Proc. Fla. State Hort. Soc. 112:79-87. 1999. THE ERIOPHYOID COMPLEX ON FLORIDA (: AND DIPTILOMIOPIDAE)

C. C. CHILDERS AND D. S. ACHOR the biologies and economic importance of most of these species University of Florida, IFAS except sheldoni (Ewing) and (Ash- Citrus Research and Education Center mead). More than one eriophyoid species occurs on citrus in many 700 Experiment Station Road different geographical areas of the world including: South Africa, Lake Alfred, FL 33850 Egypt, Italy, Croatia, Australia, China, India, Thailand, Paraguay and Florida (Burditt et al., 1963; Flechtmann and Aranda, 1970; Additional index words. Citrus rust mite, Phyllocoptruta oleivora Jeppson et al., 1975; Keifer and Knorr, 1978; Hong and Kuang, (Ashmead), pink citrus rust mite, pelekassi (Keifer), cit- 1989; Kuang and Zhang, 1991; Amrine and Stasny, 1994; Boczek rus bud mite, (Ewing), frequencies, survey. and Chandrapatya, 1996). This raises further questions about the Reprinted from actual distributions of many of the listed species as well as others Abstract. Seven species of eriophyoid in two families (Ac- that likely exist in other citrus growing regions of the world, espe- ari: Eriophyidae and Diptilomiopidae) were identified from cially in Asia and Latin America. The purpose of this paper is to 64,887 slide-mounted specimens collected from 120 commer- present results of surveys conducted on citrus in Florida, discuss cial citrus groves in Florida between 1986 and 1999. Species the identification of the three main species, characterize damage, and their frequencies were: citrus rust mite, Phyllocoptruta ole- and discuss the need for monitoring and controlling the pink citrus ivora (Ashmead) (76.6%); pink citrus rust mite, Aculops pele- rust mite independently of citrus rust mite. kassi (Keifer) (22.6%); citrus bud mite, Aceria sheldoni (Ewing) (0.8%), and rare vagrant species including single specimens of Materials and Methods Acaricalus sp., sp., and sp., all Eriophy- idae and Rhynacus sp. in the Diptilomiopidae. Results from field Beginning in 1986-87, then in 1990-92, 1994-95 and 1998-99, surveys identified 22 citrus groves with citrus bud mite. Citrus several surveys of the mite fauna within different citrus grove sites rust mite was identified as the only rust mite species in 83 citrus grove sites compared with 37 sites having both citrus rust and pink citrus rust mite species. Of the 37 sites with both rust mite Table 1. Eriophyoid mites found on citrus and their geographical distribution. species, only three had higher frequencies of pink citrus rust mites. None of the 120 citrus groves sampled for eriophyoid Eriophyidae mites had only pink citrus rust mites. Pink citrus rust mites de- Aceria sheldoni (Ewing) Worldwide velop early in the Spring and are capable of moving from Aculops pelekassi (Keifer) Japan, Thailand, Paraguay, Italy, Croatia, onto very small less than 3 cm in diameter. Extensive rind Florida, Greece blemish damage from early feeding by pink citrus rust mite was Aculops suzhouensis Xin & Dong China observed in many grove sites during 1999. Early monitoring for advens (Keifer) California pink citrus rust mites is important for growers, especially in Calacarus citrifolii Keifer South Africa years following warm winter temperatures and/or dry weather in Circaces citri Boczek Thailand the Spring. Only citrus rust mite and pink citrus rust mite are Cosella fleschneri (Keifer) India currently recognized as economic pests on Florida citrus. Phyllocoptruta citri Soliman & Abou-Awad Egypt Phyllocoptruta oleivora (Ashmead) Worldwide Phyllocoptruta paracitri Hong & Kuang China The is a superfamily of mites consisting of three Tegolophus australis Keifer Australia families: Phytoptidae with 18 genera, Eriophyidae with 168 genera Diptilomiopidae and the Diptilomiopidae with 40 genera (Lindquist and Amrine, Diptilomiopus assamica Keifer India 1996). The mites are referred to as gall, rust, bud and blister mites or collectively as eriophyoids (Keifer et al., 1982). They form a significant component of the complex on citrus throughout the were conducted throughout Florida. Sampling consisted of collect- world and occur in both arid and humid citrus growing regions. ing 20 fruit from randomly selected trees within each grove site. The species complex of eriophyoid mites on citrus worldwide is di- verse, comprising at least 12 species within the families Eriophy- Each fruit within that sample was immediately agitated in a bucket containing 80% ethanol and then discarded. The alcohol wash was idae and Diptilomiopidae (Table 1). Limited data are available on then poured into a labeled jar and returned to the laboratory for pro- cessing. Between 20-50 leaves per selected sample tree were Florida Agricultural Experiment Station Journal Series No. N-01787. The au- picked from the outer canopy and washed in a manner similar to thors wish to acknowledge The Sustainable Agriculture Research and Education the fruit. Fruit and samples were collected separately and (SARE), United States Department of Agriculture and Environmental Protection stored in labeled jars containing the retained alcohol solution. Agency program, Agriculture in Concert with the Environment (ACE), The Citrus In 1990, a series of citrus groves was monitored at three differ- Production Research Advisory Council research grant, BASF Corporation, and the ent times during the Summer by collecting 20 fruit and 20 leaves Rohm and Haas Company for partial support of this research. Appreciation is ex- tended to W. P. Wergin, USDA, ARS, PSI, NL and R. Ochoa, USDA, ARS, SEL and processed as above. In addition, a field experiment, to evaluate and J. W. Amrine, Jr., University of West Virginia for their technical support and the efficacy of a miticide, was conducted in a grove at the Citrus expertise with eriophyoid mites. A special appreciation is extended to M. G. Warm- Research and Education Center in Lake Alfred, Fla. Eriophyoid ington and D. K. Threlkeld for their tireless efforts in slide mounting and sorting mite counts on fruit and leaves were taken at approximately week- mites and to T. L. Gainey for field monitoring of eriophyoid mite species. Appreci- ation is extended to J. C. Bergh and J. P. Michaud for their comments and sugges- ly intervals between April and late June from five replicated trees tions in reviewing the manuscript. per treatment. Twenty fruit were examined at random around the

