Insect infestation can adversely affect tomato (Solanum lycopersicum L.; Solanaceae) development and yield. Fruit flies (Diptera: Tephritidae) are a serious pest of tomato, and are spreading to areas where they were not previously found. This study was undertaken to determine if tephritid fruit flies were present, which species were most abundant, how tomato cultivars responded, and what amount of damage occurred in the Eastern Himalayas of India during May 2014 and 2015. Mature and ripe fruit (n = 20) per cultivar were picked at random from 12 cultivars at weekly intervals to assess percentage of infestation, fly species composition, larval infestation, pupal mortality, adult emergence, and sex ratio during 2 seasons. Seasonal fluctuation of male adults of Zeugodacus tau (Walker) (Diptera: Tephritidae) in tomato was studied by installing 3 modified clear traps, made from plastic bottles, that were baited with 0.5 mL Cue-lure and the insecticide dichlorovos 76% EC (Nuvan®). Survey and subsequent identification confirmed the presence of Z. tau in tomato in the Himalayas of India. This is the first report of the insect in the province, and of population outbreaks resulting in serious damage to tomato in India. Among fruit fly species present on tomato, Z. tau was more abundant (71.4–96.4%) in all geographical regions of Mizoram, India, than were Bactrocera correcta (Bezzi), B. dorsalis (Hendel), and B. latifrons (Hendel), which ranged from 3.6 to 28.6%. The highest percentage of infestation was in Champhai (72.7 ± 6.7%) and Kolasib (80.7 ± 3.5%) and the lowest in Mamit (14.7 ± 4.8%) and Serchhip (19.3 ± 4.7%). Cultivar influenced pupal mortality and adult emergence of Z. tau. Seasonal fluctuation of Z. tau males on tomato varied; the greatest numbers were trapped during May and Dec. Occurrence of Z. tau at high population densities was associated with high levels of damage and could lead to high economic losses in tomato fruit production.
The Eastern Himalayas of India is unique in its agro-ecosystems, and consequently the insect pest problems are also distinct from the rest of the country. Pest problems in the region are innumerable and as many as 6,000 species of insects have assumed pest status on various crops over the decades (Boopathi et al. 2014). Tomato, Solanum lycopersicum L. (Solanaceae), is one of the most important vegetable crops in the Eastern Himalayas of India. In tomato, pests are the main limiting factor in production. Fruit flies (Diptera: Tephritidae) reduce tomato quality and cause abortion of infested fruit (Gupta et al. 1990; Boopathi et al. 2013a). Losses caused by fruit flies vary between 30 and 100% depending on the season (Hasyim et al. 2004; Dhillon et al. 2005; Boopathi 2013; Boopathi et al. 2013b). Fruit flies damage tomato fruit by laying eggs under the skin. The larvae that hatch from these eggs feed in the decaying flesh. Infested fruit become rotten and inedible, or abort, causing considerable loss in production (Boopathi 2013).
Fruit flies in the taxon Zeugodacus (= Bactrocera) tau (Walker) (formerly Dacus tau) are widespread in Asia and Australia (Drew & Hancock 2000; De Meyer et al. 2015). Several Bactrocera species are serious pests of vegetables (Allwood et al. 1999; Boopathi 2013; Boopathi et al. 2013a,b). Although these flies commonly attack fruit of species within the Cucurbitaceae, they also infest fruit of species from the following families: Leguminoseae (Phaseolus vulgaris L.), Moraceae (Ficus racemosa L.), Myrtaceae (Psidium guajava L.), Oleaceae [Myxopyrum smilacifolium (Wallich) Blume], and Sapotaceae [Manilkara zapota (L.) P. Royen] (Allwood et al. 1999; Boopathi et al. 2013a). Adult females prefer to lay eggs in soft fruit by piercing with their ovipositor.
Understanding fruit fly diversity, seasonal fluctuation of fruit fly populations, infestation level, species composition, and damage to fruit may contribute to improved management of the pest. This study was undertaken to assess seasonal fluctuation of Z. tau male adults in tomato, assess the level of infestation, and determine the species composition in 8 geographical regions of Mizoram (India) and in different tomato cultivars.
