Contribution to the knowledge of schultzei (Thysanoptera: )

G. Vierbergen & W. R Mantel

VIERBERGEN, G. & W. P. MANTEL, 1991. CONTRIBUTION TO THE KNOWLEDGE OF (THYSANOPTERA: THRIPIDAE). - ENT BER, AMST 51 (1): 7-12.

Abstract: In The Netherlands a new species has settled in glasshouses: Frankliniella schultzei (Trybom). Although quite a common species in the tropics, so far settlings in glasshouses were not recorded in literature. A study has been started on its identification, host-specificity, world distribution and economic importance. The systematics do not seem to be clear. Possibly more species are involved. F schultzei is mainly feared because of its ability to transmit Spotted Wilt Virus (TSWV). Direct thrips damage is seldom of interest. Especially the international flower trade has to realize the risks associated with F schultzei.

G. Vierbergen, Plant Protection Servive, P.O. Box 9102, 6700 HC Wageningen. W. P. Mantel, Research Institute for Plant Protection, P.O. Box 9060, 6700 GW Wageningen.

Introduction

In the tropics Frankliniella schultzei (Trybom, ton, 1933). A few months after elimination of 1910), the cotton bud thrips, is known as a the population at Eiden the dark form of the common pest (Mound et al, 1976) and mostly thrips was found again in great numbers in feared for its ability to transmit the Tomato flowers of Cactaceae in some nurseries. An Spotted Wilt Virus (Hill, 1983). It can live in inspection of imported, still packed cactus flowers of plants belonging to different fami¬ plants from Brazil was in one of the nurseries lies. Introduction of this species into the tem¬ successful: the dark form of F schultzei was perate climate zone has been reported from found in low numbers on the plants. These rooms used for vegetative propagation of hya- specimens were identical to the thrips collected cinthbulbs in The Netherlands (Van Rossem et in the nurseries. Occurrence of F schultzei in al, 1968; Mantel, 1968). Other settlings in tem¬ the glasshouse environment has never been perate regions have not been reported. reported before. Because of the virus transmis¬ From an inspection of Dutch flower auc¬ sion ability of F schultzei and its settling in tions for Thysanoptera in 1987 it appeared that Dutch glasshouses a study on its identification, F schultzei can be considered as a quite com¬ host-specificity, world distribution and eco¬ mon species of thrips in the international nomic importance was started. flower trade. Other species regularly found were Frankliniella occidentalis (Pergande) and Synonymy Thrips tabaci Lindeman (Vierbergen & Ulen¬ berg, 1988). Both species occur world-wide in The great variability of the species and the glasshouses. Hence settling in glasshouses of large area of distribution (fig. 1) has resulted in the pantropical species F schultzei could also the description of different forms of F schult¬ be expected. zei. They can be divided in two more or less Early 1988 the dark form of F schultzei was distinguishable forms: a pale one and a dark found in a glasshouse in flowers of Saintpaulia one. The natural distribution of the pale form ionantha Wendl in The Netherlands (Eiden). is mainly north, that of the dark form south of This dark form is originally described as the equator. Frankliniellapaucispinosa from Brazil (Moul¬ It is not possible to judge on morphological Ent. Ber., Amst. 51 (1991)

Fig. 1. Distribution of Frankliniella schultzei (Trybom). characteristics only whether all synonyms of F VIII the comb is only developed laterally schultzei mentioned by Jacot-Guillarmod - male: the glandular areas on stemites III-VII (1974) are correct. More than one species broad, about half the width of the sternite. might be involved. Before this is sorted out F schultzei has to be considered as a variable Only the form of F schultzei, which has been species. described as F paucispinosa, with the almost completely dark brown body, has settled in the Dutch glasshouses. By import inspection of cut Diagnosis flowers other colour forms, such as interme¬ The genus Frankliniella is a rather well defined diates and light yellow forms have also been genus. Satisfactory descriptions of the genus found. Morphological differences between the are given by Priesner (1964) and Sakimura & colour forms could not be determined except O’Neill (1979). F schultzei can be distinguished for one female specimen imported on Limo- from the other, approximately 150 Frankli- nium sp. from Kenya in 1987. This thrips, with niella-species by the combination of the follow¬ only the antennal tips brown, has ocellar setae ing morphological characteristics (males and with a length of 22 pm, whereas the normal females): length of these setae is 34-48 pm. The specimen - length of one pair postocular setae more fits well in the description of Frankliniella than twice the length of the other postocu¬ dampft Priesner, 1923, which is now regarded lars (fig. 2) as a junior synonym of F schultzei (Mound, - ocellar setae situated between the posterior 1968). ocelli (fig. 2) - on the pronotum between the anteromargi- Distribution nals usually two setae (sometimes three or four) present F schultzei has a pantropical distribution (Ja¬ - metanotal pores absent (fig. 3). cot-Guillarmod, 1974). In the subtropics the species is probably less common, while in the Additional characters: temperate regions the is restricted to - female: at the posterior margin of tergite heated places such as glass- and storehouses. Ent. Ber., Amst. 51 (1991) 9

Fig. 2. Head of Frankliniella schultzei (Trybom), $, Lisse, The Netherlands, 1965, Hyacinthus. Scale bar: 25 pm.

