Season‐long mating disruption of citrus leafminer,Phyllocnistis citrella Stainton,with an emulsified wax formulation of pheromone

The citrus leafminer, Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae), is a major worldwide pest of citrus. Larval feeding by this insect facilitates proliferation of citrus bacterial canker, Xanthomonas axonopodis pv. citri. Herein, we describe a season‐long disruption trial of P. citrella with a newly developed, emulsified wax dispenser of pheromone (SPLAT‐CLM^TM). A formulation containing a 3 : 1 blend of (Z,Z,E)‐7,11,13‐hexadecatrienal:(Z,Z)‐7,11‐hexadecadienal at a 0.2% loading rate of active ingredient by weight and deployed twice per season (24 weeks total) at 490 g of formulation/ha caused season‐long disruption of male moth catch in pheromone traps as well as reduced leaf infestation. Analysis of pheromone release from dispensers by gas chromatography revealed that effective disruption of P. citrella occurred at a deployment rate of 126 μg of (Z,Z,E)‐7,11,13‐hexadecatrienal/ha/h. Direct observation of moth behaviour in the field suggested that disruption by this formulation occurred by a non‐competitive mechanism. A formulation of the 3 : 1 attractive blend at a 0.02% pheromone loading rate caused only 2–6 weeks of disruption per deployment and did not reduce leaf infestation during mid and end of the season evaluations. A formulation containing 0.2% of (Z,Z)‐7,11‐hexadecadienal alone and deployed at 490 g/ha caused 6–7 weeks of moth disruption to pheromone traps and did not prevent leaf infestation, while an identical formulation loaded with 0.02% (w/w) of (Z,Z)‐7,11‐hexadecadienal alone had no effect on P. citrella orientation to pheromone traps. The SPLAT formulation evaluated herein appears to be an excellent release device for (Z,Z,E)‐7,11,13‐hexadecatrienal given that approximately 100 days of steady release occurred following an initial brief (ca. 7 days) burst of higher release. The advantages of SPLAT as a formulation for P. citrella disruption include low cost of manufacturing, biodegradable and weather resistant characteristics, and flowability allowing machine application. Mating disruption should be an effective alternative to insecticides for management of P. citrella and may reduce the incidence of citrus canker.     

Factors influencing adult female oviposition in the citrus leafminer Phyllocnistis citrella

1 The citrus leafminer (CLM) Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) is a serious pest in most citrus‐growing regions of the world. The influence of leaf length, citrus species or variety, leaf colour tone and temperature on CLM oviposition was studied from field observations and laboratory experiments. The spatial distribution of eggs on leaves was also examined. Field data were obtained from 1100 samples collected in eastern Spain for 7 years. 2 Significant differences in oviposition rate were found among citrus species in ‘no choice’ laboratory experiments. This tendency was not apparent in the field due to the confounding effect of such factors as the intensity of new flushes and adult CLM abundance. Leaf colour tone and air temperature in the range studied (18–27°C) had no effect on CLM egg‐laying. 3 The distribution of eggs among leaves was random for population densities lower than four eggs per leaf, but became strongly aggregated above this, when not all eggs could survive and complete development. 4 The CLM developmental stage found on leaves depended on the leaf length, and most of the egg‐laying occurred only on leaves that were 10–25 mm long. These leaves had the highest CLM stages in the field and thus give the best estimate of CLM oviposition.     

Natural mortality factors acting on citrus leafminer, Phyllocnistis citrella, in lime orchards in South Florida

