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INTERNATIONAL JOURNAL OF PEST MANAGEMENT, 2000, 46(4) 257± 266
Leafminers in vegetables, ornamental plants and weeds in Indonesia: surveys of host crops, species composition and parasitoids (Keywords: leafminers, Indonesia, vegetables, ornamental plants, weeds, parasitoids, surveys)
AUNU RAUF² , B. MERLE SHEPARD*³ and MARSHALL W. JOHNSON§
² Department of P lant P ests and Diseases, F aculty of Agriculture, Bogor Agricultural University (IP B), Bogor 16144, Indonesia ³ Coastal R esearch and E ducation C enter, C lemson University, 2865 Savannah Highway, Charleston, SC 29414, USA §Department of E ntomology, University of Hawaii at Manoa, 3050 Maile Way, 310 Gilmore Hall, Honolulu, HI 96822, USA
Abstract. Extensive surveys of vegetable, ornamental and weedy plant species were conducted in highland and lowland vegetable production areas in Indonesia with the aim of recording leafminer species present and their associated natural enemies. The most common dipterous species reared from samples was the pea leafminer, Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae). This introduced pest was particularly serious in highland vegetables in Java, Sumatra and South Sulawesi, causing yield losses as high as 60 ± 70%. Another alien species, the vegetable leafminer, Liriomyza sativae Blanchard, contributed to problems in lowland areas on the north coast of West Java, where cucumbers were heavily damaged. An Asian leafminer species, Chromatomyia horticola Goureau, was more common in snow peas (Pisum sp.). Intensive sampling of leafminer-infested leaves from surveyed host plants yielded 11 species of hymenopteran parasitoids: 10 eulophids (Asecodes sp., Chrysocharis sp., Cirrospilus ambiguus (Hansson and LaSalle), Closterocerus sp., Hemiptarsenus varicornis (Girault), Neochrysocharis formosa (Westwood), Neochrysocharis sp., Pnigalio sp., Quadrastichussp., Zagrammosoma sp.) and 1 eucoilid (Gronotoma sp.). The most abundant parasitoid species was H. varicornis. Levels of parasitism varied among crops and growing seasons, but were usually low, especially on potato ( < 3%). Surveys revealed that most farmers (63%) attempted to control leafminers by applying insecticides twice weekly although these applications were neither effective nor economical according to responses of about 72% of the farmers. An integrated pest management approach is suggested that emphasizes IPM training for vegetable farmers and includes reduction or elimination of broad spectrum chemicals that would adversely affect parasitoids that may already be present as well as those that may be introduced. The initiation of a classica l biological control programme is recommended to enhance the limited parasitoid complex present in Indonesia and increase levels of biological control.
1. Introduction During the last 25 years, two agromyzid leafminer species, Liriomyza sativae Blanchard (the vegetable leafminer), and Liriomyza trifolli Burgess, were unintentionally introduced and established in numerous countries worldwide (Parrella, 1982; Waterhouse and Norris, 1987; Johnson, 1993; Weintraub and Horowitz, 1995). Within the last several years, the pea leafminer, Liriomyza huidobrensis (Blanchard), has become established in several countries including Israel (Weintraub and Horowitz,
1995) and Indonesia (Shepard et al., 1998). Following establishment, all these species frequently achieved significant pest status on vegetable and ornamental crops due to many factors including, but not limited to, use of ineffective insecticides and pesticide resistance (Parrella and Keil, 1984; Johnson, 1987; Mason et al., 1987), difficulties in delivering insecticide materials to the protected life stages (egg, larvae and pupae) (Parrella, 1987), and lack of effective natural enemies in new areas of infestation (Johnson, 1993). Of particular concern, but not well studied, is the potential of Liriomyza species to exploit new host plants that they might encounter in newly colonized habitats (Via, 1984, 1986; Carolina and Johnson, 1992), especially under conditions where their common host plants are rare or absent in the area. If successful, these species