Summary PRA Questions

CSL Pest Risk Analysis for Trialeurodes ricini CSL copyright, 2005

05-11614 P PM point 8.2 CSL PEST RISK ANALYSIS FOR TRIALEURODES RICINI

STAGE 1: PRA INITIATION

1. What is the name of the pest? Trialeurodes ricini (Misra) Hemiptera Aleyrodidae castor whitefly*

* = not an official UK DEFRA common name Synonyms Aleyrodes ricini Misra Trialeurodes rara Singh

Note: It is difficult to identify this organism, it may be confused with Trialeurodes vaporariorum, the glasshouse whitefly. Trialeurodes ricini may be the senior synonym of T. lauri, a native Mediterranean species, present in France, Greece, Italy, Turkey & the former Yugoslavia (Martin et al., 2000).

Update: Taxonomic research by Malumphy et al (2004) investigated molecular and morphological characteristics and confirmed that T. ricini and T. lauri are distinct species.

2. What is the reason for the PRA? A previous UK PRA on this organism was carried out in Sept. 1997. The current PRA updates the earlier PRA following a second finding of a live immature specimen on produce (unidentified leaves, suspected to be Amaranthus, from Nigeria) by PHSI. The first finding was on unidentified leaves from Cameroon in August 1997. The pest has also recently spread to the Canary Isles (La Gomera) (EPPO, 2000).

3. What is the PRA area? This PRA considers the whole EPPO region concentrating on the European and Mediterranean area, i.e. EPPO west of the Ural mountains.

STAGE 2: PEST RISK ASSESSMENT

4. Does the pest occur in the UK, EU or EPPO region or does it arrive regularly as a natural migrant? UK: No. This pest does not occur in the UK. It is not a natural migrant. EU/ EPPO: Occurs in Israel and Egypt (Egypt is not an EPPO member but is in the EPPO region). Recently spread to Canary Isles (EPPO, 2000).

5. Is there any other reason to suspect that the pest is already established in the UK, EU or EPPO region? Yes. See 4.

6. What is the pest’s EU Plant Health Directive status? Not listed. 7. What is the pest’s EPPO Status?

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Trialeurodes ricini was added to the EPPO Alert List in April 2000 at the suggestion of the UK NPPO.

8. What are its host plants? Polyphagous, feeding on hosts in at least thirteen plant families (Table 1).

Table 1: Trialeurodes ricini host plants Family Binomial plant name Common name Reference Annonaceae Annona glabra - Mound & Halsey, 1978 Asteraceae Bidens bipinnata - Abd-Rabou et al., 2000 " Cichorium endivia - Abd-Rabou et al., 2000 " Sonchus oleraceus - Abd-Rabou et al., 2000 Convulvulacea Ipomea batata sweet potato Mound & Halsey, 1978 e Cucurbitaceae Cucurbita maxima pumpkin Shishehbor & Brennan 1996 a " Cucumis melo melon Shishehbor & Brennan 1996 a " Cucumis sativus cucumber Shishehbor & Brennan 1996 a Ericaceae Arbutus sp. - Mound & Halsey, 1978 Euphorbiaceae Breynia rhamnoides - Mound & Halsey, 1978 " Euphorbia sp. - Mound & Halsey, 1978 " Phyllanthus sp. - Mound & Halsey, 1978 " Ricinus communis castor oil plant Mound & Halsey, 1978 Leguminoseae Lablab niger Indian bean Martin, 1987 " Phaselous vulgaris French beans Shishehbor & Brennan 1996 a Malvaceae Gossypium hirsutum cotton Mound & Halsey, 1978 Myrtaceae Psidium sp. - Martin, 1987 Rosaceae Rosa sp. - Mound & Halsey, 1978 Rutaceae Murraya koenigi - Mound & Halsey, 1978 Sapotaceae Achras zapota sapodilla Hill, 1983 Solanacea Lycopersicon esculentum tomato Idriss et al., 1997 " Solanum melongena aubergine Shishehbor & Brennan 1996 a " Solanum tuberosum potato Shishehbor & Brennan 1996 a

Note: This whitefly is polyphagous and its full host list could potentially be greater than the hosts listed in Table 1 or recorded in the literature to date. T. ricini may be able to adapt to feed on other hosts as it expands its geographic distribution.

9. What hosts are of economic and/or environmental importance in the PRA area? Pumpkins, melons, cucumbers, French beans, tomatoes, aubergines and potatoes. Also Rosa sp. and Euphorbia sp. at certain times of the year.