Materials and Methods
DIVERSITY OF TEPHRITID FRUIT FLIES IN TOMATO IN MIZORAM, INDIA
Tomato fruit samples were taken from 8 geographical regions in Mizoram, India (Table 1) during May of 2014 and 2015. Mizoram is located in the extreme southern part of the Eastern Himalayas of India, bordering Myanmar in the east and south, and Bangladesh in the west. Fifty mature and ripe fruits per region were picked at random to assess the level of infestation (%) by fruit flies and species composition in each region. Emerging flies were collected and sent to Dr. S. Ramani, University of Agricultural Sciences, GKVK, Bengaluru, Karnataka, India, for identification.
Location and altitude of tomato fruit sampled for fruit fly infestation and diversity in 8 geographical regions of Mizoram, India during 2014 and 2015.
A study was undertaken to determine percentage of infestation, larval infestation, biology, and species composition in tomato cultivars, in order to assess seasonal fluctuation of Z. tau male adults in tomato. The study was done at the research farm of ICAR Research Complex for NEH Region, Mizoram Centre, Kolasib, Mizoram, India, from May to Jun 2014 (season 1) and Nov 2014 to Jan 2015 (season 2). The research farm is located at 634.5 m above mean sea level at 24.12°N and 92.40°E, and has a mild-tropical climate. Cultivars of tomato were produced on raised beds, 1.5 × 1.0 m, in greenhouses. At 25 d after sowing, seedlings were transplanted at a spacing of 60 × 60 cm. Each cultivar was replicated 3 times in a randomized complete block design. Weeding, application of manure and fertilizers, irrigation, and other cultural practices were followed as per crop production guidelines (TNAU 2012). No plant protection measures were applied throughout cropping seasons.
PERCENTAGE OF INFESTATION, SPECIES COMPOSITION, AND BIOLOGY OF FRUIT FLIES IN TOMATO
Percentage infestation by fruit flies was assessed by randomly sampling mature and ripe fruit (n = 20) from each cultivar at weekly intervals to assess fly species composition, larval infestation, pupal mortality, adult emergence, and sex ratio during seasons 1 and 2. Fruit were placed in separate buckets (30 × 15 × 15 cm), each containing a slightly moist, finely sieved sand layer to facilitate pupation of emerging larvae (Vayssières et al. 2007). Fruit were observed weekly until they dried. Pupae were removed by sifting the sand through a 12 mesh sieve. Pupae were counted and placed in containers with fresh sand inside insect cages (15 × 15 × 15 cm) for adult emergence. Larval infestation, pupal mortality, adult emergence, fruit fly abundance, and male-to-female sex ratio were determined from recovered puparia. Emerging flies were collected and sent to Dr. S. Ramani, University of Agricultural Sciences, GKVK, Bengaluru, Karnataka, India, for identification.
SEASONAL FLUCTUATION OF Z. TAU MALE ADULTS IN TOMATO
Three modified clear traps, made from plastic bottles (Steiner et al. 1965), were baited with 0.5 mL Cue-lure (Yasho Industries Pvt. Ltd., Mumbai, India) and the insecticide dichlorovos 76% EC (Nuvan®, Syngenta India Ltd., Mumbai, India). Cotton wicks were soaked in the mixture of lure and insecticide for 5 s and suspended in the trap from one end of a piece of string. The piece of string passed through the lid of the trap and was used to hang the trap on a bamboo stick. Care was taken to avoid contamination of the outer parts of the traps with the mixture. The traps were hung on the bamboo stick about 1.5 m above ground level and traps were spaced 25 m apart in tomato fields. Traps were collected weekly and the numbers of fruit flies in traps were counted; old traps and lures were replaced with new traps and lures.
Data were subjected to analysis of variance using SAS (SAS 2011). Effects of cultivar, season, and collection date on fruit fly abundance, and effects of season and collection date on the pattern of Z. tau male adults captured by Cue-lure-based traps were analyzed using 2-way ANOVA. If interactions were significant, they were used to explain the data; if interactions were not significant, means were separated using Tukey's HSD test.
