Luc Leblanc

An Overview of Pest Species of Bactrocera Fruit Flies (Diptera: Tephritidae) and the Integration of Biopesticides with Other Biological Approaches for Their Management with a Focus on the Pacific Region

Fruit flies (Diptera: Tephritidae) are among the most economically important pest species in the world, attacking a wide range of fruits and fleshy vegetables throughout tropical and sub-tropical areas. These species are such devastating crop pests that major control and eradication programs have been developed in various parts of the world to combat them. The array of control methods includes insecticide sprays to foliage and soil, bait-sprays, male annihilation techniques, releases of sterilized flies and parasitoids, and cultural controls. During the twenty first century there has been a trend to move away from control with organophosphate insecticides (e.g., malathion, diazinon, and naled) and towards reduced risk insecticide treatments. In this article we present an overview of 73 pest species in the genus Bactrocera, examine recent developments of reduced risk technologies for their control and explore Integrated Pest Management (IPM) Programs that integrate multiple components to manage these pests in tropical and sub-tropical areas.

An Evaluation of the Species Status of Bactrocera invadens and the Systematics of the Bactrocera dorsalis (Diptera: Tephritidae) Complex

ABSTRACT The genus Bactrocera (Tephritidae) contains >500 species, including many severe pests of fruits and vegetables. Although native to tropical and subtropical areas of Africa, India, Southeast Asia, and Australasia, a number of the pest species, largely members of the Bactrocera dorsalis (Hendel) complex, have become widespread through accidental introduction associated with agricultural trade. The B. dorsalis complex includes several morphologically and ecologically similar pests, making species designations uncertain. One of these, Bactrocera invadens Drew, Tsuruta, and White, endemic to Sri Lanka, has spread across Africa in the last decade and become a major agricultural pest. We sequenced one mitochondrial and two nuclear genes from 73 specimens, belonging to 19 species to construct phylogenies and examine species relationships and limits within the genus Bactrocera and several species of the B. dorsalis complex-specifically addressing the placement of B. invadens. Results indicate the B. dorsalis complex is polyphyletic. B. invadens and several other species within the B. dorsalis complex (B. dorsalis, Bactrocera papayae Drew &Hancock, and Bactrocera philippinensis Drew & Hancock) are also paraphyletic with respect to each other and probably represent a single genetically indistinguishable, phenotypically plastic, pest species that has spread throughout the world.

Recent advances in methyl eugenol and cue-lure technologies for fruit fly detection, monitoring, and control in Hawaii.

Worldwide, an important aspect of invasive insect pest management is more effective, safer detection and control systems. Phenyl propanoids are attractive to numerous species of Dacinae fruit flies. Methyl eugenol (ME) (4-allyl-1, 2-dimethoxybenzene-carboxylate), cue-lure (C-L) (4-(p-acetoxyphenyl)-2-butanone), and raspberry ketone (RK) (4-(p-hydroxyphenyl)-2-butanone) are powerful male-specific lures. Most evidence suggests a role of ME and C-L/RK in pheromone synthesis and mate attraction. ME and C-L/RK are used in current fruit fly programs for detection, monitoring, and control. During the Hawaii Area-Wide Pest Management Program in the interest of worker safety and convenience, liquid C-L/ME and insecticide (i.e., naled and malathion) mixtures were replaced with solid lures and insecticides. Similarly, Male Annihilation Technique (MAT) with a sprayable Specialized Pheromone and Lure Application Technology (SPLAT), in combination with ME (against Bactrocera dorsalis, oriental fruit fly) or C-L/RK (against B. cucurbitae, melon fly), and the reduced-risk insecticide, spinosad, was developed for area-wide suppression of fruit flies. The nontarget effects of ME and C-L/RK to native invertebrates were examined. Although weak attractiveness was recorded to flower-visiting insects, including bees and syrphid flies, by ME, effects to native Drosophila and other Hawaiian endemics were found to be minimal. These results suggested that the majority of previously published records, including those of endemic Drosophilidae, were actually for attraction to dead flies inside fruit fly traps. Endemic insect attraction was not an issue with C-L/RK, because B. cucurbitae were rarely found in endemic environments.