Seasonal mortality of the citrusleafminer, Phyllocnistis citrellaStainton, was studied from 1994 through 1998 in`Tahiti' lime, Citrus aurantifolia (Christm.) Swingle,in Homestead, Florida. Survival of eachdevelopmental host stage and the proportionattacked by indigenous and introduced naturalenemies were determined. Before the recovery ofthe introduced parasitoid, Ageniaspiscitricola Logvinovskaya, in 1995, thethird-instar host had the highest averageproportion of parasitized individuals (0.14)followed by the prepupa (0.11) while the firstinstar had the lowest proportion parasitized(0.02). After the first recovery andestablishment of A. citricola, theproportion of pupae parasitized increased to0.56 followed by the prepupa (0.14) and thethird instar (0.11). Before the introduction ofA. citricola, the highest proportion ofhosts killed by predation was observed insecond instar (0.17) and third instar (0.15).After the establishment of the introducedspecies, the proportion of dead individuals dueto predation was greater for second instar(0.31) and third instar (0.21) larvae.Mortality caused by indigenous natural enemieswas significantly correlated with increases ofP. citrella density. Parasitism ofP. citrella by the exotic parasitoid,A. citricola, correlated less well to hostdensity over the season (r² = 0.12) thandid mortality caused by indigenous naturalenemies (r² = 0.76). Moreover, a higherpercent mortality in population of P. citrellawas obtained from predation by theindigenous natural enemies than the introducedparasitoid as shown in the mortality estimatesfrom 1995 to 1998.     

Volumes of petroleum spray oil required for control of Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) in mature citrus orchards

Studies on the relationship between volume of spray and suppression of citrus leafminer ( Phyllocnistis citrella ) oviposition by petroleum spray oil on 4 m-high mature orange trees showed a negative exponential relationship between spray volume and the number of mines per leaf. Significant reductions in the number of mines per leaf compared to unsprayed trees was achieved at spray volumes of ≥ 3300 L/ha using oscillating boom and at ≥ 3200 L/ha using rotary atomiser sprayers. However, improvements in efficacy at volumes over 3200–3300 L/ha were not significant and so of little practical value. The optimal spray volumes for citrus leafminer control are therefore suggested to be 3000–3500 L/ha. No significant difference in effectiveness was found between the oscillating boom at 3300 L/ha and a rotary atomiser at 3200 L/ha. The effect of oil spray on the citrus leafminer parasitoid Semielacher petiolatus (Girault) (Hymenoptera: Eulophidae) was inconsistent. Improved droplet deposition and coalescence may enhance the coverage of new growths and increase the efficacy of oil spray for protection of plants from oviposition.     

Towards the identification and synthesis of the sex pheromone of the citrus leafminer, Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae)

The objective of this work was to characterize the sexual behavior of the citrus leafminer, Phyllocnistis citrella Stainton, as the foundation for the isolation, identification, and synthesis of the complete sex pheromone of this species. Mating occurred in a time window of 2h, starting 1h before the onset of photophase. The large majority of tested insects mated in the first two days after emergence, with no significant difference between mating at day 1 and day 2. A stereotypical courtship and copulation behavior were described for this species. When mating was successful, the copulation was recorded in average for 49.6 min. In Y-olfactometer tests conducted at the time of mating activity, males were strongly attracted to caged virgin females as well as to extracts from putative pheromone glands.     

Factors affecting male Prays oleae (Lepidoptera: Yponomeutidae) captures in pheromone-baited traps in olive orchards

Effects of trap design, height and side of trap placement on olive trees, pheromone doses in dispensers, aging of dispensers in the field, and secondary pheromone components were evaluated for the development of an effective pheromone monitoring system for Prays oleae (Bernard) Lesne (Lepidoptera: Yponomeutidae) in olive orchards. Field trials showed that trap design, pheromone dose, and trapping side affected male captures, whereas dispenser age, trap height, and secondary components had no influence. Pherocon 1C and Delta traps baited with 1 mg of (Z)-7-tetradecenal captured more male moths than Pherocon II or Funnel traps. Placement of traps at different cardinal directions significantly affected captures, but this trend was not consistent and varied with flight period and trap position internal or external to the tree canopy. Moth phenology as determined by pheromone traps from early April to mid-October was consistent with published field data. Results indicate that Pherocon 1C or Delta traps baited with 1 mg of (Z)-7-tetradecenal provide an effective tool for monitoring the flight activity of P. oleae and the time of application of control measures.     

