Insects 2015, 6, 297-318; doi:10.3390/insects6020297 OPEN ACCESS insects ISSN 2075-4450 www.mdpi.com/journal/insects/ Review 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 Roger I. Vargas 1,*, Jaime C. Piñero 2,† and Luc Leblanc 3,† 1 Daniel K. Inouye, U.S. Pacific Basin Agricultural Research Center, Agricultural Research Service, United States Department of Agriculture, 64 Nowelo St., Hilo, HI 96720, USA 2 Cooperative Research and Extension, Lincoln University, 900 Chestnut St., Allen Hall 212, Jefferson City, MO 65101, USA; E-Mail: [email protected] 3 Department of Plant and Environmental Protection Sciences, College of Tropical Agriculture and Human Resources, University of Hawaii, 3050 Maile Way, Room 310, Honolulu, HI 96822, USA; E-Mail: [email protected] † These authors contributed equally to this work. * Author to whom correspondence should be addressed; E-Mail: [email protected]; Tel.: +1-808-959-4329; Fax: +1-808-959-5470. Academic Editor: Michael J. Stout Received: 10 March 2015 / Accepted: 25 March 2015 / Published: 3 April 2015 Abstract: 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. Insects 2015, 6 298 Keywords: area wide control; reduced risk insecticides; IPM; Bactrocera dorsalis; Bactrocera cucurbitae; Bactrocera tryoni 1. Introduction Fruit flies of the family Tephritidae constitute a group of agricultural pests of worldwide importance that attack a wide range of fruits and vegetables [1]. Numerous fruit fly species constitute enormous threats to fruit and vegetable production throughout the world, causing both quantitative and qualitative losses. Furthermore, due to their susceptibility to invasive tephritid species, many fruit-producing countries have imposed quarantine restrictions on the import of products from countries infested with particular fruit fly species, and/or require that fruits and vegetables undergo quarantine treatment before their importation is allowed [2]. Thus, suppression or eradication of fruit flies has often been the goal of control programs. Integrated Pest Management (IPM) is one method to achieve sustainable agricultural production with less damage to the environment [3]. While IPM has many definitions, it often includes a diverse mix of approaches to manage pests and keep them below economically damaging levels, using control options that range from cultural to chemical components. In practice, IPM ranges from chemically-based systems that involve the targeted and judicious use of synthetic pesticides, to biologically-intensive approaches that manage pests primarily or fully through nonchemical means [4]. In recent years, IPM has been seen as an effective method for managing pestiferous fruit flies in an attempt to make fruit production more sustainable [2]. The genus Bactrocera Macquart comprises 651 described species. It is the most economically significant fruit fly genus with at least 50 species considered to be important pests, many of which are highly polyphagous [1,5] (Table 1). The genus Bactrocera is widely distributed throughout tropical Asia, the south Pacific and Australia. Relatively few species exist in Africa, and only olive fly, B. oleae (Rossi), occurs in Southern Europe [1]. Recently, B. oleae became established in California and two species in the B. dorsalis complex became established on two new continents: B. carambolae Drew & Hancock, the carambola fruit fly, in South America (Suriname) and B. dorsalis (formerly B. invadens Drew, Tsuruta & White) in Africa (Kenya) [6,7]. The oriental fruit fly, B. dorsalis (Hendel), is native throughout tropical Asia, and has been recorded from over 270 host plant species [1,5,8]. While IPM of fruit flies has made many unique contributions to agriculture through the incorporation of ecological principles into pest management, truly effective IPM systems are scarce. A literature search performed in ISI Web of Science in early-March, 2015 returned 4841 articles published since 1984 when “Tephritidae” was searched, and 1543 articles were returned when IPM (focusing on agriculture) was used as key word. Surprisingly, the search returned only 54 articles when both “Tephritidae” and “IPM” were searched and less than half of those truly referred to IPM components. By refining these studies by the term “Bactrocera”, only 28 articles were returned. Clearly, while different search terms certainly would change the corresponding results, it can be seen that IPM of fruit flies, including Bactrocera make up only a small proportion of the overall Tephritidae literature. Examples of IPM programs targeting