8 FAO PLANT PROTECTION BULLETIN

Distribution of the PsylHd Vectors of Citrus Greening Disease, with Notes on the Biology and Bionomics of Diaphorina citri.·

H.D. .Catling, Malkerns Research Station, Malkerns, Swaziland

In 1968, the author, under the auspices of The two main vectors responsible for green­ FAD, assisted the Philippine Bureau of Plant ing disease are Trioza erytreae (Del G.) and Industry in initiating research on the Oriental Diaphorina citri (Kuw.). insect vector of citrus greening disease. Sur­ veys vI/ere carried out in the Philippines on Distribution of Trioza erytreae the distribution of the vector, and observa­ tions on symptoms in declining citrus groves In 1965, McClean and Oberholzer (22) prov­ were made during short visits to Hong Kong, ed that greening in South Africa is transmitted Thailand, India and Nepal. by the psyllid T. er.vtreae. This vector is restricted to Africa south of the Sahara (see Figure 1), and has also been recorded in Mad­ Greening diseases agascar (3), Mauritius (26), Reunion (4, 26) and Saint Helena (15). It is suspected to occur In the last three decades a number of closely in Angola,l and has been observed by the author related citrus virus diseases have appeared in in Rhodesia, and in Swaziland (10). most regions of the world where citrus is grown. A number of workers now believe that the greening disease of South Africa, leaf mottling Distribution of Diaphorina citri of the Philippines, and much of the citrus It has been shown conclusively that the dieback in India are caused by one and the psyllid D. citri, is the main vector of greening same virus. It is also becoming increasingly disease in Asia and the Far East. In 1965 clear that the stubborn disease of America, Tirtawidjaja et al. (34) demonstrated that the vein-phloem degeneration of Indonesia, yellow vein-phloem degeneration disease of Indonesia shoot of China (Mainland), and likubin of is transmitted by D. citri. Salibe and Cortez China (Taiwan) are very similar to greening. (28) published preliminary evidence that D. Results described in this paper tend to support citri is the vector of Philippine leaf mottling this view. and this was later confirmed by Celina et al. Excellent descriptions of the symptomology (14) and Martinez and Wallace (21). In India. of greening, leaf mottling and stubborn disease Capoor et al. (6) have shown convincingly may be found in recent papers (5, 21, 23, 28). that D. citri is an efficient vector of greening. In the field, however, particularly in Asia and Figure I and Table 1 show that D. citri is the Far East, recognition of the disease from widely distributed in the Orient and is present symptoms alone is often difficult. Very sim­ in Brazil. The vector occurs in the Ryukyu ilar leaf symptoms may be caused by a wide archipelago (24) but as far as can be ascer~ variety of factors varying from nutritional tained it has not been recorded in Japan. disorders to the presence of other diseases such Greening-like diseases have been reported from as root rots and gummosis, and even other 11 out of the 15 countries where this vector virus diseases such as tristeza and exocortis. is known to occur on citrus. Furthermore, Hence, tissue graft and insect transmission studies are often necessary before a reliable 1 Eastop. V.F. 1969. Personal communication (spec­ diagnosis can be made. imens in the British Museum). PLANT PROTECTION BULLETIN 9 ~~~~~~~~~~~~~~~~----,~,.,'--

-T. ~ytreae ~-- D.citri

Figure I. Distribution of Trioza erytreae and Diaphorina cUn. (From Map No. 234, Commonwealth Institute of Entomology) the disease is suspected in Malaysia and Hong D. citri was collected by the author in the Kong and there is a strong possibility that it Philippines, China (Taiwan), Hong Kong, Thai­ is present in Burma and Pakistan - especially land and Nepal, and he has since received in West Pakistan bordering the Indian Punjab. specimens from Brazil and Reunion. Both D. citri and T. erytreae occur in Reunion and TABLE 1. - DISTRIBUTION OF D. citri AND THE PRESENCE Mauritius. OF GREENI;\IG-L1KE DISEASES OF CITRUS

