Roger I. Vargas

Potential for Areawide Integrated Management of Mediterranean Fruit Fly (Diptera: Tephritidae) with a Braconid Parasitoid and a Novel Bait Spray

Abstract The braconid wasp, Fopius arisanus (Sonan), a biological control agent for Mediterranean fruit fly, Ceratitis capitata (Wiedemann), was studied in coffee, Coffea arabica L. Fopius arisanus, comprised 79.3% of the total parasitoids (7,014) recovered from fruits collected at three small coffee farms. Data from seasonal host/parasitoid studies at a large coffee plantation also suggested that the most effective natural enemy of C. capitata in coffee may now reside in Hawaii. The original parasitoids introduced into Hawaii for C. capitata control (Diachasmimorpha tryoni (Cameron), Tetrastichus giffardianus Silvestri, and Dirhinus giffardii Silvestri) are now rare. Abundance of F. arisanus with respect to other parasitoids collected was influenced by elevation (274, 457, 610 m). Fopius arisanus was the dominant parasitoid at all three elevations, Diachasmimorpha longicaudata (Ashmead) occurred consistently, and T. giffardianus was abundant only at low elevation. The impacts on C. capitata and F. arisanus populations of bait sprays containing malathion, spinosad, or phloxine B applied to coffee were also evaluated. All three bait sprays suppressed C. capitata populations. Spinosad and phloxine B bait sprays appeared less harmful to the wasp than malathion. Fopius arisanus offers the potential for areawide management of C. capitata that includes biological control and integration with more environmentally safe chemical controls such as spinosad and phloxine B bait sprays.

Incorporating Ecologically Relevant Measures of Pesticide Effect for Estimating the Compatibility of Pesticides and Biocontrol Agents

Abstract The compatibility of biological control agents with pesticides is a central concern in integrated pest management programs. The most common assessments of compatibility consist of simple comparisons of acute toxicity among pest species and select biocontrol agents. A more sophisticated approach, developed by the International Organisation of Biological Control (IOBC), is based on a tiered hierarchy made up of threshold values for mortality and sublethal effects that is used to determine the compatibility of pesticides and biological control agents. However, this method is unable to capture longer term population dynamics, which is often critical to the success of biological control and pest suppression. In this article, we used the delay in population growth index, a measure of population recovery, to investigate the potential impacts that the threshold values for levels of lethal and sublethal effects developed by the IOBC had on three biocontrol agents: sevenspotted lady beetle, Coccinella septempunctata L.; the aphid parasitoid Diaeretiella rapae (M’Intosh), and Fopius arisanus (Sonan), a parasitoid of tephritid flies. Based on life histories of these economically important natural enemies, we established a delay of 1-generation time interval as sufficient to disrupt biological control success. We found that delays equivalent to 1-generation time interval were caused by mortality as low as 50% or reductions of offspring as low as 58%, both values in line with thresholds developed by the IOBC. However, combinations of mortality and reduction of offspring lower than these values (from 32 to 43% each) over a simulated 4-mo period caused significant population delays. Furthermore, the species used in these simulations reacted differently to the same levels of effect. The parasitoid D. rapae was the most susceptible species, followed by F. arisanus and C. septempunctata. Our results indicate that it is not possible to generalize about potential long-term impacts of pesticides on biocontrol agents because susceptibility is influenced by differences in life history variables. Additionally, populations of biocontrol agents may undergo significant damage when mortality approaches 50% or when there is mortality of ≈30% and a 30% reduction in offspring caused by a sublethal effect. Our results suggest that more ecologically relevant measures of effect such as delays in population growth may advance our knowledge of pesticide impacts on populations of beneficial species.