Proc. Fla. State Hort. Soc. 112: 1999. 79 canopy perimeter of each sample tree at recorded time intervals. Results and Discussion Live rust mites were counted from two areas outside of the sunspot on each fruit using a 10´ hand lens equipped with a l cm 2 grid sub- Citrus bud mite-Aceria sheldoni (Ewing). The citrus bud mite divided into 4 mm 2 subunits (Childers and Selhime, 1983).Popula- (CBM) is different in appearance from both the pink citrus rust tion density estimates were obtained by counting the number of mite and the citrus rust mite. Adults and immatures are white and living motile rust mites present within the combined 2 cm2 area per 50 to 180 micrometers in length. Dorsal and ventral annuli (rings) fruit and recorded as one observation. are closely spaced and number 65-70 on the opisthosomal area of Twenty leaves from the Spring flush were picked at random the body as compared with dorsal and ventral annuli that number around the canopy perimeter of each sample tree at designated time 31 and 58, respectively for the citrus rust mite and 36 and 50, re- intervals. Each 20 leaf sample was placed in a separately labeled spectively for the pink citrus rust mite. In addition, the dorsal setae paper bag and returned to the laboratory. A stereomicroscope was of CBM are quite long compared with the other two species (Figs. used to examine a 2.25 cm 2 area on both the upper and lower leaf 1A, B). surfaces. Live motile rust mites were counted within each area on According to Jeppson et al. (1975) CBM requires about 15 both the upper and lower leaf surfaces and combined as l observa- days to develop from egg to adult during the Summer and 20-30 tion that equaled 4.5 cm 2. Samples of rust mites from both fruit and days in winter. Each female lays about 50 eggs and duration of egg leaf samples were slide-mounted for identification to species. development lasts from 2-6 days. CBM lives in sheltered places in- During 1994-95, a series of 7 selected citrus grove sites was cluding under the calyx of fruit, under bud scales, at petiole bases sampled at monthly intervals to determine the complex of mite next to buds, in developing blossoms, or in axillary buds (Boyce species present on Florida citrus. A total of 10twigs was collected and Korsmeier, 1941; Jeppson et al., 1975). Mite feeding in the ax- at random from each of 6 different trees within each grove site. In illary buds damages embryonic bud tissues (Walker et al., 1992). addition, non-replicated twig samples were collected from other Twigs, leaves, flowers and fruit that develop from damaged buds sites to determine presence or absence of citrus bud mites. The are frequently distorted. Ishaaya and Sternlicht (1969) found that twigs were collected into a labeled paper bag, placed in a cooler bud mites increased phenol concentrations in infested buds that ul- and returned to the laboratory for processing. Leaf buds were tim-ately interfered with normal development. Distorted teased apart using micro knives. Buds were examined on current leaves, shortened internodes and bunchy-type growth resulting year, first and second year wood for presence of mites between the from CBM feeding injury are shown in Keifer et al. (1982), Smith bud scales with the aid of a stereomicroscope. et al. (1997) and Searle and Smith-Meyer (1998). None of these Twenty fruit were picked at random from each of 6 trees within types of injuries has been directly attributed to citrus bud mite in- each grove site at monthly intervals and processed in 80% ethanol festations in Florida. However, presence of this mite in commercial as above. Fifty inner and 50 outer leaf samples were collected sep- citrus has been overlooked until now. arately from each of the same 6 trees and placed directly into la- CBM is considered a key pest on citrus throughout the world. beled jars containing 80% ethanol. Individual leaves were agitated It is a recognized problem in California (Jeppson et al., 1975), the in solution in the laboratory and removed from each sample jar. Mediterranean area, including Israel, Egypt, Turkey, Greece, Motile rust mite numbers per sample were counted against a black Croatia, Italy, Portugal and Spain (Mijuskovic, 1973; Talhouk, background within six randomly selected 4 cm2 gridded areas in 1975), South Africa and Australia (Schwartz and Riekert, 1967; the center of a 150 ´ 25 mm diameter Falcon Petri dish (model no. Smith et al., 1997), Chile and Argentina (Santa Maria and Brugno- 1013, Fisher Scientific, Pittsburgh, PA). Individual samples were ni, 1952; Talhouk, 1975). In California, citrus bud mite is a pest of then multiplied by 6 to estimate the total number of rust mites , Citrus limon (L.) Burmann F. in the coastal areas (Walker present within that sample. etal., 1992) whereas ‘Lisbon’ lemon is attacked more frequently in In 1999, fruit samples were collected from selected citrus Queensland, and navel oranges in New South Wales (Smith et al., grove sites and washed in ethanol as above. Sub-samples of mites 1997). Sternlicht (1969) found higher populations of CBM on lem- were removed from each sample and slide-mounted for species on followed by grapefruit in Israel. Both varieties were more sus- identification. ceptible to injury than ‘Jaffa’, ‘Valencia’ or bitter orange. In Microscopic slide mount preparation. In order to accurately Croatia, lemon was more susceptible followed by grapefruit and identify species or sexes of eriophyoid mites on citrus they must be navel orange (Mijuskovic, 1973). The only record of citrus bud properly slide-mounted. Mites in these studies were placed in Ke- mite collected in Florida was by Attiah (1959) from sweet orange ifer’s Booster solution and then slide-mounted in a modified Ber- in south Miami. lese medium for identification (Amrine and Manson, 1996). A total of 535 A. sheldoni were identified from 64,887 slide- Scanning Electron Microscopy (SEM). For typical observation mounted eriophyoid mites between 1986 and 1999. This represent- of the mites and eggs on fruit tissue, a thin slice of the fruit peel, ed less than 1% of the mites identified. However, this comparison with eggs and mites attached, was placed in 70% ethanol for 1 hr, is misleading since CBM usually are not found on twig, leaf or fruit then completely dehydrated in ethanol, followed by critical point surfaces. They congregate in protected sites as previously indicat- drying in carbon dioxide using a Ladd Critical Point Dryer. The ed. We collected CBM between leaf bud scales on wood less than samples were then mounted on stubs, coated with gold/palladium one year old, and between bud scales on 1- and 2-yr-old wood in 9 using a Ladd Sputter Coater and observed with an Hitachi S530 of 11 grove sites sampled between September 1994 and May 1995. scanning electron microscope. Using an alternative method, the A total of 347 CBM were recovered from buds on wood less than same type of samples were mounted in Tissue-Tek, frozen in liquid 1-yr-old compared with 98 and 30 CBM from buds on wood 2- or nitrogen and observed with an Hitachi S4100 equipped with an 3-yr-old, respectively. Data from 3 sites are shown in Table 2 to il- Oxford Instruments cryo stage using methods developed by Wer- lustrate their comparative numbers and seasonal occurrence. Citrus gin and Erbe (paper in progress). varieties infested with citrus bud mites in Florida included: ‘Nine pounder’ lemon, Citrus jambhiri, ‘Temple’ tangor, ‘Hamlin’, ‘Va- lencia’, ‘Ambersweet’, navel oranges, ‘Marsh’, ‘Duncan’ and