So far, reports on the presence of this thrips in Anonymus (1974); 11. Sakimura (1986); 12. temperate zones have been rare (England, The Ortiz (1973). Netherlands). In general its range lies between latitude 40° north and 40° south (fig. 1). Host-specificity Countries where F schultzei has been found so far (the figures refer to the literature cited F schultzei is a polyphagous species, mainly below): living in the flowering parts of plants. Repre¬ Europe - The Netherlands (introduced), Eng¬ sentatives of at least twelve dicotyledonous land (found incidentally)1’2 Italy1. plant families are known as host plants. Large Asia - Israel1, Iraq3, Iran4, India1, Sri Lanka1, families like Leguminosae, Solanaceae and Bangladesh5, Indonesia: Java6, New Guinea1. Compositae are included. Also representatives Africa - Canary Islands1, Morocco1, Egypt1, of monocotyledonous families are visited and Sudan1, Cape Verde Islands7, Senegal1, Gam¬ serve as host plants, e.g. Liliaceae, Iridaceae bia1, Ghana1, Togo8, Nigeria9, Somalia1, Ke¬ and Graminae. nya1, Uganda1, Congo1, Zimbabwe1, Nami¬ In contrast with the above mentioned angio- bia1, South Africa1. spermous families, needle leaved trees, other Australia and Pacific Islands - Australia (in¬ gymnosperms and lower plants are not ap¬ troduced?)1, 3, Mariana Islands1, Johnston Is¬ propriate for the reproduction of F schultzei. land1, Hawaii1. F schultzei is likely as polyphagous as a North America - U.S.A.: Florida10. number of other Frankliniella species as e.g. Central America and the West Indies - St. Frankliniella intonsa (Trybom) and F. occi¬ Thomas11, Puerto Rico11, Dominican Repub¬ dent alis. More host-plant records, however, lic11, Jamaica1. will be needed to justify this statement. South America - Colombia1, Peru12, Brazil1, Argentina1. Economic Importance

1. Jacot-Guillarmod (1974); 2. Mound et al. Direct damage (1976); 3. Kirk (1987); 4. Bournier & Couilloud (1969); 5. Zur Strassen (1984); 6. Miyazaki et Like many other species of thrips F schultzei al. (1984); 7. Zur Strassen (1981); 8. Zur can cause suction damage and probably also Strassen (1982); 9. Okwakpam (1967); 10. damage by laying eggs in the leaves and flow- 10 Ent. Ber., Amst. 51 (1991)

