SPearoceedingssonal abundance of the H awaiianof fruit E flientomologicals in Banglade Societysh (2019) 51(2):25–37 25

Seasonal Abundance of Economically Important Fruit (Diptera: : Dacinae) in Bangladesh, in Relation to Abiotic Factors and Host Plants

M. Aftab Hossain1, Luc Leblanc2, Mahfuza Momen1, M. Abdul Bari1, and Shakil Ahmed Khan1 1Insect Biotechnology Division, Institute of Food and Radiation Biology, Bangladesh Atomic Energy Commission, Dhaka-1349, Bangladesh. 2Department of Entomology, Plant Pathology and Nema­tology, University of Idaho, 875 Perimeter Drive, MS2329, Moscow, Idaho, 83844-2329, USA.

Abstract. Fruit monitoring traps baited with male lures (cue lure, methyl eugenol, zingerone) were maintained for two years (Nov 2016–Oct 2018) at ten sites (reduced to three on year two), in village-style subsistence agriculture envi- ronments, at the Atomic Energy Research Establishment campus, Savar, Dhaka, Bangladesh. A total of 15 species and 135,034 flies were collected, dominated by polyphagous fruit pest dorsalis (58.0% of all trapped flies), cu- curbit pests cucurbitae (23.6%) and Z. tau (13.5%), and non-pest B. rubigina (3.6%). Three other pest species, collected in much smaller numbers, were polyphagous fruit pests B. zonata and B. correcta and cucurbit pest longicornis. Data was used to document the seasonal abundance of the above- mentioned species, in relation to host fruit availability and abiotic factors. Seasonal abundance of B. dorsalis, with peaks during wet summer months, was positively correlated with rainfall (r=0.70), temperature (r=0.66) and host availability (r=0.72). Seasonal trends in captures of B. zonata and B. rubigina were similar to those of B. dorsalis. Captures of Z. cucurbitae peaked in March 2017, early in the rainy season, and May 2018, in the middle of the rainy summer season, with no clear correlation with rainfall, humidity, or host availability. Captures of the two other cucurbit pests were inversely related to rainfall, with abundance peaks during the dry winter months. Data on seasonal abundance of these species will be utilized in formulating an area-wide pest management strategy in the agro-ecological system under consideration.

Key words: Bactrocera, Zeugodacus, Dacus, dorsalis, cucurbitae, tau, zonata, male lures, trapping