80 Proc. Fla. State Hort. Soc. 112: 1999. occurring on green wood less than 1-yr-old. Maximum numbers of CBM collected per bud were: 7 in ‘Ambersweet’ on 18 October, 5 in ‘Valencia’ orange on 25 October, 7inboth “Nine pounder” lem- on and Citrus jambhiri hybrid on 10 November, 10in‘Hamlin’ or- ange on 6 February and 10 from ‘Marsh’ and ‘Duncan’ grapefruit on 6February. Both Boyce and Korsmeier (1941) and Walker et al. (1992) found bud mites infesting buds on twigs of all ages. Infes- tations declined between buds that were on wood 3-yr-old and younger versus on wood that was 4-yr-old in California (Walker et al. 1992), suggesting that mites continually re-infest new buds as the tree grows. We collected CBM in very low numbers on leaves, twigs and fruit throughout the year or from citrus leaf buds from 22 commer- cial citrus grove sites in Lake, Polk, Hardee, DeSoto, Hendry, Col- lier, Martin, Palm Beach and Dade counties. Since the mites prefer protected sites to feed and develop, these low numbers likely reflect dispersing individuals moving to new buds or other protected sites (Table 3). Data from only a partial season have been collected. Ac- cording to Searle (1973), CBM peaks in populations are erratic and not consistent from year to year. Research is needed to determine the potential of this mite in reducing vegetative growth and yields on Florida citrus. For example, distorted flower buds are frequently observed in different citrus groves in Florida during bloom with no direct association and correspond to CBM flower bud damage shown by Phillips and Walker (1997). Pink citrus rust mite-Aculops pelekassi (Keifer). The pink cit- rus rust mite (PCRM) differs from the citrus rust mite by having a concave back (opisthosomal area) and dorsal tubercles that arise at the rear shield margin (Keifer, 1959). The dorsal setae extend be- yond the distal margin of the prodorsal shield (Figs. 2A, B). Fe- males are 140-150 micrometers in length and golden yellow to pink in color. PCRM has been collected in Japan, Thailand, Paraguay, Croat- ia, Italy, Greece and Florida (Keifer, 1959; Ciampolini and Rota, 1963; Flechtmann, 1970; Mijuskovic and Kosac, 1972; Keifer and Knorr, 1978). This mite was first discovered in Florida on calam- Figure 1. (A) Citrus bud mite in leaf bud tissue. (B) Prodorsal shield of citrus ondin in the Orlando area in 1961 (Burditt et al., 1963). The Florida bud mite with long dorsal setae evident. Division of Plant Industry initiated surveys in northeastern and central Florida in April 1962 and found PCRM in over 50 citrus mixed grapefruit varieties. Highest numbers of mites occurred be- nurseries in Alachua, Baker, Citrus, Lake, Marion, Orange, Pinel- tween September and February with maximum numbers per bud

Table 2. Occurrence of citrus bud mite, Aceria sheldoni from different citrus varieties in Florida.

Current year green wood 1 year wood 2 year wood

No. buds No. buds Total No. buds No. buds Total No. buds No. buds Total Location Variety Date examined w/ mites mites examined w/ mites mites examined w/ mites mites Pollard Marsh/Duncan 28 Sep 94 84 8 14 23 0 0 17 0 0 Pollard Marsh/Duncan 1 Nov 94 58 0 0 60 1 2 58 0 0 Pollard Marsh/Duncan 29 Nov 94 60 8 16 60 8 13 45 0 0 Pollard Marsh/Duncan 20 Dec 94 55 — 5 55 — 1 55 — 0 Pollard Marsh/Duncan 12 Jan 95 60 5 9 60 1 2 60 1 1 Pollard Marsh/Duncan 6 Feb 95 60 8 39 60 0 0 60 0 0 Pollard Marsh/Duncan 30 Mar 95 60 0 0 60 0 0 60 0 0 Pollard Marsh/Duncan 17 Apr 95 60 0 0 60 0 0 51 0 0 Pollard Marsh/Duncan 22 May 95 60 0 0 60 0 0 60 0 0 Hart I Ambersweet 18 Oct 94 60 19 42 51 6 12 40 2 7 Hart I Ambersweet 30 Nov 94 55 1 2 55 0 0 25 0 0 Hart I Ambersweet 19 Dec 94 60 1 2 60 0 0 60 0 0 Hart I Ambersweet 19 Jan 95 20 0 0 20 0 0 20 0 0 Hart I Ambersweet 8 Feb 95 60 — 8 60 — 17 60 — 2 Hart I Ambersweet 15 Mar 95 60 0 0 60 0 0 60 0 0 Hart I Ambersweet 19 Apr 95 60 0 0 60 0 0 60 0 0 Hart I Ambersweet 15 May 95 48 1 1 53 0 0 44 0 0 Trask Hamlin 1 Nov 94 60 2 6 60 0 0 58 0 0

Proc. Fla. State Hort. Soc. 112: 1999. 81 Table 2. Occurrence of citrus bud mite, Aceria sheldoni from different citrus varieties in Florida.