Bactrocera species include the Regional Fruit Fly Project in the Pacific that targeted Bactrocera fruit flies in Pacific Island Countries and Territories [9,10]and the Insects 2015, 6 299 Hawaii Area-Wide IPM program (HAWPM), implemented over a 10-year period in Hawaii. The HAWPM program was not aimed at eradication of fruit flies, but predicated on a pest management strategy that would reduce the entire population in and around cropping areas where economic damage occurred [2]. In practice, implementation of IPM programs targeting fruit flies should be based on a particular crop/pest/environment scenario, IPM goals, e.g., temporal/spatial scales for implementation, knowledge of pest ecology and natural enemies, as well as knowledge of socio-economic factors [11,12]. IPM programs against pestiferous fruit fly species can be implemented at local (e.g., single orchard) and regional (e.g., area-wide IPM) levels and not all IPM components that may be available for a given system would be appropriate or affordable for implementation in small-scale farming operations. In this article we present an overview of the tropical pest species in the genus Bactrocera, examine recent developments of reduced risk technologies for control and explore IPM programs that utilize multiple components to manage these pests in tropical and sub-tropical areas. 2. Overview of Pest Bactrocera Species Seventy-three species of Bactrocera have been reared from commercial and/or edible host fruit, hence they are treated here as destructive or potential pests, out of a total of 210 species reared from over 811 host species [8,13–19]. Individual species are generalist or specialist pests of fruit (57 species). Some species infest fruit and/or flowers of cucurbits (16 species). All 73 Bactrocera species that are economically important are listed in Table 1, ranked under four categories, based on pest severity, host range, invasiveness, and frequency of infestation. Category A includes widespread invasive polyphagous generalists or highly destructive specialists that have become established outside of their native range (Figures 1–3). Category B pests are polyphagous fruit pests or destructive specialists more restricted in distribution, but at elevated risk of spreading to new locations (Figure 4). Under category C we list relatively minor oligophagous or specialist fruit or cucurbit pests. Category D includes species that have been occasionally bred from commercial/edible fruit or cucurbits. Among the most destructive Category A species are B. dorsalis (oriental fruit fly), B. cucurbitae (Coquillett) (melon fly) and B. tryoni (Froggatt) (Queensland fruit fly). The B. dorsalis complex is a large group composed of 85 species [14,16,20], of which five are polyphagous fruit pests (Figure 1). Recently, B. philippinensis Drew and Hancock was declared a synonym of B. papayae Drew and Hancock [16], and the latter was in turn, along with B. invadens, declared a synonym of B. dorsalis [21]. This regrouping has greatly increased the geographic range of B. dorsalis. Two of the most destructive species in the complex (B. dorsalis and B. carambolae) have invaded and become established in the Pacific region, Africa, South America, and debatably in California [22,23] (Figure 1). Bactrocera cucurbitae is primarily a pest of cucurbits, and females can infest unripe fruit and flowers. It is also a pest of papaya and infrequently infests other non-cucurbit hosts as well. It is native to Southeast Asia, and was introduced into Africa and parts of Oceania (Figure 2). The B. tryoni complex is composed of four very closely related species. While Queensland fruit fly (B. tryoni) and the lesser Queensland fruit fly (B. neohumeralis (Hardy)), both sympatric, are genetically indistinguishable, yet reproductively isolated by time of mating (dusk for the former and day time for the latter), B. aquilonis (May) and B. melas (Perkins & May) may be conspecific variants of B. tryoni [24]. In the early 1970s, B. tryoni was introduced and became established in New Caledonia and French Polynesia (Figure 3). Insects 2015, 6 300 Table 1. List of pest species of Bactrocera, ranked by category of severity. Species Hosts Distribution CATEGORY A pests B. carambolae Drew & Hancock Polyphagous fruit pest Vietnam to Indonesia. Introduced into South America. B. correcta (Bezzi) Polyphagous fruit pest Pakistan to Vietnam. Primarily Cucurbitaceae B. cucurbitae (Coquillett) Tropical Asia (widespread). Introduced into Africa and Oceania. (fruit & flower) B. dorsalis (Hendel) Polyphagous