Effects of Physiological Status and Environmental Factors on the Lure Responses of Three Pest Fruit Fly Species (Diptera: Tephritidae).

Biotic and abiotic factors influence how insects respond to stimuli. This can make it challenging to interpret captures in traps used to monitor pest abundance in management programmes. To address this, the lure response of three pest fruit flies (Diptera: Tephritidae) was evaluated in a semi-field setting with respect to several physiological and environmental factors. Using standardised methods with known fly numbers in field cages, the response to Biolure (food-based lure) was evaluated for Ceratitis capitata, Ceratitis cosyra and Bactrocera dorsalis. Response to the male lures was tested: E.G.O PheroLure for C. capitata and C. cosyra, Trimedlure for C. capitata, and methyl eugenol for B. dorsalis. The physiological variables evaluated were fly age, sex, weight, and total body nutritional composition. The environmental effects of temperature, relative humidity and light intensity were also assessed. Protein-deprived adults responded more strongly to Biolure. The response to Biolure was not sex-specific. Fly age influenced the response of all species to all tested lures. However, this effect was species and lure specific. Temperature was the most influential environmental factor, with response generally increasing with temperature. Lower thresholds for lure response, despite the proximity of responsive flies, range from 12.21 to 22.95 °C depending on the species and lure tested. These results indicate that trapping systems and management activity thresholds must take physiological and environmental variation into account to increase their accuracy.

Tethered-flight performance of thermally-acclimated pest fruit flies (Diptera: Tephritidae) suggests that heat waves may promote the spread of Bactrocera species.

BACKGROUND: Thermal history may induce phenotypic plasticity in traits that affect performance and fitness. One type of plastic response triggered by thermal history is acclimation. Because flight is linked to movement in the landscape, trapping and detection rates, and underpins the success of pest management tactics, it is particularly important to understand how thermal history may affect pest insect flight performance. We investigated the tethered-flight performance of Ceratitis capitata, Bactrocera dorsalis and Bactrocera zonata (Diptera: Tephritidae), acclimated for 48 h at 20, 25 or 30 °C and tested at 25 °C. We recorded the total distance, average speed, number of flight events and time spent flying during 2-h tests. We also characterized morphometric traits (body mass, wing shape and wing loading) that can affect flight performance. RESULTS: The main factor affecting most flight traits was body mass. The heaviest species, B. dorsalis, flew further, was faster and stopped less often in comparison with the two other species. Bactrocera species exhibited faster and longer flight when compared with C. capitata, which may be associated with the shape of their wings. Moreover, thermal acclimation had sex- and species-specific effects on flight performance. Flies acclimated at 20 °C stopped more often, spent less time flying and, ultimately, covered shorter distances. CONCLUSION: Flight performance of B. dorsalis is greater than that of B. zonata and C. capitata. The effects of thermal acclimation are species-specific. Warmer acclimation temperatures may allow pest fruit flies to disperse further and faster. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Selection on female reproductive schedules in the marula fly, Ceratitis cosyra (Diptera: Tephritidae) affects dietary optima for female reproductive traits but not lifespan.

Introduction: A changing environment can select on life-history traits and trade-offs in a myriad of ways. For example, global warming may shift phenology and thus the availability of host-plants. This may alter selection on survival and fertility schedules in herbivorous insects. If selection on life-histories changes, this may in turn select for altered nutrient intake, because the blend of nutrients organisms consume helps determine the expression of life-history traits. However, we lack empirical work testing whether shifts in the timing of oviposition alter nutrient intake and life-history strategies. Methods: We tested in the marula fruit fly, Ceratitis cosyra, how upward-selection on the age of female oviposition, in comparison with laboratory adapted control flies, affects the sex-specific relationship between protein and carbohydrate intake and life-history traits including lifespan, female lifetime egg production and daily egg production. We then determined the macronutrient ratio consumed when flies from each selection line and sex were allowed to self-regulate their intake. Results: Lifespan, lifetime egg production and daily egg production were optimised at similar protein to carbohydrate (P:C) ratios in flies from both selection lines. Likewise, females and males of both lines actively defended similar nutrient intake ratios (control =1:3.6 P:C; upward-selected = 1:3.2 P:C). Discussion: Our results are comparable to those in non-selected C. cosyra, where the optima for each trait and the self-selected protein to carbohydrate ratio observed were nearly identical. The nutrient blend that needs to be ingested for optimal expression of a given trait appeared to be well conserved across laboratory adapted and experimentally selected populations. These results suggest that in C. cosyra, nutritional requirements do not respond to a temporal change in oviposition substrate availability.