may not only utilize a new plant host but also find themselves in `enemy free’ space that their common natural enemies would not search even if present (Price et al., 1980; Price, 1981; Johnson and Hara, 1987; Gratton and Welter, 1999). The first documented infestation of L. huidobrensis in Indonesia was on potato in Cisarua, West Java in 1994 (Rauf, 1995; Shepard et al., 1998). Subsequently, the pest invaded other regions of Java, Sumatra and South Sulawesi. Yield losses due to this pest may reach 70% in several crops (e.g. potato and snap bean), and total crop losses can occur in potato (Shepard et al., 1998). Commonly grown vegetables in the lowlands include chillies, shallot, yard-long bean, cucumber, and eggplant; in the highlands, cabbage, broccoli, potato, shallot, tomato, carrot and snap bean are grown. The major highland vegetable production areas in Indonesia include Lembang, Pangalengan, Garut and Cipanas in West Java, Banjarnegara and Magelang in Central Java, Batu in East Java, Alahan Panjang in West Sumatra, Berastagi in North Sumatra, and Malino in South Sulawesi. Our paper reports on results of surveys to determine the relative importance and species composition of leafminers and their associated parasitoids in vegetable, ornamental and weedy plants in the major vegetable-growing areas of Indonesia. In
*To whom correspondence should be addressed. Fax: +1 843 571 4654; e-mail:
[email protected] International Journal of Pest Management ISSN 0967-0874 print/ISSN 1366-5863 online Ó 2000 Taylor & F rancis Ltd http://www.tandf.co.uk/journals
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addition, results of surveys of pesticide use by farmers are presented along with a proposed strategy for L. huidobrensis control.
2.
Materials and methods
To determine the relative abundance of leafminer species and the incidence of parasitism, 50 vegetable, ornamental and weed species in 13 families were sampled by collecting leafminer-infested leaves. Foliage surveys were conducted from March through December, 1998 in Bandung and Garut, West Java; Banjarnegara and Wonosobo, Central Java; Batu and Probolinggo, East Java; Solok and Agam, West Sumatra; and Karo and Simalungun, North Sumatra. Sample sizes were variable, depending on the availability of the host plants, at different locations but generally 10 ± 15 leaves per field were removed from crops with large leaves (cabbage, etc.), whereas 25 ± 35 leaves were taken from plants with small leaves (onions, etc.). Leaves were held in emergence containers as described by Shepard et al. (1998) until adult parasitoids and leafminer adults emerged. Pupae that did not yield adults were counted and recorded along with leafminer adults and parasitoids. John LaSalle, CABI Bioscience, London, United Kingdom, identified leafminer parasitoids and Sean T. Murphy, also with CABI Bioscience, assisted with identification of leafminers. Additionally, farmer surveys were carried out in the same localities as the foliage surveys to determine the frequency and kinds of pesticides used on vegetables as well as other impacts of leafminers in these crops.
3. 3.1.
Results and discussion Leafminer species
Intensive collections of infested leaves revealed at least three agromyzid species: L. huidobrensis, L. sativae and Chromatomyia horticola Goureau. The latter species is native to Asia (Kalshoven, 1981), and is easily separated from the others based on its generally darker body and larger size. Chromatomyia horticola emerged only from pea (Pisum sativum) foliage collected from Banjarnegara and Wonosobo, Central Java (table 1). The most abundant species present in the majority of the samples was L. huidobrensis. It infested many vegetable, ornamental and weed species (table 1). Liriomyza sativae was the only species found in Karawang, a lowland area in West Java, where it attacked angled luffa, wax gourd, yard-long bean and cucumber (table 1). It also was collected from castor bean and French bean in Karo, North Sumatra, and a few flies emerged from tomato leaves from collections carried out in 1996 at Tugu (Bogor), West Java. In all highland areas surveyed, numbers of L. sativae were low, however.
3.2.