Toxicity of Spinosad in Protein Bait to Three Economically Important Tephritid Fruit Fly Species (Diptera: Tephritidae) and Their Parasitoids (Hymenoptera: Braconidae)

Abstract The feeding toxicity of the natural insecticide spinosad in Provesta protein bait was evaluated for three economically important fruit fly species, the Mediterranean fruit fly, Ceratitis capitata (Wiedemann); the melon fly, Bactrocera cucurbitae Coquillett; and the oriental fruit fly, Bactrocera dorsalis Hendel. Both females and males were evaluated. Spinosad was remarkably similar in toxicity to all three fruit fly species. Male C. capitata (24 h LC50 values and 95% fiducial limits = 2.8 [2.60–3.0] mg/liter spinosad) were significantly, although only slightly more susceptible to spinosad than females (4.2 [3.8–4.6] mg/liter). Male (5.5 [4.7–6.6] mg/liter) and female (4.3 [3.7–4.9] mg/liter) B. cucurbitae were equally susceptible to spinosad. Female (3.3 [3.1–3.6] mg/liter) and male (3.1 [2.9–3.3] mg/liter) B. dorsalis also were equally susceptible to spinosad. Provesta bait containing spinosad also was evaluated against two parasitoids of tephritid fruit flies, Fopius arisanus (Sonan) and Pysttalia fletcheri (Silvestri). These parasitoids did not feed on the bait, so a contact toxicity test was conducted. Significant amounts of mortality were found only after exposure of parasitoids to spinosad-coated glass vials with concentrations ≥500 mg/liter spinosad. Parasitoids were less susceptible than fruit flies to such a degree that use of spinosad in bait spray should be compatible with these parasitoid species. Because the fruit flies tested in this study were so susceptible to spinosad, this product seems to be promising as a bait spray additive and a replacement for malathion for control of these species.

Comparative Demography of Three Hawaiian Fruit Flies (Diptera: Tephritidae) at Alternating Temperatures

Abstract Reproductive and population parameters of melon flies, Bactrocera cucurbitae Coquillett, oriental fruit flies, B. dorsalis Hendel, and Mediterranean fruit flies, Ceratitis capitata (Wiedemann), were measured in environmental chambers maintained at temperatures of (maximum:minimum) 24:13, 24:24, 29:18, and 35:24 ± 1°C. Alternating temperature regimes more realistically approached the variation found in nature and produced higher parameters than an optimal constant temperature (24°C). Intra- and interspecific comparisons were done with 4 separate generations of wild fruit flies reared on a common natural host. All species attained their highest intrinsic rates of population increase at 29:18 or 35:24°C; C. capitata exhibited the highest intrinsic rates of increase at all temperature regimes. All species attained maximum net reproductive rates at 29:18°C, in the order C. capitata > B. dorsalis > B. cucurbitae. The 35:24°C regime caused reductions in net reproductive rates of all species, with B. dorsalis affected most strongly. Male longevity was greater than that of females for all species in all temperature regimes. Two distinctly different life history patterns were evident: (1) early reproduction, short life span, and a high intrinsic rate of increase (C. capitata), and (2) later onset of reproduction, longer life span, and a lower intrinsic rate of increase (B. cucurbitae).

Methyl eugenol and cue-lure traps for suppression of male oriental fruit flies and melon flies (Diptera: Tephritidae) in Hawaii: effects of lure mixtures and weathering.

Abstract Methyl eugenol (4-allyl-1,2-dimethoxybenzene-carboxylate) and cue-lure [4-(p-acetoxyphenyl)-2-butanone] are highly attractive kairomone lures to oriental fruit fly, Bactrocera dorsalis (Hendel), and melon fly, B. cucurbitae (Coquillett), respectively. Plastic bucket traps were evaluated as dispensers for methyl eugenol and cue-lure for suppression of the 2 fruit flies in Hawaii. Methyl eugenol and cue-lure mixtures were compared with pure methyl eugenol or cue-lure over 4 seasons. B. dorsalis captures differed significantly with treatment and season. B. dorsalis captures with 100% methyl-eugenol were significantly greater than all other treatments (25, 50, and 75%). B. cucurbitae captures also differed significantly with treatment but not with season. Captures with 100, 75, and 50% cue-lure were not significantly different. Bucket traps baited with cue-lure (+ malathion) and weathered under Hawaiian climatic conditions were attractive to B. cucurbitae up to 8 wk. Two methyl eugenol dispensers (canec disks and Min-U-Gel) were compared with bucket traps. Dispensers (methyl eugenol + malathion) were weathered for 2–16 wk under Hawaiian climatic conditions and bioassayed during summer and winter. Initially, captures of B. dorsalis were not significantly different for the 3 dispensers. Bucket traps and canec disks were most resistant to weather, remaining attractive to B. dorsalis flies up to 16 wk. Min-U-Gel was least resistant, losing attractiveness to B. dorsalis flies within 2 wk. On the basis of performance, bucket traps and canec disks were equally long-lived up to 14 wk; thereafter, bucket traps were slightly more attractive during winter. Canec disks were cheapest, but on the basis of possible environmental concerns, bucket traps may be the best all-around choice for areawide suppression of fruit flies.

