preferred over unparasitized ones.

Development of a Dry Plastic Insect Trap with Food-Based Synthetic Attractant for the Mediterranean and Mexican Fruit Flies (Diptera: Tephritidae)

A dry plastic insect trap for monitoring populations of tephritid fruit flies is described. The plastic trap is constructed of acetate film that is painted to provide a visual cue and contains a toxic ant panel that provides a visual cue and a feeding stimulant to flies that have entered the trap. The trap baited with a 2-component blend of ammonium acetate and putrescine was tested against feral populations of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), and the Mexican fruit fly, Anastrepha ludens (Loew), in field trials conducted in Guatemala. The combination of ammonium acetate and putrescine was better than either ammonium acetate-only, putrescine-only, or unbaited traps. More female Mediternmean fruit flies were trapped in green traps than in colorless traps, and capture of male Mediternmean fruit flies was greater in yellow traps than in orange traps. Neither female nor male Mexican fruit flies differentiated among orange, green, and yellow traps, but the percentage trapped in any colored trap was higher than in colorless traps. McPhail traps with standard protein bait caught more Mexican fruit flies than either of the plastic traps at any of the doses of synthetic baits tested. However, plastic traps baited with either the medium or high dose of synthetic blend caught equal numbers of Mediterranean fruit flies as McPhail traps. Although McPhail traps caught more female Mediterranean fruit flies than plastic traps baited with the low dose of synthetic blend, a greater percentage of females captured in plastic traps were unmated (55-65% versus 22% in McPhail traps). Increase in dose of the synthetic lure increased the percentage of mated females captured in the plastic traps. Unlike McPhail traps, which catch large numbers of miscellaneous Diptera, the plastic traps were highly specific and caught few nontarget flies.

Effects of mating and accessory gland injections on olfactory-mediated behavior in the female mediterranean fruit fly, Ceratitis capitata

The female Mediterranean fruit fly, Ceratitis capitata, exhibits a preferential switch in certain olfactory-mediated behaviors as a result of mating. Unmated, laboratory-reared, virgin females chose the odor of male-produced pheromone over host fruit odor (guava) in a dual-choice flight tunnel bioassay. Females continued to preferentially respond to the male pheromone for several weeks if not allowed to mate. Mated females chose the host fruit odor over the male-produced pheromone and deposited significantly greater amounts of fertile eggs if given the opportunity. Virgin females injected with accessory gland fluid (AGF) from sexually mature males will “switch” their response from choosing the pheromone odor to choosing host fruit odor in the flight tunnel bioassay and exhibit egg-laying behavior typical of mated females. Significant differences in the number of female landings, time on the source (sphere) and number of eggs laid occurred when females were injected with AGF levels of 0.2 male equivalents or greater. Thus AGFs associated with sexually mature males contain factors that appear to influence olfactory-mediated flight behavior.