Changes in predation and parasitism of the citrus leafminer Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) populations in Spain following establishment of Citrostichus phyllocnistoides (Hymenoptera: Eulophidae)

The citrus leafminer, Phyllocnistis citrella, is a pest native to Southeast Asia which threatened the citrus industry in the Mediterranean region upon its introduction in 1993. Immediately afterward, a classical biological control program was implemented in Spain. The exotic parasitoid Citrostichus phyllocnistoides was the only introduced parasitoid to become established. In 2006, data on both the incidence of P. citrella and the impact of its natural enemies were collected following the same protocols used in 1997–1999 when C. phyllocnistoides was not yet present. C. phyllocnistoides constituted 99.4% of the parasitoids collected in 2006 corresponding to a decrease in the incidence of P. citrella from 3.2–5.1 to 1.8–2.4 mines per leaf in 1997–1999 and 2006, respectively. Mortality caused by natural enemies on P. citrella in 2006 was 93.3% (18.0% parasitism, 40.8% feeding punctures and 34.5% predation). C. phyllocnistoides, which preferentially parasitizes P. citrella second instar larvae, has displaced most of the indigenous parasitoids that moved onto P. citrella mainly parasitizing third instar larvae, upon its introduction. Because C. phyllocnistoides is an idiobiont parasitoid and preferentially parasitizes P. citrella second instars, this stage has become dominant in the orchards. The shift in the relative abundance of P. citrella larvae has prompted generalist predators to prey mostly on second instars and has contributed to the displacement of the native non-specific parasitoids, which principally utilize third instars, from the system. Both indigenous predators and the introduced parasitoid are key players in the natural regulation of P. citrella.     

Sex pheromone traps for monitoring the codling moth: effect of dispenser type, field aging of dispenser, pheromone dose and type of trap on male captures

The effects of dispenser type, dispenser aging in the field, pheromone dose in the dispenser and trap type on trapping efficiency of codling moth,Cydia pomonella (L.), males were investigated in Israel. An Israeli-manufactured rubber septum was significantly better than the CM Pherocon cap in attracting males to a Pherocon 1C cap trap or an IPS trap. The effect of aging of the dispenser in the field on trapping efficiency was significant in CM Pherocon caps and the Israeli septa. Captures in traps were negatively correlated with aging of septa. The effect of aging of dispensers was more marked during summer than during spring. The fairly rapid loss of attractancy indicates that the lures should be replaced after 2 weeks at the most. The release rate of the pheromone from the dispensers was measured in a flow system. The emission from the Israeli septa and Pherocon caps decreased sharply after 2 weeks and then was almost constant, which explains the lower attractancy of aged septa. However, there was a marked difference in the release profiles of the pheromone from the two types of dispensers, which may explain the different performance of the two dispensers. Within the range of 0.1 to 100 μg pheromone per dispenser, male response increased positively with the pheromone dose. Pheromone loadings of 100 or 1000 μg per dispenser did not differ significantly in their attractiveness for males. A load of 5000 μg per dispenser was significantly less attractive to males than was 100 or 1000 μg per dispenser. The non-sticky IPS trap was significantly better in capturing codling moth males than was the sticky, commonly used Pherocon 1C trap, provided it was baited with the Israeli dispenser. The two traps were equally effective when baited with the CM Pherocon caps. The possibility of using the non-sticky, nonsaturating and easy-to-handle IPS traps for monitoring codling moth is of great importance. Contribution from the Agricultural Research Organization, The Volcani Center, Bet Dagan 50-250, Israel. No 3702-E, 1992 series.     

悬挂高度和位置对性诱剂诱集柑桔潜叶蛾雄虫效果的影响

本文研究了红心蜜柚园和新余蜜橘园中诱捕器悬挂高度、设置距离对性诱剂诱集柑桔潜叶蛾Phyllocnistis citrella Stainton雄虫效果的影响.结果表明,诱捕器悬挂的垂直高度明显影响性诱剂对柑桔潜叶蛾雄虫诱集量,同时这个影响随着高度相对树干的水平位置变化而变化.诱捕器最佳悬挂位置是三分之二树高的树冠底部边...     