Current year green wood 1 year wood 2 year wood

No. buds No. buds Total No. buds No. buds Total No. buds No. buds Total Location Variety Date examined w/ mites mites examined w/ mites mites examined w/ mites mites Trask Hamlin 29 Nov 94 60 5 14 60 1 2 56 1 1 Trask Hamlin 20 Dec 94 60 — 8 60 — 1 60 — 0 Trask Hamlin 19 Jan 95 60 — 8 60 — 2 60 — 4 Trask Hamlin 6 Feb 95 60 6 29 57 0 0 60 0 0 Trask Hamlin 5 Apr 95 60 — 2 60 0 0 60 0 0 Trask Hamlin 17 Apr 95 60 0 0 60 1 2 60 0 0 las, Putnam and Volusia counties (Denmark, 1963). However, A. pelekassi were identified from slide-mounted eriophyoid mites their data was never quantified and by the late 1960s the mite was collected from 37 citrus grove sites in Florida between 1986 and no longer considered important. 1999. This represented 22.6% of the mites identified. During the In Croatia, A. pelekassi had 18-22 generations per year be- last two periods of observed activity, we collected eriophyoid fre- tween May and October (Mijuskovic, 1973). The time required quency data from a number of different citrus grove sites (Table 3). from egg to adult varied with temperature and ranged from 6.3 Our data showed that we had two species of citrus rust mites in 37 days at 30°C (86°F) to 14.9 days at 20°C (68°F) (Seki, 1979). of 120 citrus grove sites sampled between 1986 and 1999 while the PCRM eggs are translucent white and deposited indiscriminately remaining 83 sites had only citrus rust mite. Of the 37 sites identi- over leaf and fruit surfaces (Figs. 2C, D). This is in contrast to cit- fied with both PCRM and CRM, only 3 groves had higher numbers rus rust mite eggs that are spherical and tend to be deposited in de- of PCRM compared with CRM during 1990 and 1991. The per- pressions on the fruit surface (Figs. 3A, B). The pre-oviposition centages of sites with PCRM increased substantially in samples period was 1.8 days and the number of days from egg to egg was taken during 1990 and 1999. For example, of the 10 sites sampled 7.5 days at 30°C. Oviposition was maximum at 25°C with 21.8 during 1990, 8 had both rust mite species and 2 of these sites had eggs per female and oviposition ceased when temperatures greater numbers of PCRM. In 1999, 7 of the 10 sites sampled had dropped to 15°C (59°C) (Seki, 1979). A. pelekassi overwinters both PCRM and CRM. only in terminal and lateral buds on citrus in Japan with migration In 1990, PCRM populations were recorded on both fruit and occurring in early October (Seki, 1979) and Mijuskovic (1973) leaves beginning in April and ending in June (Fig. 5). The popula- found that PCRM overwintered in buds in Croatia. In late, Septem- tion densities attained on both fruit and leaves were considered ex- ber we recovered immature PCRM from leaf buds in a ‘Hamlin’ tremely high and resulted in significant damage to the fruit (Fig. block in Lake Alfred. Seki (1981) found, in Japan, that overwinter- 4C). This data illustrated the rapidly developing populations of ing females began laying eggs on the sprouting buds and newly PCRM and their sustained density levels in early season on both emerging leaves in the Spring, then moved to developing leaves in fruit and leaves. In a ‘Valencia’ grove in Tavares in Lake County, early May, and onto fruit in late June. In Florida, PCRM will begin we recovered high frequencies of PCRM on 23 April (420PCRM to feed on very small fruit during April or May. Numerous young vs 24 CRM) and 19 July 1991 (678 PCRM vs 20 CRM). However, ‘Hamlin’ and ‘Valencia’ fruit 3cm or less in diameter were com- by 24August 1991 the ratio of the two species approached 1:1 (42 pletely russetted by PCRM during 1999 (Figs. 4A,B). Injuries to PCRM vs 45 CRM). During 1995, PCRM were not abundant in twigs or young leaves were not observed in this case. Burditt etal. sampled grove sites (Table 3). Bergh and McCoy (1997) recovered (1963) reported that A. pelekassi caused distortion of young leaves frequencies of 8.4%, 8.7% and 14.6% eriophyoid mites not identi- when large populations occurred on new citrus growth, a form of fied as CRM from three grove sites in Polk County. Many of these damage not caused by the citrus rust mite (Reed et al., 1964; Seki, mites were identified as PCRM. 1979). By the end of June or early July 1999, PCRM populations were On three occasions (i.e., 1961-62, 1990-91 and 1999) notice- rapidly declining and CRM began to increase in several blocks in able increases in frequencies of PCRM were identified in different Lake and Polk counties. High density aggregations of PCRM were citrus growing areas within Florida. The first occurrence docu- observed on numerous occasions in the sunspot areas of fruit at mented the presence of PCRM on Florida citrus. A total of 14,640

Table 3. Frequencies of eriophyoid mites from selected citrus groves in Florida.