DIVERSITY OF TEPHRITID FRUIT FLIES ON TOMATO IN MIZORAM, INDIA
Percentage of infestation of tomatoes by fruit flies in the 8 geographical regions of Mizoram, India, varied during 2014 (14.7–72.7%) and 2015 (19.3–80.7%) (Table 2). The highest infestation (± SE) was in Champahi (72.7 ± 6.8%) and Kolasib (80.7 ± 3.5%) during 2014 and 2015, respectively; the lowest infestation was in Mamit (14.7 ± 4.8%) and Serchhip (19.3 ± 4.7%) during 2014 and 2015, respectively. Among fruit fly species reared from fruit, Z. tau was the most abundant species in the fruit fly complex in all geographical regions (71.4–96.4%) (Table 2). Other species reared from fruit [B. correcta (Bezzi), B. dorsalis (Hendel), and B. latifrons (Hendel)] were less frequently encountered (3.6–28.6%) in the regions surveyed.
CHARACTERS USED TO DISTINGUISH ZEUGODACUS TAU
The following characters were used to distinguish Z. tau: a mediumsized species; abdominal terga III–IV fulvous with a black “T” pattern and anterolateral corners of terga IV and V with broad black markings; face fulvous with a pair of medium-sized circular to oval black spots; wings with a narrow dark fuscous costal band overlapping wing veins R2+3 and expanding into a distinct apical spot and broad dark fuscous cubital streak; cells bc and c colorless; microtrichia in outer corner of cell c only; postpronotal lobes and notopleura yellow; scutum black with large areas of red-brown centrally and anterocentrally; lateral and medial postsutural vittae present; yellow spot anterior to mesonotal suture in front of lateral postsutural vittae; mesopleural stripe reaching midway between anterior margin of notopleuron and anterior notapleural seta; scutellum entirely yellow.
PERCENTAGE OF INFESTATION BY FRUIT FLIES IN TOMATO CULTIVARS
Percentage of infestation by fruit flies did not vary with season although the infestation varied among cultivars (Table 3). The cultivar by season interaction was not significant. None of the cultivars were free from fruit fly infestation. Percentage of infestation by fruit flies varied in season 1 (15.0–83.3%) and season 2 (18.3–86.7%) among the cultivars (Table 4). The highest level of infestation was in cultivar Badshah during season 1 (83.3 ± 7.3%) and season 2 (86.7 ± 4.4%) and the lowest level of infestation was in cultivar 9005-Siri during season 1 (15.0 ± 7.6%) and season 2 (18.3 ± 6.0%).
Percentage of fruit fly infestation and diversity of fruit flies in tomato fruit in 8 geographical regions of Mizoram, India, during 2014 and 2015.
EFFECTS OF CULTIVAR AND SEASON ON BIOLOGY OF FRUIT FLIES IN TOMATO
Cultivar affected the numbers of puparia recovered, numbers of adults emerged, and numbers of males and females. The season by cultivar interaction affected the number of non-emerged puparia and percentage of adult emergence. The cultivar Badshah had the most fruit fly puparia per 20 fruit during season 1 (29.0 ± 7.6) and season 2 (30.0 ± 1.2) (Table 4). The fewest fruit fly puparia per 20 fruit were in cultivars Bhulaxmi (5.3 ± 2.9) and 9005-Siri (5.3 ± 1. 5) during season 1. In season 2, cultivar Nun-7610 had the fewest fruit fly puparia per 20 fruit (4.0 ± 0.6). The fewest non-emerged puparia were found in cultivar Emerald during season 1 (0.7 ± 0.3). In season 2, the fewest non-emerged puparia (0.3 ± 0.3) were found in cultivars Nun-7610 and JK Akshay. The most non-emerged fruit fly puparia were found in cultivars Nun-7610 (14.7 ± 3.7) and Badshah (9.0 ± 1.2) during seasons 1 and 2, respectively (Table 4).