10. If the pest needs a vector, is it present in the PRA area? No vector is needed. This is a free living organism.

11. What is the pest’s present geographical distribution? (Sources: Mound & Halsey, 1978; Martin, 1987; Idriss et al., 1997).

North America: Absent. Central America: Absent. South America: Absent. Caribbean: Absent. Europe: Canary Islands (EPPO, 2000). Africa: Cameroon (unconfirmed), Chad, Egypt, Ivory Coast, Kenya, Malawi, Nigeria, Sierra Leone, Sudan, Uganda. Middle East: Egypt, Iran, Iraq, Israel, Saudi Arabia. Asia: Brunei, Hong Kong, India, Malaya, Pakistan, Philippines, Thailand. Oceania: Absent.

12. Could the pest enter the PRA area? Yes. T. ricini has spread and established in the Canary Isles (EPPO, 2000). The pest is already established in Israel. This PRA was initiated after a second finding of a live immature on produce (possibly Amaranthus leaves from Nigeria) by PHSI. The first finding was on unidentified leaves from Cameroon in August 1997. T. ricini was again detected in a consignment on unidentified leaves (possibly okra) from Nigeria in May 2001. It was also detected in January 2004 on “African leaves” from Nigeria and in October 2004 in a consignment of Murraya koenigii (curry leaves) from India.

13. Could the pest establish outdoors in the PRA area? Northern EU/EPPO: No. This is a pest with a high threshold temperature for development. Eggs require a mimimum 17C for development. The optimum temperature for development is 30C (Shishehbor & Brennan, 1995).

Southern EPPO: Yes. this pest is already present in the Canary Isles. It has been reported in Egypt (it was already known in Israel) where it occurs in all governates on many different crops in huge numbers during the summer (Idriss et al., 1997).

In laboratory studies, Shishehbor & Brennan, (1996a) showed that adults developed in 18 to 30 days, depending upon the host, at daytime temperatures of 25C (Table 2).

Table 2: Development time and % survival on different T. ricini hosts (Day temp = 25C, night = 17C) Host Development time % survival (days from egg to adult) (eggs to adult) Aubergine 18 72 Cotton 18 68 Potato 20 41 French bean 21 58 Pumpkin 30 59

In field conditions in northern India, populations are seen from February to November. In September, the life cycle is completed in 19-21 days (Nair, 1986).

Temperatures of 25 to 30 C appear to best suit T. ricini population development (Table 3) (Shishehbor & Brennan, 1996b).

Table 3 : Life traits of T. ricini at different constant temperatures (Unspecified host). (from Shishehbor & Brennan, 1996b)

Temperature Mean no. Longevity Daily intrinsic rate Generation time (C) eggs laid (days) of increase (days) 20 183 39 0.05 70 25 224 28 0.11 - 30 294 16 0.18 - 35 132 10 0.15 25

14. Could the pest establish in protected environments in the PRA area? Yes. Although it has not been reported from protected cultivation, this pest could probably establish on hosts in heated protected environments in northern EU/EPPO. The main crops at risk would be cucumbers, tomatoes, and aubergines grown in protection.

In the UK, 283 ha of heated tomatoes were grown in 1996 (MAFF, 1998). Other hosts grown in protected cultivation are Rosa and poinsettia (a species of Euphorbia). The mean area of protected Rosa grown between 1985 and 1994 was 12.2ha, (MAFF, 1996). Poinsettia is also grown at certain times of the year in protected cultivation.

Southern EU/EPPO members growing cucumbers, tomatoes, melons, pumpkins and aubergines are likely to be at greater risk.

15. How quickly could the pest spread within the PRA area? The finding in the Canary Isles and interceptions by the UK show that this pest can spread in trade. T. ricini may have been slow to spread up to now but its presence in a place, such as the Canary Isles, with strong European trading links suggest that spread may now increase.

16. What is the pest’s potential to cause economic and/or environmental damage? In the EPPO region, protected crops and the outdoor cultivation of crops such as potatoes and French beans in the warm climate of southern MS are primarily at risk from this pest. The potential of Trialeurodes ricini as an outdoor pest is limited in northern EC due to the unsuitable climatic conditions. In Egypt, T. ricini is a serious pest of tomatoes and although there are no details of the extent of the damage, it is this observation that primarily triggers concern at the threat posed by this species.

