RUST MITE ON CITRUS DAMAGE CAUSED BY ACULUS PELEKASSI KEIFER, A BURDITT AND REED: RUST MITE 41. for lemonade. Rumpled fruits can also be used

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1 BURDITT AND REED: RUST MITE 41 Microscopic examinations of affected rind have so far failed to demonstrate a culpable microorganism, and isolations yield only the fungi usually found on fruits as surface con taminants. used safely in the making of frozen concentrate for lemonade. Rumpled fruits can also be used for the recovery of oil since, for all practical purposes, the resulting product is not affected in quality or yield. Control Though rumple causes no harm to lemons destined for the canning plant, it must be con trolled if lemons are to be sold as fresh fruit. Rumple may be avoided by picking fruits while still immature. This practice should work no hardship; rather it is to be preferred since 1) it provides small-sized fruits that are so popular with the housewife, and 2) it yields lemons that, when properly cured, are more resistant to stor age breakdown. These remedies will enable the lemon grower to cope with rumple until such time as the cause of rumple is established and the disease can be prevented. Conclusion Rumple is a rind breakdown that disqualifies lemons for the fresh-fruit market. However, fruits affected by either the first or second stage of rumple, as described in this report, can be Acknowledgments The authors are indebted to Minute Maid Corporation for providing the land, grove care, and help needed in operating the varietal lemon trials at Avon Park. To Dr. A. E. Willson, Vice President, Research and Development Division, acknowledgment is made for assistance in analyz ing the data on yield. To Mrs. Harriet Long, ap preciation is expressed for providing photographs A, B, and D. LITERATURE CITED 1. Fawcett, H. S Citrus diseases and their control. McGraw-Hill Book Company, Inc., New York. 656 p. 2. Haas, A. R. C The relation of phosphorus to creasing and puffing in Valencia oranges. California Citrograph 35: , Klotz, L. J Color handbook of citrus diseases. University of California Press, Berkeley. 75 p. 4. Knorr, L. C Finding the best lemon for Florida a report of progress. I. The growing of lemons in Florida: Historical, varietal, and cultural considerations. Florida State Horticultural Society Proceedings 71: Knorr, L. C Selecting lemons for Florida production. Florida Agr. Exp. Stas. Ann. Rept., p Russo, F. and L. J. Klotz Wrinkle rind of lemons in Sicily. California Citrograph 48: 264. DAMAGE CAUSED BY ACULUS PELEKASSI KEIFER, A RUST MITE ON CITRUS A. K. Burditt, Jr., and D. K. Reed Entomology Research Division Agric. Res. Serv. U.S.D.A. Orlando In 1961 a second species of rust mite, Aculus pelekassi Keifer, was found on citrus in Florida (Burditt et a., 1963). Inspectors from the Flor ida Division of Plant Industry initiated surveys for this species in April 1962 (Denmark, 1963) and found it in over 50 citrus nurseries in the northeastern and central part of the State. A. pelekassi was also found in a few citrus groves, generally in mixed populations with the citrus rust mite (Phyllocoptruta oleivora (Ashmead)). A. pelekassi has been reported from Greece, Thailand, Japan, Italy, and Sicily (Keifer, 1962). C. A. Fleschner (Keifer, 1959) stated that dam age to mandarin (Citrus reticulata) "was the most severe case of citrus rusting he had ever seen." However, in a discussion of the subject in December, 1962, Fleschner indicated that both A. pelekassi and P. oleivora were present and that he was not sure which species caused the rusting. Distortion of leaves on terminal growth of citrus seedlings, first observed in laboratory colo nies of rust mites at the Horticultural Field Sta tion of the U.S.D.A., Orlando, Florida, late in 1961, was subsequently associated with large populations of A. pelekassi under greenhouse con ditions (Burditt, 1963). This type of injury first appeared as a crinkling of infested leaves, but in severely damaged leaves the sides were twisted inward. Such damage could easily be distin guished from aphid injury, which causes the ends of the leaves to be coiled in a spiral form. How ever, injury caused by A. pelekassi may be con fused with symptoms of some virus diseases of