Phyllocoptruta oleivora Aculops pelekassi citrus rust mite pink citrus rust mite Other eriophyoids

County Location Date(s) Variety Fruit Leaves Fruit Leaves Fruit Leaves Polk Wauchula Jun 1986 Marsh GF 15 0 0 0 0 0 Polk Frostproof Jun Marsh GF 0 7 0 0 0 0 Polk Brewster Jun Marsh GF 0 9 0 0 0 1 Polk Brewster Mar-Jun Pineapple O 0 9 0 0 3 0 Hardee Bowling Green May-Jun Duncan GF 84 64 0 0 0 0 Hardee Bowling Green Jun Hamlin O 0 3 0 0 0 0 DeSoto Ft. Ogden Jun Marsh GF 5 0 0 0 0 0 DeSoto Ft. Ogden Jun-Oct Pineapple O 41 75 0 11 0 0 DeSoto Arcadia Dec Hamlin O 0 24 0 0 0 0 O = orange; GF = grapefruit; T = tangerine; Orlando = tangelo variety. Other eriophyoids: A = Aceria sheldoni; B = Abacarus sp.; C = Rhynacus sp.; D = Tegolophus sp.; E = Acaricalus sp.

82 Proc. Fla. State Hort. Soc. 112: 1999. Table 3. (Continued) Frequencies of eriophyoid mites from selected citrus groves in Florida.

Phyllocoptruta oleivora Aculops pelekassi citrus rust mite pink citrus rust mite Other eriophyoids

County Location Date(s) Variety Fruit Leaves Fruit Leaves Fruit Leaves Hillsborough Ft. Lonesome Jun Marsh GF 40 4 0 0 0 0 Brevard Merritt Island Feb-Oct Marsh GF 24 39 0 0 0 1 Brevard Merritt Island Mar Marsh GF 0 2 0 0 0 0 Indian River Vero Beach Jun Marsh GF 0 5 0 0 0 0 Indian River Vero Beach Jul-Sep Marsh GF 917 721 1 0 0 0 St. Lucie Ft. Pierce Sep Marsh GF 0 4 0 0 0 0 St. Lucie Ft. Pierce Apr-Sep Valencia O 339 102 0 0 0 0 Hendry Fellsmere May Hamlin O 0 65 0 0 0 0 Hendry Fellsmere Jun Valencia O 11 0 0 0 0 0 Hendry Fellsmere Jun Valencia O 0 26 0 0 0 0 Collier Sunniland Mar-Oct Hamlin O 72 67 0 2 0 0 Collier Sunniland Mar Valencia O 8 10 0 0 0 0 Hardee Bowling Green Feb-Jun 1987 Duncan GF 20 144 0 0 0 0 DeSoto Ft. Ogden Feb-Jun Pineapple O 4 24 0 2 0 0 Collier Sunniland May-Jun Hamlin O 71 50 0 0 0 0 Polk Babson Park May-Sep 1990 Valencia O 2,832 3,042 9 42 0 1(A) Polk Frostproof May-Sep Hamlin O 1,168 744 1 11 0 0 Polk Babson Park May-Sep Hamlin O 0 0 0 0 2(A), 1(B) 0 Polk Lake Alfred Jun-Sep Hamlin O 215 12 8,648 2,763 0 0 Polk Lake Alfred Oct Hamlin O 52 0 223 0 0 0 Polk Haines City Dec Robinson T 0 115 0 7 0 0 DeSoto Arcadia May-Sep Valencia O 306 115 23 2 1(A) 0 Martin Indiantown May-Sep Pineapple O 1,312 1,788 0 0 6 3(A) Hendry LaBelle Jul-Sep Hamlin O 191 201 0 11 1(A) 0 Hendry LaBelle Jun Parson Brown O 637 327 0 0 0 0 Lee Alva May-Sep Valencia O 105 229 0 2 0 0 Lake Howey-in-the-Hills May 1991 Red GF 121 158 0 0 0 0 Lake Howey-in-the-Hills May Hamlin O 0 121 0 11 0 0 Lake Howey-in-the-Hills May-Jun Sunburst T 376 623 82 139 0 0 Lake Howey-in-the-Hills May Orlando 0 88 0 0 0 0 Lake Howey-in-the-Hills May Valencia O 38 0 0 0 0 0 Lake Tavares May Valencia O 45 3 0 0 0 0 Lake Yalaha May Hamlin O 39 237 0 2 0 0 Lake ConServ May Hamlin O 2 0 0 0 0 0 Lake Tavares Apr-Aug Valencia O 0 89 0 1,140 0 0 Lake Cherry Lake Jun Hamlin O 321 0 0 0 0 1(C) Lake Clermont Aug Hamlin O 23 0 0 0 0 0 Lake Clermont Aug Hamlin O 20 0 1 0 0 0 Lake Clermont Aug Hamlin O 18 0 1 0 0 0 Polk Lake Alfred Aug-Sep Hamlin O 668 1,841 3 1,137 0 2 Polk Ft. Meade Apr Hamlin O 194 5 0 0 0 0 Polk Lake Alfred May Hamlin O 7 0 1 1 1(E) 0 Polk Waverly Jul Sunburst T 70 54 1 1 0 0 Polk Haines City May Robinson T 0 52 0 1 0 1 Hardee Bowling Green Apr Hamlin O 249 419 0 0 0 0 Hardee Bowling Green Apr Hamlin O 202 109 0 0 0 1(D) Hardee Bowling Green Apr Hamlin O 349 285 0 0 0 0 Hardee Bowling Green Apr Hamlin O 358 172 0 0 0 1(A) Hardee Bowling Green Apr Hamlin O 118 13 0 0 0 0 Hardee Bowling Green Apr Navel O 201 59 0 0 0 0 Hardee Bowling Green Apr Pineapple O 176 175 0 0 0 0 DeSoto Arcadia Feb Valencia O 671 41 0 0 0 0 Highlands Lake Placid May Hamlin O 361 311 0 1 0 0 Highlands Lake Placid May Valencia O 427 427 1 0 0 0 Highlands Lake Placid May Orlando 338 182 0 0 0 0 Hillsborough Ruskin Jul Hamlin O 351 153 0 0 0 0 Brevard Fellsmere Sep Marsh GF 109 94 0 1 1 0 Indian River Vero Beach Feb Marsh GF 0 883 0 0 0 0 St. Lucie Ft. Pierce Sep Marsh GF 817 938 0 0 0 0 St. Lucie Ft. Pierce Feb Valencia O 265 336 0 0 0 0 St. Lucie Ft. Pierce Feb Valencia O 265 197 0 0 0 0 St. Lucie Ft. Pierce Feb Marsh GF 102 31 0 0 0 0 St. Lucie Ft. Pierce Jun Navel O 146 84 0 3 0 0 St. Lucie Ft. Pierce Feb Pineapple O 256 113 0 0 0 0 Martin Indiantown Feb Pineapple O 0 419 0 0 0 0 Martin Indiantown Sep Red GF 436 15 0 0 0 0 Martin Hobe Sound Sep Marsh GF 0 3 0 0 0 0 Hendry Clewiston Mar Hamlin O 66 14 0 0 0 0 O = orange; GF = grapefruit; T = tangerine; Orlando = tangelo variety. Other eriophyoids: A = Aceria sheldoni; B = Abacarus sp.; C = Rhynacus sp.; D = Tegolophus sp.; E = Acaricalus sp.