Introduction vegetables. As their larvae feed in the Fruit flies (Diptera: Tephritidae) are decaying fruit flesh, infested hosts quickly among the most serious pests on become rotten and inedible or drop to horticultural crops throughout the tropi- the ground prematurely, thus causing cal and subtropical regions (Aluja et al. considerable yield losses, between 30 1996, Armstrong and Jang 1997, Hasyim and 100% depending on the fruit species et al. 2008, Vargas et al. 2015). They lay and season (Dhillon et al. 2005). Besides eggs under the skin of fruits and fleshy causing billions of dollars in direct losses 26 Hossain et al. to a wide variety of fruit, vegetable, and vantages, such as pesticide residues and flower crops, they limit the development of the inability of the insecticides to pen- agriculture in many countries because of etrate infested fruits to kill larvae. More- strict trade quarantines imposed to prevent over, the public demand for insecticide- their spread (Heather and Hallman 2008). free fresh fruit has encouraged the use of All fruit flies in the tribe Dacini are fru- environmentally friendly methods of pest givorous or florivorous, and about 10% of control. Dacine fruit flies is a well-suited the 940 currently recognized species are group to demonstrate how pests can be ef- pests of commercial fruits and vegetables fectively controlled using minimal quanti- (Fletcher 1987, White and Elson-Harris ties of pesticide by integrating the use of 1992, Vargas et al. 2015, Doorenweerd male lures, female food-based attractants, et al. 2018). Fruit flies in the genera Bac- crop sanitation, augmentative releases of trocera, Zeugodacus, and Dacus are of parasitoids, and sterile insect releases into particular concern throughout much of the an area-wide control program, as was suc- Old-World tropics, where they constitute a cessfully implemented in Hawaii (Mau et significant threat to agricultural resources. al. 2007; Vargas et al. 2008, 2016). Before In Bangladesh, 13 pest and 16 non-pest a fruit fly management program can be species of dacine fruit flies have been re- designed for a specific agro-ecosystem, it corded, the most destructive of which are is necessary to generate baseline informa- the oriental fruit fly B.( dorsalis [Hendel]), tion on levels of fruit infestation and the melon fly (Z. cucurbitae [Coquillett]), seasonal incidence of the pest in relation to pumpkin fruit fly Z.( tau [Walker]), peach host availability and weather parameters. fruit fly B.( zonata [Saunders]), and the That information will help determine recently discovered carambola fruit fly B.( the appropriate methods of control and carambolae Drew & Hancock) (Leblanc timing of action (Laskar and Chatterjee et al. 2013, 2014a, 2019). Most of these 2010). Monitoring fruit fly populations species have been detected repeatedly in year-round is one of the first requirements survey traps in all the districts of Bangla- for compiling basic information needed desh, although B. carambolae, a recent to formulate an effective area wide IPM introduction to Bangladesh as evidenced program, towards sustainable agriculture by the genetic profile of the invasive popu- in Bangladesh. lation (C. Doorenweerd, pers. comm.), is Continuous population monitoring was still restricted to the southeastern portion initiated in Dhaka in 2016, as a prelude to of the country (Leblanc et al. 2019). Field the development of a pilot area-wide sup- research on dacine fruit flies in Bangla- pression project for Bangladesh in collabo- desh has mainly focused on fruit fly diver- ration with the FAO/IAEA Coordinated sity surveys (Leblanc et al. 2013, 2014b, Research Project D41027, “Simultaneous 2019); surveying their damage (Kabir et Application of SIT and MAT to Enhance al. 1991, Akhtaruzzaman et al. 1999a); Pest Bactrocera Management.” We are developing field control for cucurbit- presenting here the results of two full years infesting pest species (Chowdhury et al. of male lure trapping for seven species of 1993; Akhtaruzzaman et al. 1999b; Khan dacine fruit flies—cucurbit pestsZeugoda - et al. 2007a, b); and preliminary popula- cus cucurbitae, Z. tau, Dacus longicornis tion cycle monitoring (Alim et al. 2012, (Wiedemann); fruit pests B. dorsalis, B. Uddin et al. 2016). zonata, B. correcta (Bezzi); and non-pest Traditional control measures using B. rubigina—in relation to abiotic factors chemical insecticides have many disad- (daily temperature and rainfall) and host Seasonal abundance of fruit flies in Bangladesh 27 fruit availability, to help improve manage- Establishment (AERE) Campus (N 23.954 ment of these fruit fly species. E 90.280), Savar, Dhaka, a 263.5-acre ex- perimental area comprised of agricultural Materials and Methods land, dendrarium, and concrete buildings The study was conducted over two full (Fig. 1a). A diversity of fruit trees (mango, years (October 2016 to October 2018) at guava, banana, starfruit, citrus, sapodilla, the Bangladesh Atomic Energy Research etc.) and vegetables (including cucurbita-