Impact of introduction of Bactrocera dorsalis (Diptera: Tephritidae) and classical biological control releases of Fopius arisanus (Hymenoptera: Braconidae) on economically important fruit flies in French Polynesia.

Abstract Oriental fruit fly,Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), was discovered on Tahiti Island in July 1996. Eradication programs were conducted from 1997 to 2001, but failed. From 1998 to 2006,B.dorsalis was recovered from 29 different host fruit from the five Society Islands: Tahiti, Moorea, Raiatea, Tahaa, and Huahine. Analysis of coinfestation patterns byB.dorsalis,Bactrocera tryoni (Froggatt), andBactrocera kirki (Froggatt) suggestedB.dorsalis had displaced these two species and become the most abundant fruit fly in coastal areas. To suppressB.dorsalis populations, a classical biological control program was initiated to introduce the natural enemyFopius arisanus (Sonan) (Hymenoptera: Braconidae) into French Polynesia from Hawaii. Wasps were released and established on Tahiti, Moorea, Raiatea, Tahaa, and Huahine Islands. In guava,Psidium guajava L., collections for Tahiti,F.arisanus parasitism of fruit flies was 2.1, 31.8, 37.5, and 51.9% for fruit collected for 2003, 2004, 2005 and 2006, respectively. Based on guava collections in 2002 (before releases) and 2006 (after releases), there was a subsequent decrease in numbers ofB.dorsalis,B.tryoni, andB.kirki fruit flies emerging (per kilogram of fruit) by 75.6, 79.3, and 97.9%, respectively. These increases inF.arisanus parasitism and decreases in infestation were similar for other host fruit. Establishment ofF.arisanus is the most successful example of classical biological control of fruit flies in the Pacific area outside of Hawaii and serves as a model for introduction into South America, Africa, and China where species of theB.dorsalis complex are established.

Attraction and feeding responses of Mediterranean fruit fly and a natural enemy to protein baits laced with two novel toxins, phloxine B and spinosada

Studies were conducted to determine attraction and feeding propensity of Mediterranean fruit fly, Ceratitis capitata (Wiedemann), to different protein bait mixtures with and without the insecticides malathion, spinosad, and phloxine B. Protein baits were more attractive to females than to males. Protein‐starved females responded more than protein‐fed females. The type of protein (USB® yeast hydrolysate enzymatic, Mazoferm®E802, Nu‐Lure®Insect Bait, or Provesta® 621 autolyzed yeast extract) in the bait had a major influence on C. capitata attraction, which was strongest to fresh Provesta. Aged baits (four day‐old) were not as attractive as fresh baits. In feeding propensity studies, highest response was observed for USB protein. On the basis of attraction and feeding responses Provesta (attraction and feeding) and USB (feeding) outperformed the standard Nu‐Lure. Protein‐starved flies were much more likely to feed on protein compared to protein‐fed flies. For protein‐starved flies, a mixture of Provesta and malathion repelled fruit flies, compared to a mixture of Provesta and spinosad or phloxine B. This was not the case with protein–fed flies. The wasp Fopius arisanus (Sonan), one of C. capitatas primary natural enemies in Hawaii, would not consume protein baits. Our studies suggest that spinosad or phloxine B, with low contact toxicity, mixed with protein baits offers a more environmentally friendly choice for control of C. capitata and conservation of F. arisanus, whereby the nontarget effects of broad spectrum contact poisons such as malathion can be avoided. Presumably, due to greater selectivity with spinosad and phloxine B bait treatments, the host would be killed, but not the natural enemy.