Proc. Fla. State Hort. Soc. 112: 1999. 83 Table 3. (Continued) Frequencies of eriophyoid mites from selected citrus groves in Florida.

Phyllocoptruta oleivora Aculops pelekassi citrus rust mite pink citrus rust mite Other eriophyoids

County Location Date(s) Variety Fruit Leaves Fruit Leaves Fruit Leaves Hendry Clewiston Mar Hamlin O 33 48 0 0 0 0 Hendry Clewiston Mar Hamlin O 163 40 0 0 0 0 Hendry Clewiston Mar Hamlin O 59 33 0 0 0 0 Hendry Clewiston Mar-Jun Hamlin O 964 699 0 0 0 0 Hendry Fellsmere Jun Valencia O 527 213 0 0 0 0 Hendry Fellsmere Jun Hamlin O 680 907 0 0 0 0 Collier Bonita Springs Jun Hamlin O 809 411 0 0 1(A) 0 Lee Alva Feb Valencia O 282 76 0 0 0 0 Charlotte Babcock Jun Valencia O 173 860 0 0 0 0 Charlotte Babcock Jun Pineapple O 205 63 0 0 0 0 Charlotte N. Ft. Myers Jun Pineapple O 313 226 0 0 0 0 Dade Homestead Feb Tahiti Lime 1 5 0 0 0 0 Dade Homestead Feb Tahiti Lime 15 69 0 0 0 1(A) Dade Homestead Feb Tahiti Lime 289 117 0 0 0 0 Dade Homestead Feb T 7 11 0 0 0 0 Dade Homestead Feb Tahiti Lime 3 4 0 0 0 0 Dade Homestead Feb Tahiti Lime 1 0 0 0 0 0 Palm Beach Boynton Beach Sep Star Ruby GF 191 553 0 0 0 0 Palm Beach Boynton Beach Sep Marsh GF 77 5 0 0 1(A) 0 Palm Beach Boynton Beach Feb Valencia O 68 93 0 0 0 0 Palm Beach Loxahatchee May Hamlin O 970 893 0 0 0 0 Polk Baseball City Aug 1992 Hamlin O 41 0 0 0 0 0 Polk Ft. Meade Aug Hamlin O 28 0 0 0 0 0 Polk Haines City Nov Hamlin O 73 106 8 34 0 0 Martin Hobe Sound Sep Marsh GF 638 0 0 0 0 0 Lake Hart I (Mascotte) May-Oct 1995 Ambersweet O 102 143 1 0 1(A) 1(A) Lake Hart II (Mascotte) May-Jul Navel O 8 85 0 0 0 4(A) Polk Yarborough May-Oct Hamlin O — 90 — 1 — 0 Polk Pollard May-Oct Marsh/Duncan GF — 386 — 0 — 0 Polk Trask Jul-Oct Hamlin O 199 204 0 0 0 0 DeSoto Mixon I (Arcadia) May-Oct White GF 89 404 0 0 0 0 DeSoto Mixon II (Arcadia) May-Oct Valencia O 77 321 0 0 0 0 Lake Montverde (97-6) Feb 1998 Hamlin O — 105 — 3 — 1(A) Highlands Sebring Nov O 14 — 0 — 0 — Polk Lake Alfred (99-3) Sep 1999 Hamlin O 216 — 89 — 0 — Lake Clermont (99-4) Jun-Jul Hamlin O 485 — 95 — 0 — Hardee Lily (99-5) Jun Hamlin O 81 — 0 — 0 — Polk Lake Alfred (99-6) Jul-Aug Hamlin O 146 — 32 — 0 — Lake Clermont (99-6) Jul-Aug Hamlin O 99 — 0 — 0 — Polk Baseball City (99-6) Jul-Aug Hamlin O 59 — 22 — 0 — Polk Baseball City (Tract-5) Jul Hamlin O 141 — 53 — 0 — Polk Lake Alfred (R/R) Jul-Aug Valencia O 123 — 10 — 0 — Polk Haines City Aug Temple O 66 — 2 — 0 — Lake ConServ 2 Aug T 47 — 0 — — 0