Larval and adult diet affect phenotypic plasticity in thermal tolerance of the marula fly, Ceratitis cosyra (Walker) (Diptera: Tephritidae).

Introduction: Temperature fluctuations are important for the distribution and survival of insects. Rapid hardening, a type of phenotypic plasticity, is an adaptation that can help individuals better tolerate lethal temperatures because of earlier exposure to a sublethal but stressful temperature. Nutrition and sex are also known to influence a species ability to tolerate thermal stress. This study determined the effects of larval diet, adult diet, sex and hardening on the thermal tolerance of Ceratitis cosyra (Walker) (Diptera: Tephritidae) at lower and upper lethal temperatures. Methods: Larvae were raised on either an 8% torula yeast (high) or a 1% torula yeast (low) larval diet and then introduced to one of three dietary regimes as adults for thermal tolerance and hardening assays: no adult diet, sugar only, or sugar and hydrolysed yeast diet. Flies of known weight were then either heat- or cold-hardened for 2 hours before being exposed to a potentially lethal high or low temperature, respectively. Results: Both nutrition and hardening as well as their interaction affected C. cosyra tolerance of stressful temperatures. However, this interaction was dependent on the type of stress, with nutrient restriction and possible adult dietary compensation resulting in improved cold temperature resistance only. Discussion: The ability of the insect to both compensate for a low protein larval diet and undergo rapid cold hardening after a brief exposure to sublethal cold temperatures even when both the larva and the subsequent adult fed on low protein diets indicates that C. cosyra have a better chance of survival in environments with extreme temperature variability, particularly at low temperatures. However, there appears to be limitations to the ability of C. cosyra to cold harden and the species may be more at risk from long term chronic effects than from any exposure to acute thermal stress.

Male Mediterranean fruit flies prefer warmer temperatures that improve sexual performance.

Females and males have divergent strategies of energy investment, so the thermal preference of each sex in insects may differ because energetic conversion of metabolic reserves is dependent on temperature. We determined the thermal preference of virgin, sexually mature Mediterranean fruit flies, Ceratitis capitata, and found that males preferred a significantly higher temperature (23.8 ± 0.3 °C) than that of females (22.1 ± 0.3 °C). We then tested predictions for the difference in thermal preference related to the energetic demands of reproduction over a range of temperatures. The frequency and duration of calling bouts by male C. capitata were optimal at 26 °C. Mating propensity and latency, and copula duration, were optimal over the range of 22-28 °C. When mating occurred, temperature had little effect on the incidence of sperm storage by females, but there was a notable decline in the number stored at 28 °C. Female lifespan was highest at 18 °C, but lifetime egg production was optimal at 24 °C. These results illustrate temperature-related differences in the reproductive fitness of the sexes in C. capitata, although the optima for male traits align best with their thermal preference. They also support the theoretical prediction that insect thermal preference should be lower than the optimum for fitness.

Oxidative Damage Is Influenced by Diet But Unaffected by Selection for Early Age of Oviposition in the Marula Fly, Ceratitis cosyra (Diptera: Tephritidae).

The expression of life-history traits, such as lifespan or reproductive effort, is tightly correlated with the amount and blend of macronutrients that individuals consume. In a range of herbivorous insects, consuming high protein to carbohydrate ratios (P:C) decreases lifespan but increases female fecundity. In other words, females face a resource-based trade-off between lifespan and fecundity. Redox metabolism may help mediate this trade-off, if oxidative damage is elevated by reproductive investment and if this damage, in turn, reduces lifespan. Here, we test how diets varying in P:C ratio affect oxidative damage and antioxidant protection in female and male of the marula fly, Ceratitis cosyra (Diptera: Tephritidae). We use replicated lines that have been subjected to experimental evolution and differ in their lifespan and reproductive scheduling. We predicted that high fecundity would be associated with high oxidative damage and reduced antioxidant defences, while longer lived flies would show reduced damage and elevated antioxidant defences. However, higher levels of oxidative damage were observed in long-lived control lines than selection lines, but only when fed the diet promoting lifespan. Flies fed diets promoting female fecundity (1:4 and 1:2 P:C) suffered greater oxidative damage to lipids than flies fed the best diet (0:1 P:C) for lifespan. Total antioxidant capacity was not affected by the selection regime or nutrition. Our results reiterate the importance of nutrition in affecting life-history traits, but suggest that in C. cosyra, reactive oxygen species play a minimal role in mediating dietary trade-offs between lifespan and reproduction.