Figure 1. A: Fruit fly trapping sites maintained at the Atomic Energy Research Estab- lishment compound in Bangladesh in 2016–2017 (sites 1 to 10) and 2017–2018 (sites 1, 8, 9). B: Mean monthly rainfall and minimum and maximum temperature recorded in Dhaka, Bangladesh, during the study period. 28 Hossain et al. ceous and solanaceous hosts) are grown weekly and counted and identified at the in village-style small gardens, rather than fruit fly research laboratory of AERE’s as commercial orchards and large gardens, Insect Biotechnology Division, Institute of which is typical of subsistence fruit and Food and Radiation Biology. Specimens fleshy vegetable production across much requiring further species confirmation of Bangladesh. The AERE campus was were sent, preserved in 95% ethanol, to selected because of easy access, and all taxonomist co-author LL (University of major cultivated fruit and vegetable crops Idaho). Information on the monthly avail- grown in Bangladesh were represented ability of host plants at the fruiting stage, and commonly infested with fruit flies. recorded during year 1 of the study, was Starting October 16, 2016, three traps provided by Dr. Md. Zainul Abedin, a baited with male lures (cue-lure, methyl retired AERE scientist in charge of the eugenol, and zingerone) were maintained station dendrarium. Daily temperature and in trees, 1.8 m above the ground and about rainfall data for Dhaka were provided by 10 m apart, at each of 10 sites throughout the Bangladesh Meteorological Depart- the AERE campus (Fig. 1a). The number ment, Agargaon, Dhaka 1207, Bangladesh. of sites was reduced to three during the Weekly trap capture data was recorded second year of monitoring (December on a Microsoft Excel spreadsheet, and 6, 2017 to October 31, 2018). Traps were numbers of captured flies for each species built out of 120 ml polypropylene contain- were divided by the actual number of days ers (Globe Scientific 5915 Polypropylene past the previous trap servicing, to gener- Specimen Container), with two 2-cm di- ate standardized flies-per-trap-per-day ameter circular lateral holes for fly entry, (FTD) data used for analysis. For each drilled just below the lid threading. For species, mean (and SE) monthly FTD was cue-lure and methyl eugenol traps, a com- calculated using all weekly FTDs for all (3 mercially available lure plug containing or 10) traps. Likewise, mean daily rainfall 2 g of lure (Scentry Biologicals, Billings, and temperature were calculated based on Montana, USA) and a 10x15-mm strip the actual day intervals used to generate containing 10% dichlorvos (2,2–dichlo- monthly FTD data. Fruit fly population rovynil dimethyl phosphate) (Vaportape® fluctuations in relation to abiotic factors II, Hercon Environmental, Emingsville, (rainfall, temperature) (Fig. 1b) and host Pennsylvania, USA) were suspended fruit availability (number of fruiting from the trap’s ceiling with a hook made host species available each month) were of tie wire. For zingerone-baited traps, analyzed using the Pearson correlation the plug was replaced by a 15-mm long coefficient (Table 1), based on FTD data cotton dental wick dipped in zingerone for the three trapping sites continuously (vanillylacetone) (Sigma-Aldrich, St. monitored over the two years. Louis, Missouri, USA) melted in a beaker over a hotplate and left to solidify in the Results and discussion wick. To protect captured flies from ant A total of 15 species and 135,034 flies attack, Tangle-Trap adhesive (Tanglefoot were collected during the two years of Company, Grand Rapids, Michigan, USA) trapping. The four dominant species were was smeared on the wire holding the polyphagous fruit pest B. dorsalis (58.0 % traps. Plastic plates (15 cm diameter) were of all trapped flies), followed by cucurbit placed over traps to prevent trap flooding pests Z. cucurbitae (23.6%) and Z. tau by frequent rain. (13.5%), and non-pest B. rubigina (3.6%). Trapped dead flies were collected Three other pest species, collected in Seasonal abundance of fruit flies in Bangladesh 29 Table 1. Correlation (Pearson) between monthly captures of seven species of fruit flies and mean monthly rainfall, temperature, and number of known hosts available at the fruiting stage for each fly species. Rainfall Temperature Hosts Year: 1–2 1 2 1–2 1 2 1 Fly species Bactrocera dorsalis 0.70 0.89 0.47 0.66 0.63 0.72 0.72 zonata 0.46 0.06 0.72 0.22 0.39 0.23 0.37 rubigina 0.52 0.47 0.80 0.31 0.44 0.39 No data correcta –0.29 –0.59 –0.09 –0.27 –0.78 0.10 –0.57 Zeugodacus cucurbitae 0.11 –0.44 0.68 –0.22 –0.55 0.05 –0.30 tau –0.39 –0.68 0.02 –0.64 –0.89 –0.48 –0.68 Dacus longicornis –0.38 –0.37 –0.52 –0.32 –0.35 –0.35 0.19 much smaller numbers, were polyphagous driver of seasonal abundance of fruit flies fruit pests B. zonata (650 specimens) and (Drew and Hooper 1983; Vargas et al. B. correcta (89 specimens) and cucurbit 1983a, b; Drew et al. 1984; Leblanc et al. pest D. longicornis (532 specimens). Other 2014a). species collected in small numbers and Seasonal abundance was positively not included on graphs were B. nigrifacia correlated with rainfall, temperature, Zhang, Chi & Chen (203 specimens), Z. and host availability for most of the fruit- diversus (Coquillett) (176), B. abbreviata infesting species, and especially for B. (Hardy) (62), B. digressa Radhakrishnan dorsalis (Figs. 2–3, Table 1). The very (46), B. syzygii White & Tsuruta (16), B. high captures of B. dorsalis in methyl nigrofemoralis White & Tsuruta (11), B. eugenol traps at AERE and its consis- propinqua (Hardy & Adachi) (5), and B. tent peaks of abundance during the wet tuberculata (Bezzi) (3). season or summer months (Fig. 2a) were Seasonal host fruit availability, docu- consistent with those documented in mented during the first year of trapping, studies in Chapai Nawabganj, Bangladesh showed that a diversity of host fruits and (Uddin et al. 2016), Hawaii (Vargas et al. vegetables were commonly available at 1983b, 1989, 1990; Leblanc et al. 2014a), the fruiting stage throughout the year at Kunming, China (Ye and Liu 2005), and AERE (Figs. 2–5). Although not quanti- India (Gupta and Bhatia 2000). By May fied, fruits from cultivated trees were in Bangladesh, most of the gutti (non- available in largest quantities during the grafted plant) varieties had matured, in hot rainy season (May–August) and and fly populations started increasing. rather scarce during the cooler, drier Between June and August, at the peak of season (November–February). Likewise, the monsoon season, most of the mangoes wild hosts were mainly observed fruiting and guavas, major hosts to oriental fruit during the hot summer months. Host fruit fly, were ready to harvest, and flies were availability is well known to be the main correspondingly most abundant. Past that 30 Hossain et al.