O = orange; GF = grapefruit; T = tangerine; Orlando = tangelo variety. Other eriophyoids: A = Aceria sheldoni; B = Abacarus sp.; C = Rhynacus sp.; D = Tegolophus sp.; E = Acaricalus sp. midday, or afternoon as they dispersed (Fig. 4D). This behavior is should be initiated. Second, if there has been a recent history of totally different from that observed with citrus rust mite where PCRM infestations in specific blocks of citrus then monitoring avoidance of direct sunlight occurs. The mites form a distinctly should be initiated. golden yellow to pinkish, dusty area on the fruit during the dispers- Based on the amount of damaged fruit observed in several cit- al phase as a result of their large aggregations. rus blocks beginning in early June 1990 and 1999, identification of High populations of PCRM in Japan were related to (1) higher PCRM populations on the fruit, frequency data of the two rust mite than average Spring temperatures and (2) low precipitation in early species, and the literature, it appears that PCRM move from leaves Summer. Precipitation patterns in Japan during early Spring to ear- to fruit very early (i.e., early April to early May) in Florida com- ly Summer are generally low until onset of Summer rains (Kohei pared with citrus rust mites. Examining young, succulent leaves Inoue, personnel communication). Similar conditions occurred in and twigs for PCRM before they move onto fruit will be necessary Florida during 1989-90 and 1998-99. to avoid potential rind blemish damage that can begin in early The need for monitoring PCRM populations on leaves and April. fruit in early April-May is a necessity especially for fresh market Citrus rust mite-Phyllocoptruta oleivora (Ashmead). The cit- fruit. Until more definitive data can be generated, two factors rus rust mite (CRM) can be separated from PCRM or CBM by the should trigger the need to monitor for this rust mite. First, if weath- following characters. First, CRM are generally yellow to straw col- er conditions resulted in mild winter temperatures and/or low rain- ored and somewhat wedged-shaped (Fig. 3C). The dorsum of the fall during the previous year, or into early Spring then monitoring opisthosoma has a longitudinal furrow that is characteristic of the

84 Proc. Fla. State Hort. Soc. 112: 1999. Figure 3. (A) Example of distribution of citrus rust mite eggs on citrus fruit sur- Figure 2. (A) Pink citrus rust mite. (B) Prodorsal shield of pink citrus rust mite face. Note clustering in depressions especially around oil glands. (B) Citrus rust showing dorsal setae (ds) extending beyond distal margin of shield. (C) Example of mite egg. (C) Citrus rust mite. (D) Prodorsal shield of citrus rust mite showing short distribution of pink citrus rust mite eggs on citrus fruit surface. (D) Pink citrus rust dorsal setae (ds) that do not extend beyond distal margin of shield. mite egg. genus Phyllocoptruta. The prodorsal shield is well defined and dis- family, Diptilomiopidae, one specimen of Rhynacus sp. was col- tinctly different by having very short dorsal setae that do not ex- lected from ‘Sunburst’ tangerine leaves in the Faryna grove in tend beyond the distal margin of the shield (Fig. 3D). Color of the Umatilla, Lake County on 9 May 1991. Citrus is not considered a mites can be determined with a 10´ handlens. The other characters host for these four mites since neither eggs nor immatures were re- are difficult to see without good magnification (i.e., 20-40´). covered. The mean developmental times for CRM stages are similar to PCRM (vanBrussel, 1975). The pre-oviposition interval was 1.8 Summary days and total egg production ranged from 26 to 29 per female or 1 or 2 eggs per day (Yothers and Mason, 1930; Swirski and Amitai, Much of the recent literature has failed to address the eriophy- 1959). oid complex that exists on Florida citrus. While CRM is the prev- CRM is found throughout the world (Jeppson et al., 1975) and alent eriophyoid mite found in most Florida citrus groves sampled was first reported on Florida citrus by Ashmead (1879). CRM has it is not the only economic pest in this family. In future studies, it been recognized generally as the most important arthropod pest on is important that we not lump the three species as “citrus rust mite” Florida citrus (Yothers and Mason, 1930; Childers, 1994). A total since their development, biology, feeding damage and seasonal ac- of 49,658 P. oleivora were identified from slide-mounted eriophy- tivities obviously differ. oid mites collected from 120 citrus grove sites between 1986 and When weather conditions become favorable to PCRM, then 1999. This represented 76.6% of the identified eriophyoid speci- different grove sites across Florida can be damaged early due to mens. Feeding by the mite results in injury to the fruit, leaves and rapidly developing populations moving onto fruit in early April- young terminal shoots (Yothers and Mason, 1930; McCoy et al., May. Extensive and serious rind blemish injuries resulted where 1976). However, none of these authors reported inclusion of early increases in PCRM populations occurred in many grove sites voucher specimens to validate which species of rust mite was feed- during 1990 and 1999. Based on the information presented in this ing on leaves or green branches. The primary feeding damage by paper it was evident that PCRM has the potential to cause signifi- CRM is to both immature and mature citrus fruit, resulting in early cant economic losses especially in fresh fruit blocks. Further stud- or late season fruit blemish referred to as russetting (Albrigo and ies are needed to identify the conditions that create outbreaks of McCoy, 1974). Epidermal cells die, wound peri-derm develops, pink citrus rust mites on Florida citrus. We also need to develop ef- with both reduced fruit size and yield reduction occurring follow- fective monitoring protocols to identify potentially injurious pop- ing early season injury. Water loss, reduced bonding force of the ulations before losses are incurred. Additional studies are needed fruit, and increased fruit drop are greater on citrus rust mite-dam- to clearly understand the biology of CBM and assess its potential aged fruit compared to clean fruit (Allen, 1978; 1979). for damage on Florida citrus. Other eriophyoid mites collected on Florida citrus. In the fam- ily Eriophyidae, one specimen of Abacarus sp. was collected from a Shinn ‘Hamlin’ orange grove on young fruit in the Green Swamp Literature Cited area of Polk County on 24 May 1991. One specimen of Tegolophus Albrigo, L. G. and C. W. McCoy. 1974. Characteristic injury by citrus rust mite to sp. was collected from young leaf flush in the Cargill NK-Rebel orange leaves and fruit. Proc. Fla. State Hort. Soc. 87:48-55. block of ‘Hamlin’ orange in the Bowling Green vicinity in Hardee Allen, J. C. 1978. The effect of citrus rust mite damage on citrus fruit drop. J.Econ. County on 26 April 1991. One specimen of Acaricalus sp. was col- Entomol. 71:746-750. lected from ‘Hamlin’ orange fruit at the West Wilson BHG grove Allen, J. C. 1979. The effect of citrus rust mite damage on citrus fruit growth. J. in Frostproof, Polk County on 25 September 1990 (Table 3). In the Econ. Entomol. 72:195-201.