Seasonal abundance
During the survey, Liriomyza infestations usually occurred at the end of the dry season (i.e. June ± July) and continued to the initial phases of the rainy season (August± November). Infestations during the intense rainy season (January ± March) were generally low. Within-field infestations were associated with crop
phenology. For example, on potato, leafminer populations increased slowly during the vegetative growth and increased rapidly during generative growth, followed by a decline as plants entered into senescence. This agrees with the findings of Supartha (1998). Shepard et al. (1998) observed seasonal variation in L. huidobrensis infestation levels and occurrence of its major parasitoid, H. varicornis, on potato and other crops. They found the highest populations in the Puncak area of West Java on potato toward the end of the wet season. Also, parasitism levels were higher in broccoli and scallions and lowest in potato. An entire potato crop was lost due to L. huidobrensis infestations towards the end of March 1996 (Shepard et al., 1998). However, leafminer infestations in broccoli and scallions did not cause reductions in vegetable yield or quality.
3.3.
Economic importance
Liriomyza huidobrensis was the most widely distributed leafminer in Indonesia and the most injurious to many important vegetables at elevations from 800 to 1700 m (AR and BMS, personal observations). This species is indigenous to the cooler, mostly highland areas of Latin America (Spencer, 1973). In Indonesia, heavily infested crops included potato, celery, cucumber, spinach, snap bean, snow pea, red bean, shallot, faba bean, and tomato. It also injured plants more seriously than did L. sativae because of the location and nature of its tunnelling behaviour within foliage. Liriomyza huidobrensis larvae feed in the spongy mesophyll of leaves where chloroplasts are located, whereas other leafminer species feed in the pallisade mesophyll (Parrella et al., 1985; Weintraub and Horowitz, 1995). Our field observations and surveys indicated that potato was especially susceptible to attack by L. huidobrensis (table 2). Infested fields were commonly observed in areas in Bandung and Garut (West Java), Banjarnegara and Wonosobo (Central Java), Alahan Panjang (West Sumatra), and Karo (North Sumatra). In those areas, most farmers reported that L. huidobrensis infestations reduced potato yields by 30 ± 70%. Additionally, in many instances crops were harvested 2 ± 3 weeks earlier than normal because of leafminer infestations (table 2). In the Alahan Panjang area of West Sumatra, devastating L. huidobrensis infestations forced growers to plant about 40% of the traditional potato-growing area in alternative crops (e.g. sweet potato) (Zamzami, personal communication). Although sweet potato also was infested by the leafminer, the damage is not serious. In Ciwidey (West Java), French bean was harvested only four times compared with seven times before the arrival of L. huidobrensis a few years ago. Heavy leafminer infestations on faba bean in Banjarnegara and Wonosobo (Central Java) reduced faba bean acreages due to seed shortages. In Puncak (West Java), heavily damaged crops included cucumber, celery and spinach. Attacks by L. huidobrensis reduced cucumber yields by 70% and on several occasions, plants were killed 30 ± 40 days after planting. Liriomyza huidobrensis also caused serious damage to ornamental plants grown in plastic houses in the Puncak area. Among heavily infested ornamentals were Petunia and Nicotiana. Estimated economic losses of about 30% were recorded in flower production in Puncak due to leafminers (Himma, personal communication).
259
Leafminers in Indonesia
Table 1.
Host plants of agromyzid leafminers in Indonesia C. horticola
L. sativae
L. huidobrensis
Scientific name
Common name
Brassica oleracea (L) Brassica chinensis L. Brassica juncea L. Brassica campestris L. Brassica rapa L. Nasturtium indicum (L). Hassk Nasturtium officinale R. Br Raphanus sativus L.
Cabbage, broccoli Pak choi cabbage Radish ``Petsai’’ Turnip `Swai tanah’ Watercress Chinese radish (Daikon)
Benincasa hispida (Thumb.) Cogn. Citrullus lanatus (Thumb.) Matsum. and Nakai Cucumis sativas L. Luffa acutangula (L.) Roxb. Melothria indica L. Sechium edule (Jacq.) Swartz
Wax gourd Watermelon
+ +
Cucumber Angled luffa Wild cucumber Chayote
+ +
Glycine max (L.) Merr. Phaseolus vulgaris L. Pisum sativum L. Vicia faba L. Vigna sinensis (L.) Hassk. Vigna unguiculata (L.) Walp.
