612 Florida Entomologist 87(4) December 2004

CHAETOSIPHON FRAGAEFOLII (HOMOPTERA: ): A POTENTIAL NEW PEST IN FLORIDA?

SILVIA I. RONDON AND DANIEL J. CANTLIFFE University of Florida, Horticultural Sciences Department, P.O. Box 110690, Gainesville, FL 32611

During the spring of 2003-2004, the straw- wintering eggs, nymphs, adult apterae (wingless) berry , fragaefolii (Cockerell) and alatae, and parthenogenetic females. Eggs (Homoptera: Aphididae), was found infesting ten are white yellowish when deposited, but soon af- different cultivars, Fragaria anan- ter, become shiny and black. Nymphs are small assa Duchesne, grown under protected culture in (0.8-1.1 mm) (n = 20) and morphologically similar a greenhouse in Marion County, FL. The cultivars to the adults. They vary in color from light green were ‘Treasure’, ‘Earlibrite’, ‘Strawberry Festi- to pale yellow. Adults are 1.3-1.5 mm long, pale to val’, ‘Sweet Charlie’, FL 97-39, ‘Camarosa’, ‘Car- yellowish green with short knobbed setae over the mine’, ‘Camino Real’, ‘Diamante’, and ‘Ventana’. body; the antennae are as long as, or longer, than This is the first report of the presence of C. fragae- the length of the body; siphunculi are long, pale folii in cultivated strawberry in Florida (Division and slender, about ¼ body length, and legs are of Plant Industry, DPI E2004-278-201). pale green and almost translucent. According to In December 2003, the strawberry aphid was Heinz (1998), sexual forms are quite rare because observed on a strawberry cultivar trial at the Uni- reproduce parthenogenetically through- versity of Florida Plant and Science Research out the winter if the temperature remains above Unit at Citra. The susceptibility of ten strawberry 4.5°C; however, C. fragaefolii was found in a cultivars to natural infestations to the cotton greenhouse (average day temperature 21°C), and aphid, Aphis gossypii Glover, was being evalu- sexual forms were observed at the cultivar trial ated. ‘Treasure’, ‘Earlibrite’, ‘Strawberry Festi- (DPI E2004-278-202). Blackman & Eastop (2000) val’, ‘Sweet Charlie’, FL 97-39, ‘Camarosa’, and suspected that day length rather than tempera- ‘Carmine’ plugs were grown at UF facilities as de- ture trigger the formation of sexual forms. The scribed by Paranjpe et al. (2003); ‘Camino Real’, large number of exuviae on the leaves indicates ‘Diamante’, and ‘Ventana’ plugs came from a Ca- proliferation of the aphid in the crop. As in other nadian nursery. Two months after the beginning of aphids, the strawberry aphid feeds on of the trial, samples of an “unknown” aphid in the the underside of leaves close to veins. The cotton aphid trial were taken to the Division of also was observed feeding on tips, petioles, small Plant Industry in Gainesville, FL, for identifica- fruits, calyxes, and young flowers. Leaf curling tion. On 22 January, samples were identified as was not observed but foliage turned chlorotic, C. fragaefolii, the true strawberry aphid. Since which probably diminished the photosynthetic ca- the strawberry aphid was detected relatively pability of the plant. Aphids were more abundant early in the season, two applications of insecti- on certain cultivars. ‘Carmine’ (4.3 ± 1.8 aphids/ cidal soap (10%) (28 January and 12 February) leaflet), ‘Strawberry Festival’ (3.7 ± 0.8 aphids/ were required to effect control. Two days after the leaflet), FL 97-39 (2.9 ± 1.3 aphids/leaflet), and second soap application, 10 Chrysoperla rufila- ‘Diamante’ (2.1 ± 1.1 aphids/leaflet) were the most bris L. and Aphidoletes aphidimyza L. per m2 affected (alpha = 0.05, confidence interval 95%). were released. Both methods were relatively suc- The strawberry aphid is considered an impor- cessful; however, resurgence of pests was heavy tant pest of in open fields worldwide, by mid March causing the early termination of including the U.S. (California, Michigan, Minne- the crop. No insecticides were used to control the sota, South Carolina, and Washington), Canada, aphid because the strawberry trial and other crop northern Mexico, Europe, Great Britain, South trials in the greenhouse depended on bumblebees Africa, New Zealand, and Australia (Dixon et al. (highly susceptible to pesticides) for pollination. 1987; Blackman & Eastop 2000). Chaetosiphon At the end of the trial, the strawberry aphid was fragaefolii is well known in most of North Amer- eliminated from the greenhouse and hopefully ica where strawberries are grown but not in Flor- eradicated from Florida. A heavy application of ida. Whether C. fragaefolii might have been in soap and oil (40%) was made before removing the Florida prior to its recent discovery or may have plant material from the greenhouse. All material come from transplants from Canada is uncertain. was buried and burned. The strawberry aphid has The of the genus is difficult. In 1938- not been detected in strawberry crops on other 1939, specimens taken from Rose spp. in Florida outdoor locations of the farms or in other produc- were identified as C. fragaefolii (DPI records); tion areas in Florida. however, it was recently determined that they ac- Based on a sample of the aphid population, the tually correspond to C. thomasi Hille Ris Lam- following observations and conclusions were bers. It was established that C. fragaefolii will not made: the life cycle of C. fragaefolii includes over- colonized rose, and that records of C. fragaefolii