Country Greening-like diseases Surveys for D. citri and greening in the Philippines

Burma (16) Surveys were carried out by two methods, Ceylon (35) Greening (26) depending mainly on the size of the grove China (Taiwan) (19) Likubin (5, 31) selected. In most large groves, 50 to 200 India (16, 19) Greening (17) flushes were examined for eggs and young Indonesia (16, 19) Decline (32), vein-phloem stages of the insect with a hand lens either degeneration (34) Asia in situ or after removal from the trees (sur­ East and West Pak- istan 1 (19) veys). In small or backyard groves, or where Hong Kong (30) Probable greening (8) trees were semidormant, a rapid search was Malaysia (16) Possible greening 2 made, lasting 10 to 20 minutes or until the Nepal l Greening (9) vector was discovered (spot checks). The rate Philippines (16, 19) Greening (leaf mottling) of discovery was taken as a measure of (21, 28) prevalence. Mauritius 1 (26) Greening (26) Greening was identified mainly by leaf and { Reunion (4) Greening (4, 26) fruit symptoms. In addition, a small number Stubborn (5), probable { Brazill (20) greening (27) of fruit and bark samples were taken from diseased trees for indexing by the fluorescent 1969. Personal communication (spec- test of Schwarz (29). ~~r~~;~:~t~!r!~~'~Ulll). - 2 Chiarappa. L. 1968. Per- The results are summarized in Table 2. 10 FAa PLANT PROTECTION BULLETIN

TABLE 2. - SURVEYS AND SPOT CHECKS FOR D. citri IN CITRUS GROVES IN THE PHILIPPINES DURING JULY AND AUGUST 1968 Surveys Spot cllccks

Region Province 'I-:N~mber I Number 1 Number I Percentage Number of groves of groves Iof flushes of flushes of spot Number surveyed infested examined infested checks infested

Batangas I" 11 11 1 100 I 35.9 I 7 6 Southern Cavite Tagalog 2~ 2~ 2~ 2;:~ I Laguna I Quezon i Albay 5 4 350 I 42.6 7 7 Bicol Camerines Norte 4 o 230 0.0 5 o Camerines Sur 4 3 250 8.4 11 8 Sorsogon 1 I 50 36.0 I 1

Mindoro Oriental 4 o 600 0.0 3 o

Cotabato 4 2 400 20.8 4 2 Mindanao Davao de Sur 2 1 150 10.0 5 1 Davao Oriental 3 1 250 27.6 3 1 Northern Benguet o 100 0.0 3 o Luzon La Union 2 1