Fig. 3. Metanotum of Frankli- niella schultzei (Trybom), $, flowerauction Aalsmeer, The Netherlands, Limonium, origin: Israël, 1987. Scale bar: 20 |im. ers. The latter, however, has never been con¬ In The Netherlands F schultzei was noxious firmed. The flowers can be damaged by the in the usual way of vegetative propagation of suction activity in such a way that they become hyacinth bulbs (Van Rossem et al., 1968; Man¬ unsalable. However, reports on this type of tel, 1968; Mantel & Van de Vrie, 1988). Prob¬ damage by F schultzei are rare. In The Nether¬ ably by the application of effective chemical lands suction damage was established in flow¬ control in the propagation room, the thrips no ers of Mammillaria sp. (Cactaceae) in a glass¬ longer occurs on hyacinths for propagation in house in October 1988. In the flowers two The Netherlands. species of thrips could be found: F schultzei The appearance on hyacinth bulbs was due and F occidentalis. Probably the unusually to the easily attainable plant-liquids from the high number of thrips per flower was respon¬ injuries of the bulb. Also T tabaci, which is sible for the damage; normally both thrips spe¬ common in glasshouses in The Netherlands, cies feed only from the nectar produced by the took advantage of this situation and settled in flowers of Mammillaria sp. the propagation rooms. The damage symp¬ According to the literature F schultzei can toms caused by both species cannot be distin¬ cause yield loss due to diminishing fruit setting guished from each other (Franssen & Mantel, as a result of suction damage. Flower shedding 1965; Mantel, 1968). and poor fruit setting by red gram (Cajanus cajan (L.) Millsp.) in India were described by Indirect damage Vaishampayan & Singh (1969). Because another thrips species was involved (Taenio- Because of its ability to transmit Tomato Spot¬ thrips nigricornis (Schmutz)), the damage par¬ ted Wilt Virus (TSWV) F schultzei is interna¬ ticularly caused by F schultzei is unclear. tionally a most feared insect (Hopkins, 1956; Still, the ability of F schultzei to injure cot¬ Klesser, 1966; Sakimura, 1969; Shaw, 1979). ton flowers in southern Iran has been con¬ The vector capacity of this thrips has been firmed (Bournier & Couilloud, 1969). In this proved in several crops (e.g. , tobacco region the thrips seems to be responsible for and tomato). Sakimura (1969) discovered that withered spots or wounds in the pericarp of the not all forms of F schultzei could be consi¬ bolls. However, a negative effect on the ripen¬ dered as vector. The pale form of Hawaii, for ing of the bolls and the quality of the seed has example, originally described as Frankliniella not been observed. Control did not seem to be sulphurea Schmutz, seems to be unable to necessary. transmit TSWV. Most likely only the dark Ent. Ber., Amst. 51 (1991) 11 form can transmit TS WV. This is supported by large host range and its ability to settle in the fact that transmission is only recorded from glasshouses and to transmit TSWV. regions south of the equator (Southern Africa, Australia and South America). This dark form Acknowledgements is also able to settle in glasshouses and thereby enhances the risks of the dispersion of TSWV. Many thanks are we indebted to Dr. Ir. A. K. TSWV has a wide host range and is one of Minks (Research Institute for Plant Protec¬ the few viruses which can pass from dicotyle¬ tion, Wageningen) and Dr. S. A. Ulenberg dons to monocotyledons. It was first recorded (Plant Protection Service, Wageningen) for in Australia in 1915 (Smith, 1957). Before the their valuable critical remarks on the manus¬ second world war the virus was found world¬ cript. We are also very grateful to Mr. C. A. wide. Later on the virus became rare in The Quint and Mr. A. C. M. Tonk, both field Netherlands. Probably because of the appear¬ inspectors of the Plant Protection Service. ance of F occidentalism another vector of Without their active help many facts about the TSWV, spotted wilt becomes more important. tramp species F schultzei should still be un¬ Especially growers of Chrysanthemum mori- known. folium de Ramatuelle have problems with the virus. References The whitefly Bemisia tabaci Gennadius, known as a vector of nineteen viruses, recently Anonymous, 1974. A thrips (Frankliniella schultzei (Try- became of interest in international flower trade bom)). - Fla coop. econ. Insect Rep. 24 (49/52): 873. (Cock, 1986). The ability of the whitefly to Bournier, A. & R. Couilloud, 1969. Les thrips du co¬ tonnier en Iran. - Cot. Fib. trop. 24: 211-218. transmit viruses is feared more than its prop¬ Cock, M. J. W., 1986. Bemisia tabaci, a literature survey erty to cause direct damage. Most likely resist¬ on the cotton whitefly with an annotated bibliography: ance against insecticides enabled F occidenta¬ 1-121. Food and Agriculture Organization of the U.N., ls and B. tabaci to settle in glasshouses in C.A.B. Int. Inst. Biol. Cont., U.K. temperate areas (Robb et al, 1988; Price et al., Franssen, C. J. H. & W. P. Mantel, 1965. Thrips tabaci op hyacintebollen. - Neth. J. PI. Pathol. 71: 67-71. 1987). F. schult zei can be compared with B. Hill, D. S., 1983. Agricultural insect pests of the tropics tabaci in many ways. The thrips is only slightly and their control, ed. 2: i-xii, 1-746. Cambridge Univer¬ noxious to plants, but its function as a vector sity Press, Cambridge, Great Britain. of TSWV makes the thrips of economic inter¬ Hopkins, J. C. F, 1956. Tobacco Diseases: with special Reference to Africa. Commonw. Mycol. Inst., Kew. est. However, in contrast with B. tabaci an Jacot-Guillarmod, C. F, 1974. Catalogue of the Thysa- insecticide resistant strain of F schultzei is not noptera of the world. - Ann. Cape Prov. Mus. (Nat. known to exist till now. Hist.) 7: 517-976. Kirk, W. D. J., 1987. A key to the larvae of some common australian flower thrips (Insecta: Thysanoptera), with a Future outlook host-plant survey. - Aust. J. Zool. 35: 173-185. Klesser, P. J., 1966. Tomato spotted wilt virus on Arachis In The Netherlands it appeared to be impossi¬ hypogaea. - S. Afr. J. agric. Sei. 9: 711-717. ble to eliminate F schultzei with insecticides Mantel, W. P, 1968. Een aantasting van hyacintebollen from the glasshouses where it infests Cacta- in de holkamer door Frankliniella schultzei Trybom. - Ent. Ber., Amst. 28: 106-108. ceae. It is expected that not the resistance Mantel, W. P. & M. van de Vrie, 1988. A contribution against insecticides, but the hiding behaviour to the knowledge of Thysanoptera in ornamental and in the flowers is the main factor responsible for bulbous crops in the Netherlands. - Acta Phytopath, surviving chemical treatment. Nevertheless in¬ ent. hung. 23: 301-311. crease of resistance can never be ruled out in Miyazaki, M., I. Kudo & A. Iqbal, 1984. Notes on the thrips (Thysanoptera) occurring on the soybean in this variable species. So, the international Java. - Kontyû 52: 482-486. flower trade must realize the risks associated Moulton, D., 1933. The Thysanoptera of South America with F schultzei with its great variability, its II. - Revta Ent., Rio de J. 3: 96-133. 12 Ent. Ber., Amst. 51 (1991)