fruit pest Tropical Asia (widespread). Introduced into Africa and Oceania. Pakistan to Taiwan; south to Sulawesi. Introduced into Hawaii B. latifrons (Hendel) Mainly Solanaceae and Africa. B. neohumeralis (Hardy) Polyphagous fruit pest Australia, New Guinea. Africa. Introduced into southern Europe, the Middle East B. oleae (Gmelin) Olive and California. B. tryoni (Froggatt) Polyphagous fruit pest Australia. Introduced in Oceania. B. zonata (Saunders) Polyphagous fruit pest India to Vietnam. CATEGORY B pests B. aquilonis (May) Polyphagous fruit pest Australia. May be conspecific with B. tryoni. B. caryeae (Kapoor) Oligophagous fruit pest Southern India. B. cucumis (French) Cucurbitaceae (fruit) Australia. B. curvipennis (Froggatt) Polyphagous fruit pest New Caledonia. B. facialis (Coquillett) Polyphagous fruit pest Tonga. Australia, Micronesia (except Marianas), New Guinea, Solomon B. frauenfeldi (Schiner) Polyphagous fruit pest Islands. B. jarvisi (Tryon) Polyphagous fruit pest Australia. B. kandiensis Drew & Hancock Oligophagous fruit pest Sri Lanka. French Polynesia, Fiji (Rotuma), Niue, Samoa (American & B. kirki (Froggatt) Polyphagous fruit pest Western), Tonga. B. kraussi (Hardy) Polyphagous fruit pest Australia. B. melanotus (Coquillett) Polyphagous fruit pest Cook Islands. B. minax (Enderlein) Citrus Bhutan, China, Nepal. B. musae (Tryon) Banana Australia, New Guinea. B. occipitalis (Bezzi) Oligophagous fruit pest Kalimantan, Philippines. B. passiflorae (Froggatt) Polyphagous fruit pest Fiji, Wallis & Futuna, Niue. B. psidii (Froggatt) Polyphagous fruit pest New Caledonia. B. tau (Walker) Cucurbitaceae (fruit) Pakistan to Philippines; south to Sumatra & Sulawesi. B. trilineola Drew Polyphagous fruit pest Vanuatu. B. tsuneonis (Miyake) Citrus China, Japan. Cook Islands, Fiji, French Polynesia (Austral group), Niue, B. xanthodes (Broun) Polyphagous fruit pest Samoa (American & Western), Tonga, Wallis & Futuna. CATEGORY C pests B. albistrigata (deMeijere) Oligophagous fruit pest Indonesia, Malaysia B. atrisetosa (Perkins) Cucurbitaceae (fruit) New Guinea. B. bryoniae (Tryon) Banana, chili pepper Australia, New Guinea. B. caudata (Fabricius) Cucurbitaceae (flowers) India to Taiwan; south to Indonesia (Lesser Sundas). B. decipiens (Drew) Cucurbitaceae (fruit) New Guinea. Insects 2015, 6 301 Table 1. Cont. Species Hosts Distribution CATEGORY C pests B. depressa (Shiraki) Cucurbitaceae (fruit) Japan, South Korea, Taiwan. B. distincta (Malloch) Sapotaceae Fiji, Samoa (American & Western), Tonga, Wallis Is. B. diversa (Coquillett) Cucurbitaceae (flowers) Pakistan to Vietnam. B. halfordiae (Tryon) Oligophagous fruit pest Australia. B. melas (Perkins & May) Polyphagous fruit pest Australia. May be conspecific with B. tryoni. B. moluccensis (Perkins) Inocarpus fagifer Java to New Guinea, Solomon Islands. B. obliqua (Malloch) Guava, Syzygium New Guinea. B. passiflorae (sp. nr.) Oligophagous fruit pest Fiji, Tokelau, Tonga (Niuas Group), Tuvalu. B. pyrifoliae Drew & Hancock Guava, peach, pear Thailand, Vietnam. (Member of B. dorsalis complex). B. scutellaris (Bezzi) Cucurbitaceae (flowers) India to Vietnam; south to peninsular Malaysia. B. scutellata (Hendel) Cucurbitaceae (flowers) Bhutan to Vietnam; north to Taiwan & Japan (Ryukus). B. strigifinis (Walker) Cucurbitaceae (flowers) Australia, New Guinea. B. triangularis (Drew) Cucurbitaceae (flowers) New Guinea. B. trivialis (Drew) Oligophagous fruit pest New Guinea. (Member of B. dorsalis complex). B. tuberculata (Bezzi) Oligophagous fruit pest Bangladesh to Vietnam. Widespread from southern Thailand through New Guinea to B. umbrosa (Fabricius) Breadfruit, jackfruit New Caledonia. CATEGORY D pests B. arecae (Fabricius) Betel nut Malaysia (Peninsular), Singapore, Thailand. B. atramentata (Hering) Pometia pinnata New Guinea. B. bancroftii (Tryon) Mulberry Australia. B. expandens (Walker) Mangosteen Australia, Indonesia (Moluccas), New Guinea. B. hastigerina (Hardy) Spondias New Guinea, Solomon Islands. B. hochii (Zia) Luffa cylindrica (fruit) Bangladesh to Vietnam; south to Sumatra. B. lineata (Perkins) Pometia pinnata New Guinea. B. mesomelas (Bezzi) Guava Africa. B. mucronis (Drew) Guava, sweetsop New Caledonia. B. munda (Bezzi) Squash (fruit) Philippines, Taiwan. B. murrayi (Perkins) Mango, Surinam cherry Australia, New Guinea. B. mutabilis (May) Guava, kumquat Australia. B. nigrofemoralis White & Tsuruta Pomelo, mamey sapote Indian subcontinent, including Sri Lanka. B. nigrotibialis (Perkins) Guava, rose-apple India to Vietnam; south to Indonesia (Lesser