Southern Tagalog. With one exception, D. in the season for a valid comparison of fruit citri was fairly abundant in all groves searched symptoms, but it would appear that they are in this region. Centered in Batangas prov­ not reliable in mandarins. No definite marker ince, this is the oldest and formerly the most substance was found in two fruit samples from important citrus-growing area in the Philip­ diseased Ladu mandarins, but a bark sample pines. Since the rampant spread of the dis­ from the same trees was clearly positive for ease in the late 1950s, however, more than greening. Greening symptoms were also ob­ a million trees have died and the 1968 crop served in several neglected Valencia trees in was estimated at about one tenth of that Batangas, three fruit samples showing low harvested in 1960. Since much of the prop­ concentrations of marker substance and a agative material used in other citrus areas single bark sample again being clearly positive, originated from Batangas, the disease has Bicol and Mindoro. Table 2 shows that the probably been inadvertently introduced into vector was common in the Bicol region, with most of the recognized citrus areas of the the exception of Camarines Norte, but was Philippines. not found in seven groves in Mindoro Orien­ Disease symptoms were found in every grove, tal. It is possible, however, that further search most trees showing severe decline, with the would reveal its presence in these areas. Scat­ exception of the Rosario/Padre Garcia area, tered leaf symptoms were observed in both where trees continue to bear and grow well. regions but in only three groves could this Apart from the absence of vein-yellowing, be associated with greening. In one grove there was a striking resemblance between leaf in Mindoro there was evidence that the dis­ symptoms and general tree appearance of man­ ease had been introduced with propagative darins in Batangas (mainly Ladu and Szin­ material from Batangas. kom varieties), with greening-affected sweet Mindanao and northern Luzon. The vector orange trees in South Africa. It was too early was present in most groves examined in Min- PLANT PROTECTION BULLETIN 11 danao and in one in northern Luzon. Very to trees examined in the Philippines. As in few symptoms were observed in either region. South Africa and the Philippines, lemons and The vector is thus widely distributed in the limes at Pokhara were only slightly affected Philippines and the potential exists for green­ by the disease and were still growing and ing to spread to most of the citrus-growing bearing well. The vector is also reported to areas. Fortunately, diseased groves outside of be present in the eastern terai (belt of marshy the severely affected Batangas areas appear to jungle between the foothills and the plains) be relatively few and are isolated. from where leaf symptoms have been noted. There is evidence that greening-infected ma­ terial has been introduced into Nepal from Surveys in other countries Uttar Pradesh, India. Hong Kong. D. citri was found in one of the three groves visited in 1968. During Notes on the biology of D. citri another visit in 1969 fairly conclusive greening symptoms were observed in sweet orange, From the literature, it appears that there mandarins and pomelos. has been little or no further study on the biol­ Thailand. Low populations of D. citri were ogy or ecology of D. citri since the work of found in two out of six groves in the Chan­ Husain and Nath in India in 1927 (19), who taburi district. Specimens in the insect col­ also included a detailed description of all lection of the Plant Industry Division indicate stages of the insect. The following notes, that the vector is widespread in Thailand. mainly from observations in the Philippines, No greening symptoms were evident in the are intended to supplement the above paper young citrus area of Chantaburi but the dis­ and are in general agreement with it. ease has been observed in other parts of the Figure 2, drawn from specimens freshly pre­ country (33). served in alcohol, shows the egg, five nymphal India. D. citri was not found in any of instal'S, and an adult female of D. citri. In the three groves visited but greened trees were the insectary, in July/August, at a mean tem­ seen at the Indian Agricultural Research Insti­ perature of 25-26°C, there was a daily egg tute, New Delhi. At Poona Agricultural Col­ production of 8.0 eggs, a mean incubation lege and in a nearby grove, severely affected period of 3 days, and nymphal development sweet orange trees were observed with the full was completed in 11 to 15 days (based on 32 syndrome of the disease. One fruit sample reared adults). The mean preoviposition pe­ was found to give a strong positive response riod of 5 females was 12 days. In Batangas, to the albedo-fluorescence test. the mean colony size per flush point was 7.8 Nepal. The vector was not observed in individuals comprising 4.5 eggs and 3.3 nymphs. Katmandu valley, and all trees appeared free Although larger colonies were observed on from greening. In the Pokhara vaHey, where some occasions, and in Camarines Sur one a virulent strain of greening has caused a se­ isolated colony was found with 160 fourth vere decline of citrus, three out of six sites and fifth-instar nymphs and 25 adults, in gen­ were infested with D. citri. At the Pokhara eral, colony size was small at this time of the Research Substation, the complete syndrome of year. Fecundity and colony size are reported the disease was observed. Sweet orange trees to be far greater on the first flush cycle at the showed abundant leaf mottling or "french­ start of the rainy season. In a group of 518 " vein-yellowing, and lopsided fruit with adults investigated, 44.8 percent were males. aborted seeds, and two fruit samples D. citri was observed on sweet orange, man­ high concentrations of the greening darins, lemons, limes, pomelos and calamon­ substance. Mandarins showed iden­ dins (Citrus X Fortunella hybrid), and heavy leaf symptoms and general tree appearance populations may cause blossom and fruitlet 12 FAD PLANT PROTECTION BULLETIN