2 42 FLORIDA STATE HORTICULTURAL SOCIETY, 1963 citrus, such as infectious variegation (Petri, 1931, Fawcett and Klotz, 1939) or tatter leaf (Wallace and Drake, 1962). Field Observations of Aculus pelekassi Damage On March 29, 1963, leaves on ten terminal branches on each of three orange trees at the Horticultural Field Station were infested with mites from a laboratory colony of A. pelekassi by tying infested seedlings to the terminal branches. Leaves on.a similar number of termi nals were infested with mites from a colony of P. oleivora. Only a few mites transferred from the infested seedlings to the terminal leaves, ap parently because the roots of the seedlings had been placed in a plastic bag so that the seedlings wilted very slowly. The infested terminals were examined on April 16, May 20, and June 10. These observa tions showed that 12, 27, and 77%, respectively, of the leaves were infested with rust mites on terminals that had been originally infested with A. pelekassi, and that 19, 47, 87%, respectively were infested with rust mites on terminals that had been originally infested with P. oleivora. In June, sampling showed that of 402 mites from terminals infested with A. pelekassi, only 36 were this species, the remaining 366 mites being P. oleivora. A pelekassi was found on only 8 of the 26 terminals examined. Of 420 mites from terminals infested with P. oleivora only 1 was A. pelekassi. On July 9, all leaves examined were infested with rust mites. But A. pelekassi was found on only 6 of 31 leaves from terminals infested with A. pelekassi and constituted only 5.3% of the 620 rust mites examined. Observations on May 20, 1963 of terminals infested on March 29 with A. pelekassi showed some leaf distortion and many brown lesions on the lower surfaces of leaves of two terminals. Such lesions were reported to the author by H. A. Denmark in April, 1963, as having been ob served by nursery inspectors from the Florida Division of Plant Industry. The lesions apparent ly resulted from feeding by large numbers of mites along the veins on the lower surfaces of immature leaves. As the leaves matured, the lesions developed. These lesions, scattered over the leaf surfaces, were associated with small veins in the leaf (Fig. 1). This type of damage has been observed on Cleopatra mandarin and Columbia sweet lemon seedlings infested with A. pelekassi in air-conditioned greenhouses but not on other types of citrus seedlings. Brown areas along the midribs on upper surfaces of these leaves were also observed. These areas were associated with feeding by large numbers of A. pelekassi along the midribs. This type of damage was usually found on leaves with brown lesions on lower surfaces. On May 22, 1963, ten oranges on each of two orange trees at the U.S.D.A. Horticultural Field Station were infested with A. pelekassi. Infested leaves from the greenhouse colony were pinned to the stem near each fruit. Mites readily trans ferred onto the fruit as infested leaves dried out. Within 3 weeks there were high populations (in excess of 100 mites per fruit) on 11 of 19 oranges remaining on the two trees. Of 138 mites ex amined on June 11, 90.6% were A. pelekassi. P. oleivora was found on only 3 of the oranges. On July 8, P. oleivora was found on 16 and A. pelekassi on 11 of the oranges originally infested with A. pelekassi on May 22. Of 213 mites ex amined on July 8, 39.5% were A. pelekassi. Twenty-six naturally infested oranges on these two trees were examined on June 12 and again on July 11. All 423 mites examined on July 11 were P. oleivora. Twelve naturally in fested oranges (46%) showed varying degrees of russet, compared with 9 oranges (47%) in fested with A. pelekassi. Oranges were rated for estimated populations of rust mites present, with zero for no mites, 1 for 1-25 mites, 2 for Figure 1. Sweet orange leaves following: feeding by large numbers of rust mites.