Patterns of Remating Behaviour in Ceratitis (Diptera: Tephritidae) Species of Varying Lifespan.

Trade-offs between life-history traits offset the energetic costs of maintaining fitness in complex environments. Ceratitis species have been recorded to have long lifespans, which may have evolved in response to seasonal resource fluctuation. It is thus likely that reproductive patterns have evolved concomitantly as part of the trade-off between lifespan and reproduction. In this study, we investigated how reproductive patterns differ between Ceratitis cosyra (Walker) and Ceratitis capitata (Wiedemann; Diptera: Tephritidae), two species with different average and maximum lifespans. Females of both species were mated and patterns of female survival, fecundity, remating and sperm storage were tested. Ceratitis cosyra had a higher rate of survival and a lower fecundity when compared with the shorter-lived C. capitata, suggesting that both species exhibit a trade-off between lifespan and reproduction. Both species showed a similar and consistent willingness to remate, despite declines in sperm storage, suggesting that sperm alone does not fully inhibit remating. As expected, C. cosyra transferred high numbers of sperm during the first mating. However, sperm stores declined unexpectedly by 14 days. This indicates that males might transfer large ejaculates as a nuptial gift, that females then later degrade as a source of nutrients. Large declines in sperm storage may also indicate that females discard excess sperm stores due to the toxicity involved with storing sperm. These results do not suggest that patterns of sperm storage and remating align with lifespan and resource seasonality in these species, but a wider range of species needs to be assessed to better understand variation in Ceratitis mating systems.

Selection on age of female reproduction in the marula fruit fly, Ceratitis cosyra (Walker) (Diptera: Tephritidae), decreases total antioxidant capacity and lipid peroxidation.

The oxidative damage caused to cells by Reactive Oxygen Species (ROS) is one of several factors implicated in causing ageing. Oxidative damage may also be a proximate cost of reproductive effort that mediates the trade-off often observed between reproduction and survival. However, how the balance between oxidative damage and antioxidant protection affects life-history strategies is not fully understood. To improve our understanding, we selected on female reproductive age in the marula fruit fly, Ceratitis cosyra, and quantified the impact of selection on female and male mortality risk, female fecundity, male sperm transfer, calling and mating. Against expectations, upward-selected lines lived shorter lives and experienced some reductions in reproductive performance. Selection affected oxidative damage to lipids and total antioxidant protection, but not in the direction predicted; longer lives were associated with elevated oxidative damage, arguing against the idea that accumulated oxidative damage reduces lifespan. Greater reproductive effort was also associated with elevated oxidative damage, suggesting that oxidative damage may be a cost of reproduction, although one that did not affect survival. Our results add to a body of data showing that the relationship between lifespan, reproduction and oxidative damage is more complex than predicted by existing theories.

Exploring the role of host specialisation and oxidative stress in interspecific lifespan variation in subtropical tephritid flies.

In herbivorous insects, the degree of host specialisation may be one ecological factor that shapes lifespan. Because host specialists can only exploit a limited number of plants, their lifecycle should be synchronised with host phenology to allow reproduction when suitable hosts are available. For species not undergoing diapause or dormancy, one strategy to achieve this could be evolving long lifespans. From a physiological perspective, oxidative stress could explain how lifespan is related to degree of host specialisation. Oxidative stress caused by Reactive Oxygen Species (ROS) might help underpin ageing (the Free Radical Theory of Aging (FRTA)) and mediate differences in lifespan. Here, we investigated how lifespan is shaped by the degree of host specialisation, phylogeny, oxidative damage accumulation and antioxidant protection in eight species of true fruit flies (Diptera: Tephritidae). We found that lifespan was not constrained by species relatedness or oxidative damage (arguing against the FRTA); nevertheless, average lifespan was positively associated with antioxidant protection. There was no lifespan difference between generalist and specialist species, but most of the tephritids studied had long lifespans in comparison with other dipterans. Long lifespan may be a trait under selection in fruit-feeding insects that do not use diapause.