Sexual communication and related behaviours in Tephritidae: current knowledge and potential applications for Integrated Pest Management

Tephritidae are an enormous threat to fruit and vegetable production throughout the world, causing both quantitative and qualitative losses. Investigating mating sequences could help to unravel mate choice dynamics, adding useful information to improve behaviour-based control strategies. We review current knowledge about sexual communication and related behaviours in Tephritidae, with a focus on six key agricultural pests: Anastrepha ludens, Bactrocera cucurbitae, Bactrocera dorsalis, Bactrocera oleae, Ceratitis capitata and Rhagoletis pomonella. We examine features and the role of male–male combat in lekking sites, cues affecting mating dynamics, and some fitness-promoting female behaviours that occur at oviposition sites [the use of oviposition marking pheromones (OMPs) and female–female fights for single oviposition sites]. We outline future perspectives and potential contributions of knowledge about sexual communication to Integrated Pest Management programs for tephritid pests. Sexually selected traits are frequently good indicators of male fitness and knowledge of sexual selection processes may contribute to the improvement of the sterile insect technique (SIT), to select genotypes with high reproductive success and to promote sexually selected phenotypes through mass-rearing optimization. Furthermore, males’ exposure to parapheromones, such as phenyl propanoids (PPs), ginger root oil and trimedlure can enhance the mating success of sterile flies used in SIT programs. PPs are also a powerful tool to improve reduced-risk monitoring dispensers and the male annihilation technique, with low side effects on non-target insects. Lastly, we outline the possibility to sensitise or train mass-reared parasitoids on OMPs during the pre-release phase, in order to improve their post-release performance in the field.

Managing Oriental Fruit Fly (Diptera: Tephritidae), With Spinosad-Based Protein Bait Sprays and Sanitation in Papaya Orchards in Hawaii

ABSTRACT The efficacy of GF-120 NF Naturalyte Fruit Fly Bait in combination with field sanitation was assessed as a control for female oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), in papaya (Carica papaya L.) orchards in Hawaii. Three different bait spray regimes were evaluated: every row (high use of the bait), every fifth row (moderate use), and every 10th row (low use). Orchard plots in which no bait was applied served as controls. For five of the seven biweekly periods that followed the first bait spray, trapping data revealed significantly fewer female B. dorsalis captured in plots subject to high and moderate bait use than in control plots. Differences in incidence of infestation among treatments were detected only by the third (12 wk after first spray) fruit sampling with significantly fewer infested one-fourth to bonehead ripe papaya fruit in plots subject to high and moderate bait use than in control plots. Parasitism rates by Fopius arisanus (Sonan) (Hymenoptera: Braconidae) were not negatively affected by bait application. Results indicate that foliar applications of GF-120 NF Naturalyte Fruit Fly Bait either to all rows (every other tree), or to every fifth row (every tree) in combination with good sanitation can effectively reduce infestation by B. dorsalis in papaya orchards in Hawaii.

Response of female melon fly, Bactrocera cucurbitae, to host‐associated visual and olfactory stimuli

In a series of studies conducted in Hawaii under seminatural conditions, we quantified the response of sexually mature, host‐seeking female melon flies, Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae), to different types of visual and chemical host‐associated stimuli with the main aim of developing a monitoring device for females. Experiments were conducted using Tangletrap‐coated fruit mimics of either spherical (8 cm diameter) or cylindrical (4.3 cm diameter; 15 cm length) shapes coated with different artificial color pigments both at the ground level and at the tree‐canopy level so as to take into account the foraging behavior of adult melon flies. Females were particularly attracted to objects of spherical shape colored either yellow, white, or orange; these three pigments offered the highest reflectance values. Cucumber (Cucumis sativus L.) (Cucurbitaceae) odor was more attractive to females than odors of three other cultivated host fruit [zucchini, Cucurbita pepo L. var. medullosa Alef. (Cucurbitaceae); papaya, Carica papaya L. (Caricaceae); or tomato Solanum lycopersicum L. (Solanaceae)] or of ivy gourd [Coccinia grandis (L.) Voigt (Cucurbitaceae)], one of the major wild hosts of melon fly in Hawaii. A combination of both visual and olfactory stimuli was needed to elicit high levels of response compared to each stimulus offered alone. We discuss our results in relation to the potential implementation of improved female monitoring and/or attract‐and‐kill strategies for melon flies in Hawaii.