3 BURDITT AND REED: RUST MITE 43 Table 1. Populations of A. pelekassi on citrus seedlings. Type of Seedling Rating of 2 weeks mite population (weeks k weeks Lower after infestation) 1/ 9 weeks Middle Upper Stem Trifoliate Troyer Temple 2.4 2/ Columbia 1.4 Cleo 1.4 Murcott Duncan Key lime 0.9 Sour l/ Classification used for rating mite population: 2 = , 3 = = no mites, 1 = 1-25, 2/ Defoliated due to feeding by mites. mites, 3 for mites, and 4 for over 500 mites per orange. Naturally infested oranges had an average rating of 2.85 compared with 2.95 for oranges infested with A. pelekassi on May 22, a nonsignificant difference. Greenhouse Observations op Aculus pelekassi Leaf distortion caused by feeding of large populations of A. pelekassi has been observed repeatedly under greenhouse conditions. Field infestations of A. pelekassi were first detected at the U.S.D.A. Foundation Farm near Leesburg after observation of distorted terminal leaves similar to that observed in greenhouses. This type of damage has resulted in finding infesta tions of A, pelekassi in many citrus nurseries. A laboratory experiment was undertaken to determine differences in population buildup of A. pelekassi and P. oleivora and to evaluate the type of damage to different varieties of citrus. Citrus seedlings germinated and grown in an insectary were infested with between 10 and 20 rust mites from greenhouse colonies of A. pelekassi or P, oleivora. These plants were placed in screen cages in an air-conditioned green house where the temperature was maintained be tween F. and humidity fluctuated between 40 and 95% R. H. Counts were made of the number of mites on each plant 2 weeks after infestation. These counts (Table 1) showed a large buildup of populations of A. pelekassi on Temple orange, trifoliate orange, Troyer citrange, Columbia sweet lemon, Murcott Honey orange, and Cleo patra mandarin seedlings, but Sour orange, Key lime, and Duncan grapefruit had lower popula tions of mites. Two weeks later the infestation of A. pele kassi remained low on Sour orange and the plants showed no damage (Fig. 2). Key lime seedlings had light to moderate infestations of mites but no apparent damage (Table 2). Duncan grapefruit seedlings had light to heavy infestations of mites but no damage symptoms typical of those ob served from A. pelekassi feeding.

4 44 FLORIDA STATE HORTICULTURAL SOCIETY, 1963 Figure BQUft ' DUJNCAN KEY Figure 2. Citrus seedlings showing little or no injury from A. pelekassi feeding for 6 weeks. Most of the remaining six types of seedlings were heavily infested with populations of A. pele kassi. Several types of symptoms were observed that could be related to feeding by A. pelekassi (Fig. 3). Symptoms on Columbia, Cleo, and Murcott seedlings consisted of a distinct downward cupping of the leaves with attendant chlorotic appearances. In Murcott, this cupping effect was found only on the older leaves, but younger leaves were curled and distorted as reported earlier (Burditt et al.t 1963) (Fig. 4). Columbia and Cleo seedlings, in addition to the cupping effect, had brown lesions on the undersides of the leaves similar to those described from field observations. These were the only seedlings that exhibited such symptoms within 4 weeks of in festation with A. pelekassi. Symptoms on trifoliate and Troyer consisted of an upward lengthwise rolling of the immature leaves. A. pelekassi built up to very large popu lations on Temple seedlings, which displayed the most serious damage. Leaves turned a silvery color, curled downward from the tip, showed mesophyll collapse, became necrotic, and soon dropped from the plants. Injury on Temple seed lings was similar to that caused by heavy popu lations of spider mites on citrus. In nearly all instances of very heavy infesta tions on leaves of other types of seedlings, there was some mesophyll collapse or chlorosis of those particular leaves, but such symptoms were not as severe as those shown by Temple seedlings within 4 weeks of infestation. Observations of seedlings infested with citrus rust mites (P. oleivora) for 2 and 4 weeks showed that populations of this species increased as rapidly as did those of A. pelekassi (Table 3), but there was no leaf damage to the seed lings from feeding by P. oleivora. Populations of P. oleivora were slightly higher on Duncan grapefruit, Foster grapefruit, Sour orange, Navel orange, Pineapple orange, Florida sweet orange, Jaffa orange, and Columbia sweet lemon seedlings than on Temple, Cleo, or Murcott seedlings. Popu lations of this species were low on trifoliate, Troyer, and Key lime seedlings. Discussion The studies reported in this paper have shown that A. pelekassiy a second species of rust mite