Figure 2. Distribution and mean monthly trap captures of Bactrocera dorsalis (A) and B. zonata (B), in relation with abiotic factors and host fruit availability. peak, populations declined slowly and zonata at AERE were similar to those of remained low until May the following B. dorsalis, with slightly earlier peaks in year. Although trapped in much lower the wet season (Fig. 2b) and strongly cor- numbers, seasonal trends in captures of B. related with rain in year 2 (Table 1), again Seasonal abundance of fruit flies in Bangladesh 31

Figure 3. Distribution and mean monthly trap captures of Bactrocera rubigina (A) and B. correcta (B), in relation with abiotic factors. within the main period of availability of et al. 2011, Draz et al. 2016). Seasonal two of its prime hosts: guava and mango. peaks in abundance were also positively These are consistent with seasonal trends correlated with rainfall and temperature documented, under higher population for B. rubigina (Fig. 3a), a non-pest first levels, in Bangladesh (Hossain et al. 2017), recorded in 2013 in Bangladesh (Leblanc India (Agarwal et al. 1999), Pakistan et al. 2013). Despite being widespread and (Mahmood et al. 2002), and Egypt (Ali common in Bangladesh and throughout 32 Hossain et al. tropical Asia, its main host plant, likely cies at AERE may be driven by a locally different from the less widespread Litsea dominant cucurbit host, possibly pumpkin verticillata host recorded in China (Liang (Cucurbita maxima) for Z. tau (Fig. 4b) et al. 1993), has yet to be determined. We and Luffa gourds for D. longicornis (Fig. suspect it may breed on flowers of Melas- 5). Systematic host fruit surveys will be tomataceae, as do two very closely related required to confirm this hypothesis. species (Leblanc et al. 2015). Bactrocera In Bangladesh, calendar pesticide correcta is a much less common pest sprays, routinely used on crops to control species in Bangladesh, reported for the fruit fly infestations, have been implicated first time in 2014 (Leblanc et al. 2014a), in the reduction of natural enemies and, and associated with localized patches of in some cases, secondary pest outbreaks. cultivated host fruit such as mango, guava, In addition, many pesticides used on non- and sapodilla (Kapoor 1993). Its numbers traditional specialty fruit crops are not in traps were not high enough to infer on registered for such specific use. Abuse seasonal abundance (Fig. 3b) or interpret and misuse of pesticides have renewed the apparently negative correlations to all concerns regarding food safety and factors (Table 1), but it likely peaks during groundwater quality in many parts of the the summer months in areas where it is world. Because of the complexity of agro- more common. ecosystems in Bangladesh and the pest With fruiting cucurbit hosts available complexes that can occur on each crop, throughout the year, captures of Z. cucur- area-wide pest management (AWPM) bitae, the second most abundant species at approaches to fruit fly suppression are AERE, peaked in March 2017, early in the proposed as an alternative to the current rainy season, and May 2018, in the middle practices. AWPM is a long-term campaign of the rainy summer season (Fig. 4a). Both against a pest population throughout a years, populations declined during the sizeable geographic area, with the objec- tail end of the rainy season. Because of tive of reducing it to a non-economic the marked difference in abundance peak status (Lindquist 2000). For fruit flies, seasons, we could not detect a clear cor- it integrates available pest control tech- relation with abiotic factors or host avail- nologies—field sanitation, protein bait ability. Nonetheless, summer population application techniques as sprays or in peaks for melon fly were largely consistent traps, male annihilation techniques using with those reported in literature in Hawaii male lures, and sterile fly and parasitoid (Harris et al. 1986; Vargas et al. 1989, releases—into a comprehensive manage- 1990; Leblanc et al. 2014a), West Bengal, ment package that can be economically India (Laskar and Chatterjee 2010), and viable, environmentally safe, and sustain- Bangladesh (Alim et al. 2012). able (Vargas et al. 2008, 2016). Captures of the two other cucurbit- Pest management programs using eco- infesting species, Z. tau (Fig. 4b) and D. friendly methods have been proposed for longicornis (Fig. 5), on the other hand, Bangladesh on many occasions. However, were inversely related to rainfall and tem- demonstration of SIT releases against perature (Table 1), with abundance peaks blowfly conducted in Cox’s Bazar in the during the dry and cooler winter months. early 2000s (Islam et al. 2017) identified Higher captures of Z. tau in December and several problems associated with the its scarcity during rainy months at AERE control technology available at that time. contradict findings in Sumatra by Hasyim These included the high economic cost of et al. (2008). Abundance of these spe- large-area programs, insufficient informa- Seasonal abundance of fruit flies in Bangladesh 33