EVALUATION OF CUE-LURE AND METHYL EUGENOL SOLID LURE AND INSECTICIDE DISPENSERS FOR FRUIT FLY (DIPTERA: TEPHRITIDAE) MONITORING AND CONTROL IN TAHITI

ABSTRACT Performance of solid male lure (cuelure (C-L)/raspberry ketone (RK) against Bactrocera tryoni (Froggatt), and methyl eugenol (ME) against oriental fruit fly, B. dorsalis (Hendel)) both formulated with insecticide, were evaluated in Tahiti Island (French Polynesia), as alternatives to current monitoring and control systems using liquid formulations of attractant and organophosphate insecticides. Captures of B. tryoni in traps with BactroMAT CL stations, Mallet C-L, Mallet MC wafers (containing both ME and RK), and Specialized Pheromone and Lure Application Technology (SPLAT) C-L were as high as with the standard liquid C-L formulation until 8 weeks, but thereafter the effectiveness of Mallet C-L baited traps declined. Captures of B. dorsalis with Mallet ME wafers outperformed any other ME formulation. Traps baited with ME and RK combined in a single Mallet MC wafer captured as many B. tryoni and B. dorsalis as traps baited with a single liquid lure. This suggested that solid Mallet dispensers with RK are longer lasting than those with CL. For control applications, the weathered SPLAT-MAT-ME-spinosad lure and kill formulation was equal to fresh material for up to 4 weeks. SPLAT C-L was more persistent than weathered SPLAT-MAT-ME under Tahitian climatic conditions, which suggested that SPLAT-MAT-ME may need to be reapplied at shorter intervals and in greater amounts for suppression of B. dorsalis than is required to suppress B. tryoni with SPLAT-MAT-C-L. Mallet ME and MC wafers and SPLAT-MAT-ME/C-L were more convenient and safer to handle than standard liquid insecticide formulations, and should be considered for monitoring and control programs in Pacific island nations. The Mallet MC wafer could be used in a single trap in place of two separate traps for detection of both ME and C-L responding fruit fly species, and thereby reduce trap and labor costs. In addition to the SPLAT-MATME or C-L for control, the Mallet MC wafer in a single trap should be tested further in Florida fruit fly programs.

Attraction of Nontarget Species to Fruit Fly (Diptera: Tephritidae) Male Lures and Decaying Fruit Flies in Traps in Hawaii

ABSTRACT Synthetic male lures are commonly used to monitor and mass trap pestiferous fruit flies (Diptera: Tephritidae: Dacinae). However, there has been much dispute as to the nontarget impacts of such lures on beneficial and native insects. To evaluate nontarget attraction effects, traps baited with Cue-Lure and methyl eugenol were maintained and emptied weekly in a range of native and non-native forest and commercial orchard and backyard sites on Hawaii and Maui Islands. Lure trap captures were compared against those from unbaited control traps and traps artificially baited with decaying fruit flies to mimic the effect of accumulation of dead trapped target flies in male lure traps. Cue-Lure did not attract nontargets, and methyl eugenol attracted low but significant numbers of five species of flower-associated insects (honey bees, syrphid flies, nitidulid beetles, and endemic crambid moths) and two endemic Hawaiian species of sciarids (Diptera) and mirids (Hemiptera). Saprophagous nontargets, mostly Diptera, were abundant and diverse in traps baited with decaying flies and in male lure traps where accumulation of dead flies occurred but not in male lure traps with few or no fruit fly captures. Most of the previously published records of attraction to methyl eugenol are shown to actually be secondary attraction to decaying fruit flies. Endemic nontargets were collected in native and adjacent forest, but almost exclusively invasive species were attracted to traps placed in non-native habitats. Attraction of flower-associated species may be minimized if methyl eugenol traps are placed in trees after flowering season in orchards.

Attraction of Ceratitis capitata (Diptera: Tephritidae) and Endemic and Introduced Nontarget Insects to BioLure Bait and Its Individual Components in Hawaii

ABSTRACT BioLure, a synthetic food attractant for Mediterranean fruit fly [Ceratitis capitata (Wiedemann) ], is composed of three chemicals (ammonium acetate, trimethylamine hydrochloride, and putrescine). We deployed these components together and in separate MultiLure traps across predominantly native forests, non-native forests, farmlands, orchards, and residential areas on the islands of Hawaii and Maui, to evaluate attraction of C. capitata and nontarget insects. Large numbers (as many as 186 per trap per day) of mainly saprophagous nontarget flies (primarily Drosophilidae, Chloropidae, Lonchaeidae, Neriidae, Otitidae, and Calliphoridae) were attracted to BioLure. Very few predators, parasitoids, or pollinators were attracted. Native species, predominantly drosophilid and calliphorid flies, were attracted in large numbers in endemic forests, but mostly (at least 88%) introduced species were collected in orchards, backyards, and non-native forest. A comparison of attraction to the three separate components versus combined components in traps revealed that ammonium acetate and, to a lesser extent, putrescine are the key components attractive to nontarget species. Omitting the putrescine ingredient from BioLure did not drastically decrease C. capitata catches but reduced nontarget captures by 20%.