Proc. Fla. State Hort. Soc. 112: 1999. 85 Figure 4. (A-B) Very small ‘Valencia’ orange fruit heavily russetted by pink citrus rust mites. (C) Pink citrus rust mites on fruit surface. (D) Aggregation of pink citrus rust mites on ‘Temple’ (tangor) fruit during dispersal.

Amrine, J. W., Jr. and D. C. M. Manson. 1996. Preparation, mounting and descrip- tive study of eriophyoid mites. pp. 383-396. In E. E. Lindquist, M. W. Sabelis and J.Bruin. (eds.). Eriophyoid mites their biology, natural enemies and con- trol. Elsevier. Amsterdam. Amrine, J. W., Jr. and T. A. Stasny. 1994. Catalog of the Eriophyoidea (Acarina: ) of the world. Indira Pub. House. West Bloomfield, Mich. Ashmead, W. H. 1879. Injurious and beneficial insects found on the orange trees of Florida. Canadian Entomol. 11:159-160. Attiah, H. H. 1959. On the discovery of two economic species of eriophyid mites on mango and citrus trees in Florida. Fla. Entomol. 42:189. Bergh, J. C. and C. W. McCoy. 1997. Aerial dispersal of citrus rust mite (Acari: Eriophyidae) from Florida citrus groves. Environ. Entomol. 26: 256-264. Boczek, J. and A. Chandrapatya. 1996. Studies on eriophyoid mites (Acari: Erio- phyoidea). XVIII. Bull. Polish Acad. Sci., Biological Sci. 44:61-70. Boyce, A. M. and R. B. Korsmeier. 1941. The citrus bud mite, sheldoni Ewing. J. Econ. Entomol. 34:745-756. Burditt, A. K., Jr., D. K. Reed and C. R. Crittenden. 1963. Observations on the mites Phyllocoptruta oleivora (Ashmead) and Aculus pelekassi Keifer under labora- tory conditions. Fla. Entomol. 46:1-5. Childers, C. C. 1994. Biological control of phytophagous mites on Florida citrus utilizing predatory . pp. 255-288. D. Rosen, F. Bennett, and J.Capinera (eds.). In Biological Control and IPM: The Florida Experience. In- tercept, Andover, United Kingdom. Childers, C. C. and A. G. Selhime. 1983. Reduced efficacy of fenbutatin-oxide in Figure 5. Pink citrus rust mite populations on ‘Hamlin’ orange fruit and leaves combination with petroleum oil in controlling the citrus rust mite, Phyllo- between April and June, 1990. Mean number of mites were based on live motiles per coptruta oleivora on citrus. Fla. Entomol. 66:310-319. 2 cm 2 of fruit surface and live motiles per 4.5 cm2 of leaf surface.

86 Proc. Fla. State Hort. Soc. 112: 1999. Ciampolini, M. and P. Rota. 1963. Polyphagy and spread of Aculus pelekassi on cit- rus in Apulia. Boll. Zool. Agr. Bachic. 2:83-91. Denmark, H. A. 1962. Aculus pelekassi Keifer, another citrus mite in Florida. Proc. Fla. State Hort. Soc. 75:25-27. Flechtmann, C. H. W. and B. R. Aranda. 1970. New records and notes on eriophyid mites from Brazil and Paraguay, with a list of Eriophyidae from South America. Proc. Entomol. Soc. Wash. 72:94-98. Hong, X. and H. Kuang. 1989. Three new genera and seven new species of the sub- family Phyllocoptinae (Acari: Eriophyidae) from China. Int. J. Acarol. 15:145-152. Ishaaya, I. and M. Sternlicht. 1969. Growth accelerators and inhibitors in lemon buds infested by Aceria sheldoni (Ewing) (Acarina: Eriophyidae). J. Exp. Bot. 20:796-804. Jeppson, L. R., H. H. Keifer and E. W. Baker. 1975. Mites injurious to economic . Univ. California Press. Berkeley. Keifer, H. H. 1959. Eriophyid studies XXVII. California Dept. 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Effect of late season fruit injury by the citrus rust mite, Phyllocoptruta oleivora (Prostigmata: Eriophyoidea), on the internal quality of Valencia orange. Fla. Entomol. 59:335-342. Mijuskovic, M. 1973. Control of the citrus bud mite. Poljoprivreda i Sumarstvo 19:41-50. Mijuskovic, M. and D. Kosac. 1972. Control of Aculops pelekassi Keifer (Acarina: Eriophyidae), an important mite injurious to Citrus on the coast of Montenegro. Jugoslovenskog Vocarstva 21/22:835-842. Norman, P. A., D. K. Reed and C. R. Crittenden. 1970. Pesticides screened against two rust mites of citrus. J. Econ. Entomol. 63:1409-1412. Phillips, P. A. and G. P. Walker. 1997. Increase in flower and young fruit abscission caused by citrus bud mites (Acari: Eriophyidae) feeding in the axillary buds of lemon. J.Econ. Entomol. 90:1273-1282. Reed, D. K., A. K. Burditt, Jr. and C. R. Crittenden. 1964. Laboratory methods for rearing rust mites (Phyllocoptruta oleivora and Aculus pelekassi) on citrus. J. Econ. 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