Figure 2. Egg, five nymphal instars and adult female of Diaphorina citri. PLANT PROTECTION BULLETIN 13

in the Philippines. 2 The insect also at­ species and varieties also affect population a wide range of rutaceOllS plants and has dynamics (l0). recorded on five different genera of this Natural enemies. Several species of inter­ in India and southeast Asia. The Phil­ nal parasites, at least two of which are probably flora is rich in Rutaceae and there is hyperparasites, were reared from D. cUri nymphs that in some areas the insect has collected in the Philippines. The three main spread to citrus from alternate hosts. species were: (a) ?Psyllaephagus sp. (Encyrtidae) females, from Batangas, Bicol and Mindanao; (b) JI,Jarietta nr exitiosa Compere (Aphelinidae) Bionomics of D. citri from Batangas; (c) Aphidencyrtus sp. (Encyr­ tidae) from Batangas. Psyllids are known to undergo violent fluc­ Of 147 parasites reared, 51.7 percent were tuations in numbers. Owing to their high ? Psyllaephagus sp., which appears to be the fecundity and short life cycle they are able most common primary parasite in the Philip­ to multiply very fast to exploit their environ­ pines. This has been recorded from China 4 ment when limiting factors are relaxed. From (Taiwan) by Dr. B.D. Burks of the U.S. field studies in South Africa, Catling and National Museum, Washington, D.C. 25.2 per­ Annecke (7) found that the main factors reg­ cent were lIfarietta Dr exitiosa, which is ulating populations of T. erytreae were flush­ probably the main hyperparasite, and 17.0 ing rhythm of citrus, flush quality, extremes of percent were Aphidencyrtus sp. weather, and natural enemies. The possible The external eulophid parasite Tetrastichus importance of such limiting factors in the pop­ radiatus Waterston was not found during the ulation dynamics of D. cUri will be discussed field surveys, nor has it been recorded in the briefly in the light of preliminary observations Philippines (2). This species has been reported in the Philippines. as an effective parasite of D. cUri in India (18) and attacks T. erytreae in South Africa (11). Flushing rhJ·thm. The population fluctua­ It is, therefore, a candidate for introduction tions of psyllids breeding on citrus are closely into the Philippines. correlated with flushing rhythm (10), because In addition, syrphid larvae, a neuropteran eggs are laid exclusively on young flush points nymph and a coccinellid larva were found and nymphs develop on immature leaves. associated with D. citri nymphs on several Populations of D. citri in Batangas are at their occasions. lowest on semidormant trees during the dry Extremes of weather. Extremes of weather season from December to April.:J The main were found to playa dominant role in regulat­ upsurge in numbers takes place during the ing the numbers of T. erytreae (12); further evi­ main flush cycle in May/June, which is stirnu- dence of this is provided by the laboratory by the first rains. Moderate populations studies of Moran and Blowers (25). Mortality observed by the author during July and of the highly sensitive egg andfirst-instar nymph 1968. stages was closely associated with high tem­ The heavy and prolonged flushing of young perature and low relative humidity. However, makes them very attractive to the vector; it appears that D. cUri is more resistant to partly explains the rapid spread of green­ extremes of weather than T. erytreae. In in replanted groves. At Lipa (Batangas) Reunion, fairly high populations of D. cUri Pokhara, healthy replants had become were observed in the hot coastal zone, whereas lnlcclted in three to four months. Pruning T. erytreae was confined mainly to cooler be carefully timed so as not to stimulate areas above 500 to 600 metres (4). In equa- flushes which may be rapidly by the vector. Differences in the "Celino. C.S. 1968. Personal communication. "Celino. C.S. 1968. Personal communication. flushing rhythm of various citrus 1 Annccke. D.P. 1969. Personal communication. 14 FAO PLANT PROTECTION BULLETIN -----~_._--~----_._._.--_._------torial regions, such combinations of tempera­ be effectively controlled with a wide range of ture and humidity are rare. An examination modern insecticides. This is also true of T. of meteorological data for the driest citrus area erytreae, concentrations of dimethoate as low of the Philippines, Batangas, revealed that the as 0.0025 percent active ingredient having provo daily maximum saturation deficits for the hot­ ed effective against eggs and nymphs (13). test days during the 1968 dry season were In a small field test in the Philippines, dime­ considerably below the critical level of 26 mil­ thoate at 0.0075 percent active ingredient gave limetres Hg (34.6 mbars), a value used in a 79 percent kill of D. citri nymphs despite predicting population densities of T. ery­ the occurrence of heavy rain two hours after treae (12). spraying. It is important that the natural balance of beneficial insects is not disturbed when chemical measures are used. Low con­ Control of D. citri centrations of fairly safe systemics, such as dimethoate or demeton methyl, should be ap­ The insect is widely distributed and well plied at the first signs of a buildup of nymphs adapted in the profusion of small" plantings on a new growth cycle. and backyard trees which characterize most citrus areas of the Orient. It has been collect­ ed on a wide range of alternate host plants Acknowledgements from which it could reinfest sprayed groves. It would therefore seem that there is little The author is greatly indebted to the many prospect of eradicating D. citri in these coun­ people who collaborated with him during this tries. assignment. Special thanks are due to the There is, however, evidence that fairly high staff of the Lipa Experiment Station, Batangas. vector populations are needed before signifi­ Philippines, and particularly to his counter­ cant transmission of the disease will occur. parts C.S. Celina, entomologist; R. E. Cortez, In South Africa it is also believed that adults plant pathologist; CJ. Gonzales, horticultur­ colonizing the spring flush cycle, which have ist; and D.R. Panaligan, junior plant pathol­ previously fed for long periods on mature ogist. leaves containing high concentrations of virus, He is also grateful to Dr. R.E. Schwarz of are particularly infective (13). This means that the Citrus and Subtropical Fruit Research the prevention of high populations .... espe­ Institute, Nelspruit, South Africa, for the cially on the first flush cycle at the start of the fluorescence tests, and to Dr. D.P. Annecke season· may be extremely important in check­ of the Plant Protection Research Institute. ing the spread of the disease. Pretoria, South Africa, for the identification Many workers have shown that D. citri can of parasites.