Adult emergence varied considerably among cultivars and seasons, with cultivars Emerald (93.1 ± 3.7%) and JK Akshay (97.4 ± 2.6%) exhibiting the highest percentage of adult emergence during seasons 1 and 2, respectively (Table 4). The lowest percentage of adult emergence was in cultivars Nun-7610 (24.2 ± 2.5%) and Arka Alok (42.4 ± 14.2%) during seasons 1 and 2, respectively. The greatest number of adults emerged in cultivar Badshah during seasons 1 (18.3 ± 2.9) and 2 (21.0 ± 2.3) (Table 4). The smallest number of adults emerged in cultivars 9005-Siri (2.0 ± 0.6) and Nun-7610 (3.7 ± 0.3) during seasons 1 and 2, respectively. The greatest numbers of males and females were found in cultivar Badshah during season 1 (9.0 ± 2.3 and 9.3 ± 1.7, respectively) and season 2 (9.0 ± 2.3 and 9.3 ± 1.7, respectively) (Table 4). The smallest numbers of males (1.3 ± 0.3) and females (0.7 ± 0.3) were found in cultivar 9005-Siri during season 1; in season 2, the smallest numbers of males (2.0 ± 0.0) and females (1.0 ± 0.6) were found in cultivars Nun-7610 and Pusa Rohini, respectively. The male-to-female sex ratio of Z. tau was lowest in cultivar Jessica (1:1.33) and highest in cultivar Bhulaxmi (1:0.33) in season 1 (Table 4). In season 2, the maleto-female sex ratio of Z. tau was lowest in cultivar Swaraksha (1:1.34) and highest in cultivar Pusa Rohini (1:0.39).
Analysis of variance values associated with analysis of cultivar and season influences on biology of fruit flies.
SPECIES COMPOSITION OF FRUIT FLIES IN TOMATO CULTIVARS
Among fruit fly species, Z. tau was the most common species in all cultivars (66.67–100.00%) (Table 5). The other species detected (B. correcta, B. dorsalis, or B. latifrons) occurred less frequently (0.0–33.3%). Cultivars Pusa Rohini, Emerald, Arka Alok, Nun-7610, Bhulaxmi, 9005-Siri, Badshah, Alankar, and Swaraksha were infested only by Z. tau. The cultivars Jessica, JK Akshay, and Chiranjeevi were infested by all 4 fruit fly species. Zeugodacus tau was found infesting 85.7% of fruit in cultivars Jessica and JK Akshay and 66.7% in cultivar Chiranjeevi. Percentage of infestation by other species was higher in cultivar Chiranjeevi (33.3%) and lower in cultivars Jessica and JK Akshay (14.3%).
SEASONAL FLUCTUATION OF Z. TAU MALE ADULTS DETECTED BY CUE-LURE-BASED TRAPS
Season (F = 108.4; df = 1; P < 0.001) and collection date (F = 31.3; df = 10; P < 0.001) affected the pattern of Z. tau males captured by Cue-lure-based traps (Table 6). The interaction of season and collection date also was statistically significant (F = 126.4; df = 10; P < 0.001). The seasonal fluctuation of Z. tau males captured in traps is shown in Fig. 1. The numbers of Z. tau males caught in Cue-lure-based traps ranged from 29.3 to 168.6 fruit flies per trap in season 1, and from 17.0 to 95.3 per trap in season 2. In season 1, numbers of Z. tau male (Fig. 1a) reached peak abundance on 8 May 2014 (168.7 ± 7.0), followed by a decline. The smallest number of Z. tau males caught was on 26 Jun 2014 (29.3 ± 5.6). In season 2, numbers of Z. tau males trapped (Fig. 1b) increased from mid-Nov, reaching a peak on 21 Dec 2014 (95.3 ± 4.9), and followed by a decline toward the end of Dec 2014. The smallest number of Z. tau males captured was on 16 Nov 2014 (17.0 ± 2.6).