Soyben French bean Snow pea Fava bean Red bean Yard-long bean
Allium ampeloprasum L. Allium cepa L. Allium fistulosum L. Allium sativum L.
Leek Shallot, onion Japanese bunching onion Garlic
Apium graveolens L. Daucus carota L.
Celery Carrot
Chrysanthemum spp. Emilia sonchifolia (L.) DC. Lactuca indica L. Luctuca sativa L. Gerbera jamesonii Bolus ex Hook. F. Dahlia sp. Ageratum conyzoides L. Erechtites hieraciifolia (L.) Raf. ex DC. Synedrella nodiflora (L.) Gaertn
Chrysanthemum Sow thistle Indian lettuce Lettuce Gerbera
+ + + + +
Dahlia Chick weed American burnweed
+ + +
Cinderella weed
+
Amaranthus sp. Deeringia amarantoides (Lamk.) Merr.
Amaranth Amaranth
Beta vulgaris L. Spinacia oleracea L.
Beet Spinach
Capsicum annuum L. Physalis angulata L. Lycopersicon esculentum Mill Solanum melongena L. Solanum americanum Mill.
Pepper Cutleaf ground cherry Tomato
Brassicaceae + + + + + + + + Cucurbitaceae
+ + +
Fabaceae + + + + + +
+ + + + + +
Liliaceae + + + + Umbelliferae + + Asteraceae
Amaranthaceae + +
Chenopodiaceae + + Solanaceae
Eggplant American black nightshade
+
+ + + + + (continued)
260
A. Rauf et al.
Table 1 (concluded). Scientific name
Common name
Solanum tuberosum L.
Potato
C. horticola
L. sativae
L. huidobrensis +
Euphorbiaceae Ricinus communis L.
Castor bean
+ Convolvulaceae
Ipmomoea batatas (L.) Lam. Ipomoea aquatica Forssk.
Sweet potato Water spinach
Basella alba L.
Indian Nightshade
Ocimum basilicum L.
Basil
+ + Basellaceae + Lamiaceae
Liriomyza sativae infested cucumbers in the lowlands of West Java. However, our information on this species is limited to only one visit to the area. Farmers in Cirebon complained about this leafminer attacking their watermelon crops. It is apparent that more field surveys are needed in these lowland areas.
3.4.
Parasitoids
Intensive sampling of infested leaves from vegetable and ornamental crops and weeds yielded 10 species of eulophid parasitoids (Asecodes sp., Chrysocharis sp., Cirrospilus ambiguus (Hansson and LaSalle), Closterocerus sp., Hemiptarsenus varicornis (Girault), Neochrysocharis formosa (Westwood), Neochrysocharis sp., Pnigalio sp., Quadrastichus sp., Zagrammosoma sp.) and one eucoilid (Gronotoma sp.). The most common parasitoid reared was H. varicornis. From a total of 2901 parasitoids that emerged from L. huidobrensis-infested leaves 92.3% were H. varicornis, and of 721 wasps that emerged from L. sativae-infested leaves 60% were H. varicornis. Levels of parasitism varied (0 ± 100%) among crops and locations, and were also affected by crop phenology. The highest levels of parasitism occurred on plants samples in Ciwidey and Cipanas (West Java): red bean (>70%), French bean, eggplant (>90%), soybean (>94%), amaranth (100%) and beet (>94%) (table 3). Conversely, parasitism was always low on potato ( < 3%), celery ( < 13%), and onion ( < 1%). Other studies have indicated low rates of parasitism of Liriomyza spp. as well as fewer parasitoid species reared from parasitized leafminers collected from onions (Johnson and Mau, 1986; Herr, 1987). In addition to parasitoids, predatory Diptera of the families Dolichopodidae, Empididae and Muscidae were observed capturing and killing agromyzid adults in Alahan Panjang (West Sumatra). In cabbage in the Cameron Highlands, Malaysia, L. huidobrensis adults were preyed upon by Coenosia exigua Stein (Diptera: Muscidae) (AR, G. R. Carner, Cahyono and BMS, personal observation). Additionally, we observed predation on leafminers by C. humilis in cabbage and Chinese cabbage in Garut, West Java, Indonesia. The impact of these flies on adult leafminer field populations is unknown.