5 BURDITT AND REED: RUST MITE 45 Table 2. Injury observed on citrus seedlings associated with infestations of A. pelekassi. of Interval after infestation Seedling b weeks 13 weeks Trifoliata Leaves curled lengthwise and up* Damaged leaves abscised. Troyer Leaves curled lengthwise and up. Damaged leaves remained. No new foliage. Temple Whitening of leaves, downward curl, necrosis, abscission. Complete defoliation. Columbia Downward cupping of leaves. Same as 6 weeks with some defoliation. Cleo Downward cupping of leaves. Same as 6 weeks. Terminal stunting. Terminal witches broom, "V" shaped necrotic area on leaf tips. Murcott Twisted and distorted leaves Damaged leaves abscised. New growth distorted. Duncan Slight terminal stunting. Black characteristic lesions. Terminal stunting. Lack of new growth. Key lime "V" shaped necrotic tips of leaves Witches brooms and leaf axis. on terminal Sour None Terminal stunting, lack of new growth. attacking citrus in Florida, is capable of causing severe damage to citrus. Under field conditions, feeding by these mites may result in severe dis tortion of smaller young leaves and some distor tion and brown lesions on larger immature leaves. Large populations of mites are able to build up in 3 to 6 weeks on nursery trees and on young terminals and water-sprouts of mature trees. Mites are capable of surviving on mature leaves but do not reproduce very rapidly and appear to be unable to compete with P. oleivora on these leaves. A. pelekassi is the dominant species on immature leaves and P. oleivora on mature leaves of citrus. Limited studies have shown that A. pelekassi will feed on citrus fruit and is able to build up to high populations within 3 weeks. Feeding by A. pelekassi will cause russet of fruit and this russet may be more severe than that caused by P. oleivora. Greenhouse studies of A. pelekassi show that there are differences in susceptibility of varieties of citrus seedlings to A. pelekassi attack. Sour orange is not a favored host for A. pelekassi in air-conditioned greenhouses. Key lime and Dun can grapefruit sustain these mites, but A. pele kassi does not build up on these seedlings as rapidly as on other types of citrus. Murcott Honey orange and Temple orange seedlings were favored host plants and more susceptible to dam age from this species of rust mite. Populations of A. pelekassi increased more rapidly on tri foliate and Troyer than did those of P. oleivora. Summary Field and greenhouse studies of two species of rust mites on citrus have shown that Aculus pelekassi is potentially capable of causing more severe damage to citrus than is Phyllocoptruta oleivora, the citrus rust mite. A. pelekassi causes

6 46 FLORIDA STATE HORTICULTURAL SOCIETY, 1963 MURCOTT TEMPLE TRIFOLIATA COLUMBIA Figure 3. Citrus seedlings showing various types of injury from A. pelekassi feeding for 6 weeks. Figure 4. Close up of leaf distortion from feeding by A. pelekassi on Murcott Honey orange seedling.

7 BURDITT AND REED: RUST MITE 47 Table 3. Populations of P. oleivora on citrus seedlings. Type of Seedling Rating of mite ] Dopulation 2 weeks i 4- weeks (weeks Lower after infestation) 1 / 9 weeks Middle Upper Stem Duncan 2.2 Navel Foster 2.2 Fla. Sweet Temple 2.k 2.k Sour 2.1 Columbia Jaffa Pineapple Murcott 1.4 Cleo l.k l.k- Trifoliata l.k Troyer Key lijne l/ Classification used for rating mite population: 0 = no mites, 1= 1-25, 2 =,26-100, 3 = mild to severe distortion of new growth, brown lesions on the lower surfaces and along the mid ribs of immature leaves, and may cause mesophyll collapse, chlorosis, and leaf drop. Such symp toms have not been observed in our experiments with P. oleivora. A. pelekassi is the predomin ant species on younger immature leaves and P. oleivora is the predominant species on older, more mature leaves. Both species of rust mites will attack fruit, resulting in russet. Russet of fruit fed on by A. pelekassi may be more severe than that of fruit fed on by P. oleivora. LITERATURE CITED Denmark, H. A Aculus pelekassi Keifer, another citrus mite in Florida. Proc. Fla. State Hort. Soc : Burditt, A. K., Jr., D. K. Reed, and C. R. Crittenden Observations on the mites Phyllocoptrota oleivora (Ashmead) and Aculus pelekassi Keifer under laboratory conditions. Fla. Ent. 46(1) :l-5. Fawcett, H. S., and L. J. Klotz, Infectious varie gation of citrus. Phytopathology 29: Keifer, H. H Eriophyid studies XXVIII. Occasional Papers, No. 2, Bur. Ent. Calif. Dept. of Agric. 20 pp. Keifer, H. H Eriophyid studies, B-6. Bur. Ent. Calif. Dept. of Agric. 20 pp. Petri, L Variegatura infecttiva della foglie de Citrus vulgaris Risse. Bol. R. Staz. Veg. 11: Wallace, J. M., and R. J. Drake Tatter leaf, a previously undescribed virus effect on citrus. Plant Disease Reptr. 46(4):