Seasonal dynamics, dispersion, sequential sampling plans and treatment thresholds for the citrus leafminer, Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae), in a mature lemon block in coastal New South Wales, Australia

Abstract  Studies of citrus leafminer in a coastal orchard in NSW, Australia indicated that an increase in abundance to about one mine per flush was followed during the midseason flush by a rapid increase in population that was related to an increase in the percentage of leaves infested within flushes and the number of mines per leaf. The fits of frequency distributions and Iwao's patchiness regression indicated that populations were highly contagious initially, and as the exponent k of the negative binomial distribution increased with increasing population density, the distribution approached random. Concurrently, the coefficient of variation of mines per flush (which was strongly related to the proportion of un-infested flushes) decreased to about unity as the proportion of un-infested flushes reached zero and fell further as the number of mines per flush increased. Both numerative and binomial sequential sampling plans were developed using a decision threshold based on 1.2 mines per flush. The binomial sampling plan was based on a closely fitting model of the functional relationship between mean density and proportion of infested flushes. Functional relationships using the parameters determined from Iwao's patchiness regression and Taylor's power law were equally satisfactory, and one based on the negative binomial model also fitted well, but the Poisson model did not. The three best fitting models indicated that a decision threshold of 1.2 mines per flush was equivalent to 50% of flushes infested. From a practical point of view, the transition from 25% infestation of flushes through 50% is so rapid that it may be prudent to take action when the 25% level is reached; otherwise, the 50% may be passed before the crop is checked again. For valuable nursery stock should infestation be detected in spring, it may be advisable to apply prophylactic treatment as the midseason flush starts.     

Characterization of the sexual responses of male tsetse flies, Glossina morsitans morsitans, to pheromone-baited decoy 'females' in the field

ABSTRACT. The sexual behaviour of male Glossina morsitans morsitans Westwood (Diptera: Glossinidae) towards decoys dosed with sex phero-mone (15,19,23-trimethylheptatriacontane) is described quantitatively from field observations. The flies responded with a standard behavioural pattern after landing. This involved: first, the perception of pheromone; second, orientation on the decoy and genitalia engagement; and third, a lengthy quiescence corresponding to natural copulation. The probability of a fly leaving a decoy decreased during the sequence and was least in the final 'copulatory' phase, when it remained constant under constant conditions. The initial, rapid rates at which flies left decoys were affected mostly by pheromone dose: the lower the dose, the higher the rate. The final, slow rate of leaving was unaffected by pheromone dose, being most affected by environmental stimuli, especially interference from other flies: at high fly densities, final rates of leaving were high. The results are discussed in the context of improving the potential for using pheromone and chemo-sterilant-dosed decoys for tsetse autosterilization.     

Parasitoid complex of citrus leafminer, Phyllocnistis citrellaon lemon in the Central Jordan Valley

From March 1997 to June 1999, samples of lemonleaves infested with citrus leafminer (CLM),Phyllocnistis citrella Stainton(Lepidoptera: Gracillariidae), were collectedfrom the Al-Masalha Citrus Orchard in theCentral Jordan Valley in order to rear CLMparasitoids and to study their populationtrends. Nine species of eulophid parasitoidswere reared from CLM larvae; these were Cirrospilus ingenuus Gahan, C. pictusNees, Pnigalio agraules, Pnigalio sp. B,Pnigalio sp. C, Citrostichusphyllocnistoides Narayanan, Ratzeburgiolaincompleata Boucek, Semielacherpetiolatus Girault, and Zagrammosoma sp.Cirrospilus ingenuus was the most commonparasitoid of CLM from March 1997 to June 1999and could be a good potential biologicalcontrol agent after rearing and releasing it incitrus orchards in the Jordan Valley. Onehyperparasitoid species was reared fromimmatures of parasitoids of CLM larvae, andidentified as Tyndrichus sp. An increasein the activity of parasitoids was observed inautumn 1999 when the temperature was between 15–20 °C and the relative humidity was between 55–65%.     