Zeugodacus tau was found to infest all tomato cultivars evaluated. This is the first report of the insect in Mizoram, India. More importantly, this is a drastic shift in feeding behavior by Z. tau, changing from feeding on cucurbits to Solanaceae such as tomatoes. Zeugodacus tau always has been regarded primarily as a cucurbit feeder. Some tephritid species have genuinely wide host ranges, both because some apparent polyphagous “species” have proven to be an unrecognized species complex, and because host shifts undeniably occur. If host shifts occur far more frequently than host speciation, then the process is similar to the theory of island biogeography, where species richness of island communities is a balance between the rate at which new species colonize the island and existing species go extinct. Fruit fly host records signifying comparative host use might be useful for recognizing lineages, races, and species (cryptic or otherwise). This assumption is consistent with the generalization that different biological species have different host requirements and are correspondingly attracted to different host species.
Fruit flies can cause significant to total crop failure on tomato (José et al. 2013). Among fruit fly species present on tomato, Z. tau was more abundant in all geographical regions of Mizoram, India, than were other fruit fly species, i.e., B. correcta, B. dorsalis, or B. latifrons. This study clearly revealed the presence of Z. tau in Mizoram (India) and its environs, and shows that the pest is well distributed in all locations studied. The highest levels of infestation were in Champhai and Kolasib (Mizoram, India) during 2014 and 2015, respectively. The relative pest abundance of the flies at the different locations appeared to be influenced by the characteristics of the area where they are situated. Champhai is situated in denser forest than the other locations, and had the highest observed pest density. This finding was expected because of the high diversity of plants; hence, there are many hosts. This is consistent with the reports of Harris & Lee (1989) and Vargas et al. (1990), who suggested the distribution and abundance of various tropical tephritids was affected by availability of host fruits. Previously, Mwatawala et al. (2010) and De Meyer et al. (2015) reported that the cucurbit feeders Zeugodacus cucurbitae (Coquillett) and Dacus punctatifrons Karsch were serious pests of tomatoes in Cameroon.
The biology of tephritid fruit flies infesting tomato fruit, as affected by season and cultivar.
Species composition of fruit flies in tomato cultivars.
The infestation level was highest as fruit matured, and little or no infestation occurred in the earlier fruit stages. Most fruits became increasingly susceptible to fruit fly damage close to harvest. Mwatawala et al. (2006) also reported that fruit flies cause more severe damage to mature tomato fruit than to young fruit. Preventing fruit fly oviposition during fruit maturation is difficult because excessive insecticide residues on the fruit make them illegal to sell. Unfortunately, none of the cultivars were free from fruit fly infestation. Zeugodacus tau was the most common species in the complex in all cultivars, and is now considered a major insect pest of tomato in India because of its prevalence, rapid spread, and destructive nature (Boopathi et al. 2013a).
The pattern of Z. tau males captured by Cue-lure-based traps varied with season and collection date. The pattern is consistent with reports of Selvaraj et al. (2006) and Sithanatham et al. (2006), where fruit flies were caught during Apr and May, also a period of fruit formation. Similarly, Boopathi et al. (2013a) and Boopathi et al. (2013b) reported that most fruit flies were caught during Apr and May in chilli and guava crops. The effectiveness and efficiency of the traps shows their importance in surveillance and detection programs involving Z. tau.
Analysis of variance of effects of seasonal pattern of Zeugodacus tau male adults on tomato captured by Cue-lure-based traps.
Presence of fruit flies was confirmed on tomato, and the extent of loss varied depending on geographical region, cultivar and season. Zeugodacus tau was the most common species in the complex in all geographical regions and tomato cultivars. Occurrence of Z. tau at high population densities is associated with the highest level of damage, and could lead to high economic losses in tomato fruit production. The apparent drastic shift of feeding by Z. tau from cucurbits to tomato means that tomato growers will need to plan to monitor and manage this new pest.
The inventory was funded by the National Innovation on Climate Resilient Agriculture (NICRA), Indian Council of Agricultural Research, Pusa, New Delhi, India. We thank the Principal Investigator (NICRA), ICAR Research Complex for NEH Region, Umroi Road, Umiam, Meghalaya, for providing the facilities and support. We thank S. Ramani, University of Agricultural Sciences, GKVK, Bengaluru, Karnataka, India, for his help in the identification of fruit fly species.