Like Bemisia tabaci, T. ricini has a number of biotypes, each of which is viruliferous (Idriss et al., 1997).

17. What is the pest’s potential as a vector of plant pathogens? T. ricicni was not known to be a virus vector until Idriss et al., (1997) reported it as a vector of Tomato Yellow Leaf Curl Virus (TYLCV) in Egypt.

Update: Nelson et al. (2004) used a T. ricini population from the Canary Isles and conducted virus transmisison experiments on beans (P. vulgaris), tomatoes (L. esculentum) and other hosts. Working with TYLCV and other viruses, they were not able to demonstrate virus transmission by T. ricini. [This can be due to genetic differences between populations of T. ricini in Egypt and the Canary Isles, i.e. Egyptian and Canary strains/ biotypes may exist].

STAGE 3: PEST RISK MANAGEMENT

18. What are the prospects for continued exclusion? Unclear. Since a first PRA was conducted in September 1997, this pest has been newly reported in Egypt where it is a serious pest of tomatoes and a vector of TYLCV. It has also recently spread to the Canary Isles (EPPO, 2000).

19. What are the prospects of eradication? Outdoors in northern EC good - the climate is unsuitable and would inhibit establishment. However in southern EC/EPPO members, and in protected cultivation throughout the PRA area, control may be difficult. There can be rapid population build up and individuals inhabit the underside of leaves affording a degree of protection from chemical spray treatments. 20. What management options are available for containment and control? In India, monocrotophos, dimethoate and quinalphos, all at 0.05%, are recommended for controlling Trialeurodes ricini on R. communis (castor) (Patel et al., 1986).

Encarsia formosa is a parasite of Trialeurodes ricini, and may be used as a biological control agent (Shishehbor & Brennan, 1996c, d).

CONCLUSION OF THE PEST RISK ANALYSIS

Since the first PRA on T. ricini was conducted in 1997,  it has spread to a new countries (Egypt, Spain (Canary Isles),  has new host plants,  is a vector of TYLCV, The new evidence from Idriss et al., (1997) and Shishehbor & Brennan (1996) has been used to re-evaluate the risk posed by T. ricini.

Trialeurodes ricini is a polyphagous, multivoltine species with several biotypes. It is difficult to control and is a virus vector. It is likely to cause serious damage if it established within protected cultivation within EPPO and could cause damage to outdoor crops in southern MS.

It is recommended that Trialeurodes ricini be considered for addition to EC Annex I/AI and EPPO list A2.

MAJOR UNCERTAINTIES AND FURTHER WORK

Section of PRA Major uncertainties Urgent futher work required to improve the PRA Taxonomy T. ricini may be the senior synonym Taxonomic studies at CSL have of T. lauri, a native Mediterranean shown that T. lauri and T. ricini are species (Martin et al., 2000). distinct species (Malumphy et al., 2004). Pathway Other than the pathways of previous Examine and target other potential interceptions, no other specific pathways. pathways have been identified. Distribution Distribution within other -EU / Contact other EU / EPPO states to EPPO states is uncertain. ask for information about presence of the pest. Hosts Very polyphagous. Table 1 listing A comprehnsive list of hosts is hosts may be incomplete. required. Establishment Area of southern EU/EPPO which CLIMEX mapping using has suitable climate for experimental data of the thermal establishment. biology of the pest. Spread Rate of spread if moved in trade. - Impact Most studies have examined the Data to determine likely damage to impact on Ricinus communis. Data EPPO hosts. on damage to other EPPO hosts is lacking. Management Test for resistance. -

Documentation in Support of the PRA Is there a complementary datasheet with supporting information? YES CABI Crop Protection Compendium, Trialeurodes ricini Basic datasheet (C)