3.5.
Current control practices
All potato farmers interviewed in Java and Sumatra applied chemicals to control L. huidobrensis, and most treated their
+
crops twice weekly (table 4). In Batu, more than 90% of the farmers applied pesticides three times weekly. Farmers generally applied insecticides from 10 to 30 days after planting and continued up to harvest. Discussions with farmers revealed that most treated their fields 16 ± 20 times during one potato-growing season, and most were not satisfied with chemical controls. On average, about 72% of the respondents said that insecticides were not effective for controlling L. huidobrensis. Interestingly, farmers continued to use insecticides, usually at higher than recommended rates. Most farmers relied on their own experiences (40%), experiences of other farmers (31%) and information provided at village kiosks (34%) in contrast to information that might be provided by an extension agent (16%) or a pesticide retailer (4%) (table 5). Over 35 conventional insecticides were used by farmers attempting to control leafminers in potato (table 5). The major insecticides applied overall according to grower responses were dimehypo (36%), profenofos (36%), carbosulfan (32%), cartap (32%), bensultap (14%), and deltamethrin (19%). Abamectin and cryomazine were gaining importance as preferred insecticides in West Java, whereas cartap was previously most widely used by farmers. However, cartap was withdrawn from the market in 1997. Some farmers ( < 11%) in East Java as well as West and North Sumatra preferred mixing two or three different compounds (table 4). Among the effective insecticides reported by farmers were cyromazine and abamectin, but both were expensive and only a few farmers could afford them. Most of the flower industries in Puncak depended on these chemicals to control leafminers. The inability of most conventional insecticides to suppress leafminer infestations motivated some farmers to try other control measures (table 4). One potato farmer in Garut used cloth sheets coated with sticky materials to capture adult flies by passing the sheets over the plant canopy twice daily (morning and afternoon). His crop appeared less damaged compared with his neighbours, but this was unsubstantiated by field data. Several farmers experimented with plant extracts (e.g. derris and tobacco), but reported that results were inadequate. Among the non-conventional insecticide methods developed was application of solutions of lime. This was commonly used in Cipanas during the dry season. It was common to see white lime residues on celery foliage. Many celery farmers believed that lime reduced leafminer populations but this was not substantiated.
40
57
43
10
0 20 40 30 10 0
Normal harvest timing 1 week earlier 2 weeks earlier 3 weeks earlier 4 weeks earlier Uncertain
0 0 0 20 80 0
0 3
Garut (n=30)
13 33
Bandung (n=30)
10 to < 30% yield loss > 30 to < 50% yield loss > 50 to > 70% yield loss > 70% yield loss
Impact parameter
West Java
Table 2.
13 13 25 47 3 0
13
19
28 41
Banjarnegara (n=32)
100
0 87
3
7 3
Probolinggo (n=30)
Percent of farmers 0 0
Batu (n=25)
East Java
Percent of farmers forced to begin initial harvest 0 0 0 3 0 0 63 0 0 34 0 13 0 100 87 0 0 0
17
23
26 34
Wonosobo (n=35)
Central Java
0 9 14 14 63 0
29
26
11 33
Solok (n=35)
63 3 7 7 13 0
13
17
27 43
Agam (n=30)
West Sumatra
Impact of leafminer infestations as percieved by potato farmers on the islands of Java and Sumatra, Indonesia
2 6 48 20 7 14
5
32
34 29
Karo (n=56)
0 0 56 38 6 0
6
56
0 38
Simalungun (n=16)
North Sumatra
8 5 25 22 37 1
34
26
15 26
Mean response across regions (%)
Leafminers in Indonesia 261
262
A. Rauf et al.
Table 3.