Suppression of melon fly (Diptera: Tephritidae) populations with releases of Fopius arisanus and Psyttalia fletcheri (Hymenoptera: Braconidae) in North Shore Oahu, HI, USA

Field experiments and surveys were conducted to evaluate the efficacy of releasing Fopius arisanus (Sonan) and Psyttalia fletcheri (Silvestri) parasitoids for suppression of Bactrocera cucurbitae (Coquillett) infesting wild Coccinia grandis L. In 2003 and 2004, P. fletcheri releases combined with natural emergence from wild fly populations resulted in better fly suppression, compared to the control site. While P. fletcheri developed freely on melon fly, F. arisanus was less successful at producing its own progeny, yet causing mortality and a twofold decrease in pupae recovered from ivy gourds. Concurrent releases of both parasitoids exerted a compounded suppressive effect on the melon fly population 2–3 times higher than during the pre-release phase. A similar, less obvious, pattern occurred in 2004, due to reduction of the ivy gourd fruit canopy. In 2005, only P. fletcheri was released, with greatly reduced impact, due to ivy gourd destruction and by growers leaving crop culls in fields, producing large numbers of melon flies unaffected by parasitoid releases.

Captures of pest fruit flies (Diptera: Tephritidae) and nontarget insects in BioLure and torula yeast traps in Hawaii.

ABSTRACT MultiLure traps were deployed in a Hawaiian orchard to compare the attraction of economically important fruit flies and nontarget insects to the three-component BioLure and torula yeast food lures. Either water or a 20% propylene glycol solution was used to dissolve the torula yeast or as capture fluid in BioLure traps. Torula yeast in water was more attractive than BioLure for male and female Bactrocera Cucurbitae (Coquillett) and Bactrocera dorsalis (Hendel) and as attractive for Ceratitis capitata (Wiedemann), and the addition of propylene glycol significantly inhibited the attractiveness of torula yeast. The known synergistic effect of propylene glycol with BioLure, resulting in increased captures of Anastrepha flies, was not observed with Bactrocera. Nontarget Drosophilidae, Neriidae, Phoridae, Calliphoridae, Sarcophagidae, and Muscidae were more strongly attracted to BioLure, and both lures collected Chloropidae equally. As with fruit flies, propylene glycol in torula yeast significantly decreased nontarget captures. The results therefore suggest that torula yeast in water is a more effective attractant than BioLure for pest Bactrocera while minimizing nontarget captures.

A phylogenetic assessment of the polyphyletic nature and intraspecific color polymorphism in the Bactrocera dorsalis complex (Diptera, Tephritidae)

Abstract The Bactrocera dorsalis complex (Tephritidae) comprises 85 species of fruit flies, including five highly destructive polyphagous fruit pests. Despite significant work on a few key pest species within the complex, little has been published on the majority of non-economic species in the complex, other than basic descriptions and illustrations of single specimens regarded as typical representatives. To elucidate the species relationships within the Bactrocera dorsalis complex, we used 159 sequences from one mitochondrial (COI) and two nuclear (elongation factor-1α and period) genes to construct a phylogeny containing 20 described species from within the complex, four additional species that may be new to science, and 26 other species from Bactrocera and its sister genus Dacus. The resulting concatenated phylogeny revealed that most of the species placed in the complex appear to be unrelated, emerging across numerous clades. This suggests that they were placed in the Bactrocera dorsalis complex based on the similarity of convergent characters, which does not appear to be diagnostic. Variations in scutum and abdomen color patterns within each of the non-economic species are presented and demonstrate that distantly-related, cryptic species overlap greatly in traditional morphological color patterns used to separate them in keys. Some of these species may not be distinguishable with confidence by means other than DNA data.

Genetic Diversity of Bactrocera dorsalis (Diptera: Tephritidae) on the Hawaiian Islands: Implications for an Introduction Pathway into California

ABSTRACT Population genetic diversity of the oriental fruit fly, Bactrocera dorsalis (Hendel), on the Hawaiian islands of Oahu, Maui, Kauai, and Hawaii (the Big Island) was estimated using DNA sequences of the mitochondrial cytochrome c oxidase subunit I gene. In total, 932 flies representing 36 sampled sites across the four islands were sequenced for a 1,500-bp fragment of the gene named the C1500 marker. Genetic variation was low on the Hawaiian Islands with >96% of flies having just two haplotypes: C1500-Haplotype 1 (63.2%) or C1500-Haplotype 2 (33.3%). The other 33 flies (3.5%) had haplotypes similar to the two dominant haplotypes. No population structure was detected among the islands or within islands. The two haplotypes were present at similar frequencies at each sample site, suggesting that flies on the various islands can be considered one population. Comparison of the Hawaiian data set to DNA sequences of 165 flies from outbreaks in California between 2006 and 2012 indicates that a single-source introduction pathway of Hawaiian origin cannot explain many of the flies in California. Hawaii, however, could not be excluded as a maternal source for 69 flies. There was no clear geographic association for Hawaiian or non-Hawaiian haplotypes in the Bay Area or Los Angeles Basin over time. This suggests that California experienced multiple, independent introductions from different sources.