Has an on-line search of CABI Abstracts been carried out? YES References Abd-Rabou, S., Hussein, N., Sewify, G. H. & Elnagar, S. (2000) Seasonal abundance of the whitefly Trialeurodes ricini (Misra) (Homoptera: Aleyrodidae) on some weeds and on castor plants in Qalyubia, Egypt. Bulletin of Faculty of Agriculture, University of Cairo. 51 (4), 501-510. EPPO (2000) EPPO Reporting Service, 2000/173, Whitefly-transmitted viruses and whitefly species in Islas Canarias, Spain. From Anonymous (2000) Canary Islands results. EWSN Newsletter, 3, p2. Hill, D.S. (1983) Agricultural Insect Pests of the Tropics and their control, 2nd Edn., Cambridge University Press, London, 746pp. Idriss, M. Abdallah, N., Aref, N., Haridy, G. & Madkour, M. (1997) Biotypes of the castor bean whitefly Trialeurodes ricini (Misra) (Hom., Aleyrodidae) in Egypt: biochemical characterization and efficiency of geminivirus transmission. Journal of Applied Entomology, 121, 501-509. MAFF (1996) Basic Horticultural Statistics for the United Kingdom, Calendar and Crop Years 1985-1995, MAFF. MAFF (1998) Basic Horticultural Statistics for the United Kingdom, Calendar and Crop Years 1986-1996, MAFF. Malumphy, C., Collins, D.W., Boonham, N. & Walsh, K.J. (2004) Identification of early larval instar and adult Bemisia tabaci and other whiteflies moving in

plant trade. Proceedings of the 2nd European Whitefly Studies Network Symposium, Cavtat, Croatia 5-9 October, 2004. Martin, J.H. (1987) An identification guide to common whitefly pest species of the world (Homoptera: Aleyrodidae). Tropical Pest Management, 33, (4), 298- 322. Martin, J.H., Mifsud, D. & Rapisarda, C. (2000) The whieflies (Hemiptera: Aleyrodidae) of Europe and the Mediterranean basin, Bulletin of Entomological Research, 90, 407-448. Mound, L.A. & Halsey, S.H. (1978) Whiteflies of the world, a systematic catalogue of the Aleyrodidae (Homoptera) with host plant and natural enemy data. British Museum (Natural History), London, 340pp. Nair, M.R.G. (1986) Insects and mites of crops in India. Indian Council of Agricultural Research, New Dehli, 408pp. Nelson, D., Hatt, G., Nelson, C. & Bedford, I.D. (2004) Trialeurodes ricini (Misra): A begomovirus vector? Proceedings of the 2nd European Whitefly Studies Network Symposium, Cavtat, Croatia 5-9 October, 2004. Patel, M.M., Naik, M.M., Vyas, H.N. & Patel, A.T. (1986) Evaluation of certain insecticides against whitefly (Trialeurodes ricini Misra) and jassid (Empoasca kerri Pruthi) infesting castor. Indian Journal of Plant Protection, 14, (1), 81- 82. de Rougemont, G.M. (1989) A field guide to the crops of Britain and Europe, Collins, London, 367pp. Shishehbor, P. & Brennan, P. A. (1995) Environmental effects on pre-imaginal development and survival of the castor whitefly, Trialeurodes ricini Misra Insect Science & its Application. 16, (3/4), 325-331. Shishehbor, P. & Brennan, P.A. (1996a) Life history traits of castor whitefly, Trialeurodes ricini Misra (Hom, Aleyrodidae), on eight host plant species, Journal Of Applied Entomology, 120, (9), 519-522. Shishehbor, P., Brennan, P.A. (1996b) Adult longevity, fecundity, and population growth rates for Trialeurodes ricini misra (Homoptera: Aleyrodidae) at different constant temperatures. Canadian Entomologist, 128, (5), 859-863. Shishehbor, P. & Brennan, P.A. (1996c) Parasitism of the castor whitefly, Trialeurodes ricini (Homoptera: Aleyrodidae) by Encarsia formosa (Hymenoptera: Aphelinidae): Bionomics in relation to temperature. Bulletin of Entomological Research, 86, (1), 67-72. Shishehbor, P. & Brennan, P.A. (1996d) Functional response of Encarsia formosa (Gahan) parasitizing castor whitefly, Trialeurodes ricini Misra (Hom, Aleyrodidae) Journal Of Applied Entomology, 120, (5), 297-299. Vora, V.J., Bharodia, R.K. & Kapadia, M.N. (1984) Pests of oilseed crops and their control - castor. Pesticides, 18, (11), 3-5

Name of pest risk analyst: Alan MacLeod Address: Central Science Laboratory, Sand Hutton, York, YO41 1LZ, UK. Date: September 1997 December 1998 (revised and updated) December 2000 (updated with information about spread to the Canary Isles) January 2002 (reformatted for EPPO Phytosanitary Measures Panel). January 2004 (interception added)

January 2005 (interceptions added, notes from 2nd EWSN symposium added [taxonomin research / virus transmission research] ). Registered file: PPH 2497

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