Figure 4. Distribution and mean monthly trap captures of Zeugodacus cucurbitae (A) and Z. tau (B), in relation with abiotic factors and host fruit availability. tion on the effects upon non-target fauna, AWPM for Bangladesh will require a environmental concerns, quarantine is- continuous application of control mea- sues, and the lack of a large-scale sterile sures over a large area, barriers to prevent fly-rearing facility. Successful fruit fly immigration of flies from surrounding 34 Hossain et al.

Figure 5. Distribution and mean monthly trap captures of Dacus longicornis, in rela- tion with abiotic factors and host fruit availability. areas (Cohen and Yuval 2000), strict crop monitor population cycles and the impact sanitation, and effective grower educa- of control measures, regular sampling of tion (Mau et al. 2017). It is best suited for fruit, starting before control is initiated, large-scale commercial farmers who can will be required to generate baseline data invest labor and resources for pest control. on levels of infestation and economic Although scientists in Bangladesh have losses and document the actual impact of developed most of the technologies over the area-wide control pilot exercise. Along the years to combat accidental fruit fly with melon fly, oriental fruit fly should outbreaks, the technologies were never also be targeted in the exercise through packaged and transferred to Bangladeshi male annihilation, female food attractants, farmers. The current pilot program, under crop sanitation, and fruit bagging. Over care of AERE, is designed to demonstrate the long term, these technologies can that area-wide control targeting multiple be transferred, in collaboration with the species can be achieved on the AERE Bangladesh Department of Agricultural compound. Mass rearing of melon fly Extension, to Bangladesh farmers and and its parasitoid Psyttalia fletcheri inhabitants, focusing on such relatively (Silvestri) (Hymenoptera: Braconidae) low-cost options as crop sanitation, male is being developed at AERE for sterile annihilation, and fruit bagging. It will pro- fly and augmentative parasitoid releases. mote the production of a greater diversity These will be most effective if the overall of higher-quality crops while reducing the population is first reduced, through male use of organophosphate and carbamate annihilation and crop sanitation, and insecticides, thus balancing the ecological, releases are initiated during periods of social, and economic aspects of farming lowest fly populations, which are deter- in a move toward sustainability for local mined by monitoring through trapping. consumption and possible niche export Although trapping is a convenient tool to markets. Seasonal abundance of fruit flies in Bangladesh 35 Acknowledgments man. 2012. Seasonal variations of melon The authors are grateful to Mr. Mozi- fly, Bactrocera cucurbitae (Coquillett) bor Rahman, Bangladesh Meteorological (Diptera: Tephritidae) in different agricul- Department, Agargaon, Dhaka 1207, for tural habitats of Bangladesh. ARPN J. Agric. Biol. Sci. 7: 905–911. providing daily temperature and rainfall Aluja M., H. Celedonio-Hurtado, P. Liedo, data. Field research was funded by the M. Cabrera, F. Castillo, J.Guillen, and E. Bangladesh Atomic Energy Commission Rios. 1996. Seasonal population fluctuations (BAEC). We greatly appreciate the help and ecological implications for manage- of Mr. Abdus Salam and Mr. Hamidur ment of Anastrepha fruit flies (Diptera: Rahman in trap servicing. Funding for Tephritidae) in commercial mango orchards author LL’s travel to Bangladesh and in southern Mexico. Environ. Entomol. 89: publication charges was provided by the 654–667. Armstrong, J.W. and E.B. Jang. 1997. An United States Department of Agriculture overview of present and future fruit fly (USDA) Farm Bill Section 10007 Plant research in Hawaii and U.S. mainland. Pest and Disease Management and Di- Aust. Centre. Intl. Agric. Res. 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