Behaviour of male European corn borer, Ostrinia nubilalis Hübner (Lep.; Crambidae) towards pheromone-baited delta traps, bucket traps and wire mesh cone traps

Abstract:  Pheromone-baited traps are used to monitor the flight of European corn borer (ECB; Ostrinia nubilalis ). Traps of various designs are available: bucket traps, delta sticky traps and wire mesh cone traps. However, these traps are not all equally efficient and little is known about the reasons for this difference in efficiency. We investigated the behaviour of ECB males towards bucket traps and delta traps by means of observation in a wind tunnel. We also carried out observations and capture trials with delta traps and wire mesh cone traps in field conditions. Our laboratory studies showed that ECB males were not optimally attracted and were poorly captured by a pheromone baited bucket trap. Furthermore, they were shown to readily enter delta traps in the wind tunnel but were caught after more than three passages through this trap. Field studies showed that wire mesh cone traps captured approximately six times more ECB males than delta traps. Observation of the behaviour of ECB males showed that this difference was due to more efficient moth capture rather than greater attraction of the moth. In total, 31.5% of the 219 males observed close to wire mesh cone traps were caught, vs. 2.5% of the 520 males observed close to delta traps. This greater efficiency is due to a better capture rate of the attracted males by wire mesh cone traps than by delta traps.     

Contribution of predation and parasitism to mortality of citrus leafminer Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) populations in Florida

The citrus leafminer (CLM), Phyllocnistis citrella Stainton, is native to southern Asia and regarded as an important pest in nurseries and young or top-worked citrus trees in Florida. Damage to the leaf cuticle increases susceptibility to citrus canker disease and further aids spread by increasing inoculum loads. Biological control agents are known to play an important role in regulating pest populations. We evaluated individual contributions of predation and parasitisation to cohorts of P. citrella by exclusion and by direct observation of leaf mines in the field. Predation, particularly by ants, was the largest single cause of P. citrella mortality, accounting for more than 30% of all deaths by natural enemies, and 60% of all deaths by predators. First and second instars of P. citrella were most subject to ant predation. Ageniaspis citricola was the most important parasitoid of P. citrella and caused 8.2–28.6% mortality compared to 9.6–14.7% from indigenous parasitoids. The total biotic mortality of P. citrella observed in exclusion experiments was 52–85%. These results were in basic agreement with 89% mortality, predominantly by predation, obtained by reconstructing a cohort from observations of recently mined leaves. A partial life table based on these data predicted an innate rate of increase (R_o) of 2.8 and thus an almost 3-fold increase per generation. These results indicate that, while biotic mortality takes considerable toll of P. citrella populations, the predominance of predation suggests that the parasitoid complex on this exotic pest in Florida is depauperate and would likely be improved by additional introductions.     

Observations on the mating behavior of the alfalfa blotch leafminer,Agromyza frontella (Rondani) (Diptera: Agromyzidae), and evidence of a female sex pheromone

The mating behavior of Agromyza frontella was studied under laboratory conditions. Adults were able to mate on the day of emergence, with no evident periodicity throughout the photophase. The host plant was essential for mating to occur, its presence affecting female receptivity rather than male copulatory behavior. Males generally entered a stationary phase once in the proximity of a female, before undertaking a final approach. This stationary behavior frequently resulted in male aggregations around a female, and under such conditions males exhibited a characteristic wing vibrating behavior. As male wing vibration was not an essential behavior for successful mating, and rarely occurred during male encounters in the absence of females or when only one male was near a female, it was considered as being primarily a male-male signal. The majority of females that mated exhibited an ovipositor pumping behavior that stimulated the male approach. However, such behavior was not essential to attract mates, as dead females elicited the entire sequence of male mating behavior. This suggested the presence of a cuticular sex pheromone, as reported for other species of higher Diptera. Whole virgin female (<24- h or 3- day-old) hexane extracts applied to male cadavers increased the time males spent on the plant, the number of contacts with the treated cadavers, the incidence of attempted copulations, and the wing vibrating behavior between males compared with controls using untreated cadavers. The results obtained indicate that females control copulation in A. frontella and that both semiochemical and visual cues are important in eliciting male mating behavior.     