Mound, L. A., 1968. A Review of R.S. Bagnall’s Thysa- Sakimura, K., 1986. Thrips in and around the coconut noptera Collections. - Bull. Br. Mus. (nat. Hist.) Suppl. plantations in Jamaica, with a few taxonomical notes 11:1-181. (Thysanoptera). - Fla Ent. 69: 348-363. Mound, L. A., G. D. Morison, B. R. Pitkin & J. M. Sakimura, K. & K. O’Neill, 1979. Frankliniella, redefi¬ Palmer, 1976. Thysanoptera. - Hndbk. Ident, br. Ins. nition of genus and revision of Minuta group species 1 (11): 1-82. (Thysanoptera: Thripidae). - United States Dept. Okwakpam, B. A., 1967. Three species of thrips (Taenio- Agric. tech. Bull. 1572: 1-49. thrips sjostedti (Tryb.), Haplothrips gowdeyi (Frank¬ Shaw, M. J. P, 1979. Insect-borne diseases of tobacco in lin) and Frankliniella schultzei (Tryb.) (Thysanoptera) Rhodesia and the role of the tobacco-free period. - in cowpea (Vigna unguiculata) flowers in the dry season Rhodesia Agric. J. 76 (2): 87-90. at Badeggi, Nigeria. - Niger. Ent. Mag. 1 (3): 45-46. Smith, K. M., 1957. A. textbook of plant virus diseases. Ortiz, P. M., 1973. Contribution al conocimiento de los ed. 2: i-vi, 1-652. J. & A. Churchill Ltd., London. Thysanoptera del Peru. - Revta peru. Ent. 16(1): 111- Strassen, R. zur, 1981. Zur Wirtspflanzen-Bindung und 114. Verbreitung von Fransenflüglem auf einigen Inseln des Price, J. F, D. J. Schuster & D. E. Short, 1987. Recent Kapverden-Archipels (Insecta: Thysanoptera). - advances in managing the sweetpotato whitefly on Senckenbergiana biol. 62: 295-312. Poinsettia. - Bradenton GCREC Research Report Strassen, R. zur, 1982. Thysanopterologische Notizen BRA 1987-21:1-6. Gulf Coast Research and Education (6) (Insecta: Thysanoptera). - Senckenbergiana biol. Center IFAS, Univ. Florida, Bradenton. 63: 191-209. Priesner, H., 1923. A Dampfs Aegypten-Ausbeute. Thy¬ Strassen, R. zur, 1984. Gelbschalenfänge von Fransen¬ sanoptera. - Ent. Mitt. 12: 63-66, resf. 115-121. flüglem aus Kartoffelkulturen in Bangladesh. - Senck¬ Priesner, H., 1964. Ordnung Thysanoptera (Fransen- enbergiana biol. 65: 75-95. flügler. Thripse). Best. Büch. Bodenfauna Eur. 2: 1-142. Trybom, F, 1910. Physapoda. - Denkschr. med. naturw. Akademie-Verlag, Berlin. Ges. Jena 16: 147-174. Robb, K. L., J. P. Newman & M. P. Parrella, 1988. The Vaishampayan, S. M. & Z. Singh, 1969. Comparative biology and control of the western flower trips. - effectiveness of some modern insecticides against the TSWV News! 3: 6-12. blossom thrips of red-gram (Cajanus cajan (L.) Rossem, G. van, H. C. Burger & C. F. van de Bund, Millsp.). - Indian J. agric. Sei. 39 (1): 52-56. 1968. Entomologisch onderzoek. - Jaarboek Vierbergen, G. & S. A. Ulenberg, 1988. Frankliniella 1965/1966: 62-75. Plantenziektenkundige Dienst, occidentalis en andere tripsen op siergewassen bestemd Wageningen. voor im- en export (Thysanoptera). - Ent. Ber., Amst. Sakimura, K., 1969. A comment on the color forms of 48: 117-120. Frankliniella schultzei (Thysanoptera: Thripidae) in re¬ lation to transmission of the tomato-spotted wilt virus. - Pacif. 11: 761-762. Accepted 16.vii. 1990.