LITERATURE CITED

1. ANONYMOUS. 1965. A host list of the insects of 5. CALAVAN, E.C. 1968. A review of stubborn and Thailand. Dept. Agric. Royal Thai Govt. and greening diseases of citrus. In Childs, J.F.L., ed. U.S. Operations Mission to Thailand. Proc. 4th Conf Int. Org. Citrus Virol., p. 105-117. 2. BALTAZAR, R. 1966. Pacific insects. Monograph Univ. Florida Press. Gainesville. No.8. Honolulu, Hawaii. Ent. Dept. Bernice 6. CAPOOR, S.P., D.G. RAO and S.M. VISWANATH. P. Bishop Museum. 1967. Diaphorina cUri Kuway, a vector of the 3. BovE, J. and J. CASSI:-';. 1968. Problems of agri­ greening disease of citrus in India. Indian J. culture: report on a survey in Madagascar. Ver . agric. Sci., 37:572-576. sailles, IFAC-CNRA (Mimeograph) 7. CATLlNG, H.D. and D.P. ANNECKE. 1968. Ecol­ 4. BovE, J. and J. CASSIN. 1968. Problems of ogy of citrus psylla in the Letaba district of north­ agriculture: report on a survey in Riunion. Ver­ ern Transvaal. S. African Citrus J., 410:8-11, sailles, IFAC-CNRA (Mimeograph) 14, 15, 17. PLANT PROTECTION BULLETIN 15

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