Sundas). B. ochroma Drew & Romig Mango Indonesia. B. perfusca (Aubertin) Mango, rose-apple French Polynesia (Marquesas only). B. pruniae Drew & Romig Peach Vietnam. B. quadrisetosa (Bezzi) Pometia pinnata Solomon Islands, Vanuatu. B. speculifera (Walker) Breadfruit New Guinea. B. tapervitta Mahmood Luffa cylindrica (fruit) Philippines. B. trichosanthes Drew & Romig Bittergourd (fruit) Indonesia (Java), Malaysia (Peninsular & East), Thailand. B. trimaculata (Hardy & Adachi) Bittergourd (fruit) Philippines. B. versicolor (Bezzi) Sapodilla India, Sri Lanka. Insects 2015, 6 302 Figure 1. Distribution and invasion history of species in the Oriental fruit fly (Bactrocera dorsalis) complex. Insects 2015, 6 303 Figure 2. Distribution and invasion history of melon fly (Bactrocera cucurbitae). Insects 2015, 6 304 Figure 3. Distribution and invasion history of species in the Queensland fruit fly (Bactrocera tryoni) complex. Insects 2015, 6 305 Figure 4. Distribution of Category B pest species in the genus Bactrocera. Insects 2015, 6 306 3. Area-Wide Control Technologies Various technologies have been developed for area-wide control of Bactrocera fruit flies and related species throughout Asia and the Pacific. These include: (1) Insecticide-based suppression tools including cover sprays [25], protein bait sprays [2,26–29] and soil drenches [30–32]; (2) Male annihilation [33–36]; (3) Sterile insect releases [37–39]; (4) Releases of natural enemies [40,41]; and (5) cultural controls [9,42,43]. When used alone, however, these tactics do not constitute, by definition, Integrated Pest Management. 3.1. Insecticide Cover Sprays, Protein Bait Sprays, and Soil Drenches The history of fruit fly control with full cover sprays started with inorganic insecticides (e.g., lead arsenate) in the early 1900s and spanned the century with a transition to synthetic insecticides, such as chlorinated hydrocarbons, organophosphates, and synthetic pyrethroids. Advantages of insecticide cover sprays are that they are affordable, convenient and provide a high level of protection against fruit fly infestation with consistent results [42]. Addition of protein food baits to insecticide sprays reduced the amount of pesticide needed for fruit fly control and has been used successfully in many eradication programs [25,26,44]. Female flies, in need of protein for full ovarian development and egg production, readily feed on a protein source containing a toxicant. Enzymatic protein hydrolysate baits were first used in Hawaii for control of B. dorsalis, and malathion became the organophosphate insecticide additive of choice due to its low mammalian toxicity, affordable price, and low levels of fruit fly resistance [25,45]. In the 1960s, one particular formulation for ground, aerial and quarantine applications was adopted and remains a common standard today for control of many fruit fly species. It consists of three to four parts Nu-Lure® Insect Bait (Miller Chemical and Fertilizer Corporation, Hanover, PA, USA) plus one part malathion [26]. Because organophosphate insecticides have been implicated in negative effects on natural enemies and human health, alternatives have been sought during the twenty first century. The Regional Fruit Fly Project in the Pacific introduced the more rain-fast fipronil-based Bactrogel formulation, mixed with a protein as a bait spray for use against Bactrocera fruit flies in Pacific Island Countries and Territories [9,10]. In the late 1990s, a new bait spray formulation containing the reduced-risk biopesticide spinosad was shown to be as effective as Nulure-malathion bait sprays for use in Central America and the USA against Ceratitis capitata (Wiedemann) [27,46]. According to the United States Environmental Protection Agency (EPA), biopesticides are “certain types of pesticides derived from such natural materials as animals, plants, bacteria, and certain minerals”. Research is also underway to incorporate plant essential oils into protein baits [47]. Spinosad, a toxin derived from a soil-dwelling actinomycete bacterium (Saccharopolyspora spinosa Mertz & Yao), has low mammalian toxicity and reduced environmental impact on natural enemies [48]. A spinosad-based hydrolysed protein bait that attracted, induced feeding and killed fruit flies was initially developed by Moreno and Mangan [49]. Later it became known as GF-120 Fruit Fly Bait (Dow AgroSciences, Indianapolis, IN) [40,50]. Traditionally, B. cucurbitae has been controlled in agricultural areas of Hawaii by using protein bait sprays on border crops [51]. GF-120 was tested and