Adult diet does not compensate for impact of a poor larval diet on stress resistance in a tephritid fruit fly.

Adult holometabolous insects may derive metabolic resources from either larval or adult feeding, but little is known of whether adult diets can compensate for deficiencies in the larval diet in terms of stress resistance. We investigated how stress resistance is affected and compensated for by diet across life stages in the marula fruit fly Ceratitis cosyra (Diptera: Tephritidae). Larvae were fed diets containing either 8% torula yeast, the standard diet used to rear this species, or 1% yeast (low protein content similar to known host fruit). At emergence, adults from each larval diet were tested for initial mass, water content, body composition, and desiccation and starvation resistance or they were allocated to one of two adult diet treatments: sucrose only, or sucrose and yeast hydrolysate. The same assays were then repeated after 10 days of adult feeding. Development on a low protein larval diet led to lower body mass and improved desiccation and starvation resistance in newly emerged adults, even though adults from the high protein larval diet had the highest water content. Adult feeding decreased desiccation or starvation resistance, regardless of the diet provided. Irrespective of larval diet history, newly emerged, unfed adults had significantly higher dehydration tolerance than those that were fed. Lipid reserves played a role in starvation resistance. There was no evidence for metabolic water from stored nutrients extending desiccation resistance. Our findings show the possibility of a nutrient-poor larval environment leading to correlated improvement in adult performance, at least in the short term.

Effects of macronutrient intake on the lifespan and fecundity of the marula fruit fly, Ceratitis cosyra (Tephritidae): Extreme lifespan in a host specialist.

In insects, lifespan and reproduction are strongly associated with nutrition. The ratio and amount of nutrients individuals consume affect their life expectancy and reproductive investment. The geometric framework (GF) enables us to explore how animals regulate their intake of multiple nutrients simultaneously and determine how these nutrients interact to affect life-history traits of interest. Studies using the GF on host-generalist tephritid flies have highlighted trade-offs between longevity and reproductive effort in females, mediated by the protein-to-carbohydrate (P:C) ratio that individuals consume. Here, we tested how P and C intake affect lifespan (LS) in both sexes, and female lifetime (LEP), and daily (DEP) egg production, in Ceratitis cosyra, a host-specialist tephritid fly. We then determined the P:C ratio that C. cosyra defends when offered a choice of foods. Female LS was optimized at a 0:1 P:C ratio, whereas to maximize their fecundity, females needed to consume a higher P:C ratio (LEP = 1:6 P:C; DEP = 1:2.5 P:C). In males, LS was also optimized at a low P:C ratio of 1:10. However, when given the opportunity to regulate their intake, both sexes actively defended a 1:3 P:C ratio, which is closer to the target for DEP than either LS or LEP. Our results show that female C. cosyra experienced a moderate trade-off between LS and fecundity. Moreover, the diets that maximized expression of LEP and DEP were of lower P:C ratio than those required for optimal expression of these traits in host-generalist tephritids or other generalist insects.

The NF-κB-like factor DIF could explain some positive effects of a mild stress on longevity, behavioral aging, and resistance to strong stresses in Drosophila melanogaster.

A mild cold stress can have positive effects on longevity, aging and resistance to severe stresses in flies (heat, cold, fungal infection), but the causes of these effects remain elusive. In order to know whether these effects could be explained by the DIF transcription factor (a NF-κB-like factor in the Toll innate immunity pathway), the Dif ( 1 ) mutant and its control cn bw strain were subjected to a pretreatment by cold. The DIF factor seems to be involved in the response to fungal infection after a mild cold stress and in the resistance to heat. However, DIF seems to have no role in the increased longevity of non-infected flies and resistance to a severe cold shock, because the cold pretreatment slightly increased longevity in females, mainly in Dif ( 1 ) ones, and resistance to a long cold shock in both sexes of these strains.