Differences in water relations among the citrus leafminer and two different populations of its parasitoid inhabiting the same apparent microhabitat

The water balance relationships of adult females and pupae of two populations (Australian and Taiwan) of the parasitic wasp Ageniaspis citricola, a biological control agent of the citrus leafminer Phyllocnistis citrella, were compared to determine whether habitat preferences might differ between them. No differences were detected between Australian and Taiwan strains of the wasp during the pupal stage, but adult females from the Australian strain had lower net water loss rates than the parasitoid adults from Taiwan. This implies a greater moisture requirement by adults of the Taiwan strain, which should be considered before they are released into a new environment in classical biological control programs.     

Disruption of male spruce budworm orientation to female moths by pheromone and pheromone analogues in a wind tunnel

Abstract. The ability of male spruce budworm moths, Choristoneura fumiferana (Clem.), to orientate to and locate virgin female moths was investigated in a laboratory wind tunnel. When presented with two caged ‘target female’ moths, more than 99% of the male moths locked on and flew directly to the females. When confined for 3 h before release, downwind of a three-dimensional array of thirty-five evenly distributed female moths (a density of 40/m³), over 90% of the males still successfully oriented to one or another of the females, although not always to the target females. With an array of thirty-five septa containing either E-11-tetradecenyl acetate on E-11-tetradecenol there was no visible change in behaviour; >90% of the males flew directly to the two target females, which indicates that neither the acetate nor the alcohol has potential for mating disruption. An array of thirty-five septa containing a 955 blend of E- and Z-11-tetradecenal, the main components of the spruce budworm sex pheromone, significantly reduced the numbers of male moths able to locate the target females, and effects were concentration-dependent. The highest concentration, which gave a release rate similar to that of a calling female, produced the same level of disruption as the thirty-five females, but sensory fatigue became a factor in addition to ‘false trail following’. Lower concentrations were significantly less effective, with no evidence of sensory fatigue. At all concentrations significant numbers of males flew to the septa (false trail following), but when male moths were left uncaged in the tunnel for a further 3h, most eventually located the females. This suggests that false trail following alone will not prevent mating. The level of disruption was not improved by the addition of 2% tetradecanal to the 955 blend. Similar levels of disruption to the 955 blend were obtained with an 80:20 blend. A 5050 blend still caused a significant amount of false trail following, but less than the other blends. The ability of male spruce budworm to orientate to off-blend trails was enhanced if the males were first exposed to the natural, female-produced pheromone.     

Population dynamics and functional response of Citrostichus phyllocnistoides (Narayanan) (Hym., Eulophidae) on citrus leaf-miner, Phyllocnistis citrella Stainton (Lep., Phyllocnistidae) in Fuzhou region of south-east China

Abstract:  Population dynamics of the citrus leaf-miner (CLM) Phyllocnistis citrella Stainton, and its major parasitoid Citrostichus phyllocnistoides (Narayanan) were investigated from June to September 1994 at the teaching and research farm of the Fujian Agricultural and Forestry University (FAFU), south-east China. Based on the field investigation, the functional and numerical responses of C. phyllocnistoides were studied in laboratory experiments. During the survey period, four peaks of CLM and C. phyllocnistoides populations were observed in the growing stage of summer shoots and two peaks of CLM and C. phyllocnistoides populations, respectively, in the growing stage of fall shoots. C. phyllocnistoides is the most abundant parasitoid both in seasonal and spatial dynamics, and demonstrates a Holling type III functional response to CLM. Parasitism varied with the densities of both parasitoid and host. A 1 : 10 ratio was recorded to be an optimal proportion of C. phyllocnistoides to CLM.