Levels of parasitism of leafminers in vegetable crops in Indonesia No. Liriomyza
Host
Location
Amaranth Angled loofah Beet Cabbage
Cipanas, W. Java Jatisari, W. Java Cipanas, W. Java Samarang, W. Java Bakal, C. Java Kabanjahe, N. Sumatra Simpang, N. Sumatra Cipanas, W. Java Kabanjahe, N. Sumatra Ciwidey, W. Java Ciherang, W. Java Kejajar, C. Java P. Banteng Samarang, W. Java Ps. Sarongge, W. Java Ciwidey, W. Java Cipanas, W. Java Jatisari, W. Java Simpang, N. Sumatra Cipanas, W. Java P. Banteng, C. Java Rawajati, C. Java Ciwidey, W. Java Cipanas, W. Java Pangalengan, W. Java Kejajar, C. Java Bakal, C. Java P. Banteng, C. Java Ciwidey, W. Java Cipanas, W. Java Tiga Panah, N. Sumatra Cipanas, W. Java Ciwidey, W. Java Pa. Sarongge, W. Java Bakal, C. Java P. Banteng, C. Java Samarang, W. Java Bakal, C. Java Rawajati, C. Java Simpang, N. Sumatra Pangalengan, W. Java Garut, W. Java Ciwidey, W. Java Cipanas, W. Java Ciherang, W. Java Kejajar, C. Java Kabanjahe, N. Sumatra Tiga Panah, N. Sumatra Ciwidey, W. Java Ciwidey, W. Java Ciherang W. Java Samarang, W. Java Tiga Panah, N. Sumatra Simpang, N. Sumatra Jatisari, W. Java Ciwidey, W. Java Bakal, C. Java Ciwidey, W. Java Bakal, C. Java Ciwidey, W. Java Ciwidey, W. Java Jatisari, W. Java
Caisin Celery
Chinese radish Chrysanthemum Cinderella weed Cucumber Dahlia Eggplant Faba bean French bean
Garlic Glossy-nightshade
Nasturtium Pea
Potato
Red bean
Ricinus Sow thistle Soybean Tomato
Wax gourd Welsh onion Wild amaranth Wil cucumber Yard long bean
No. parasitoids emerged
Emerged
Pupae aborted
Total
15 518 255 33 8 1 3 18 22 2 1 1 0 2 4 2 16 175 1 10 32 454 74 204 359 104 24 0 1 34 4 21 239 23 0 0 5 3 34 1 2 0 239 55 56 5 162 26 76 90 5 23 3 5 16 1 0 27 4 7 20 12
0 492 5 44 24 3 3 36 1 456 485 6 32 21 22 131 20 167 5 1 552 526 53 30 16 19 6 3 140 12 19 0 413 70 592 1055 372 139 568 6 3102 1282 72 2 157 244 639 18 141 1 2 12 10 104 4 122 7 76 14 58 5 18
0 68 11 46 8 261 145 94 95 518 843 1 182 7 4 30 10 8 5 0 138 34 16 27 19 6 3 4 21 22 4 1 260 0 22 15 1692 62 874 850 933 543 15 0 133 93 1226 12 26 4 0 10 5 324 0 267 2 58 8 10 0 4
15 1078 271 123 40 265 151 148 118 976 1329 8 214 30 30 163 46 350 11 11 722 814 143 261 394 129 33 7 162 68 27 22 912 93 614 1070 2069 204 1470 857 4035 1437 328 57 346 342 2027 166 243 95 7 45 18 433 30 390 9 161 26 75 25 34
Percent parasitism 100 48 94 27 20