Scientific Notes 613 on roses should be referred to C. thomasi (Black- begin early in the season and continue through- mand & Eastop 2000). out the duration of the crop. Leaflets and shoots has been reported on wild strawberry, especially must be visually inspected from random locations F. chiloensis in North America, F. vesca, F. virgin- throughout the field. After identification of the ianana, and Ponsetia anserine L. (Frazier 1974; pest, yellow sticky cards can be used to detect the Blackman & Eastop 2000). We report C. fragae- winged form; however, if alates are found, a well- folii on cultivated strawberry in greenhouses. established aphid population is already in the Chaetosiphon fragaefolii transmits viruses that crop. The presence of ants, which feed on sugar can cause strawberry yellow edge virus (SYEV), produced by the aphids, may also be a sign of a strawberry crinkle virus (SCV), and strawberry heavy infestation. mottle virus (SMV) (Krczal 1979, 1982; Blackman No extended information is available regard- & Eastop 2000; Converse 2002; Posthuma et al. ing the effect of natural enemies on C. fragaefolii. 2002). For instance, symptoms of SCV are ne- In general, augmentation of biological control suf- crotic lesions with irregular spots on veins, epini- fers from a lack of basic and well-designed strate- asty, crinkling, distortion, and uneven expansion gies for release on a large scale, especially in open of leaflets. Lesions on petioles and stolons pro- field conditions (Heinz 1998). Although parasitic duce angularity, streaking and deformation of wasps are species specific, Aphelinus species petals (Frazier & Mellow 1970; Frazier 1974). which are commercially available, may have an These symptoms were not observed on any of the effect on strawberry aphid populations (Biobest cultivars in our trial. Chaetosiphon fragaefolii Aphelinus-system http://www.biobest.be, http:// can acquire the viruses within 24 h of birth. After bugssandbees.com; Koppert, http://www.koppert. a latent period of 10-19 days, the infected aphid nl; Syngenta, http://syngenta.com). The parasitic can transmit virus for up to 2 weeks (Mellow & wasp Aphidius colemani L, was used successfully Frazier 1970). in the greenhouse to control the cotton aphid in In Florida, strawberries are an annual crop the cultivar trial; however, A. colemani was not grown on approximately 7,100 acres; 95% of the observed parasitizing C. fragaefolii. The numer- acreage is located in the Plant City area of west ous capitate setae of C. fragaefolii may protect the central Florida (NASS-USDA 2003). Production aphid from parasitic wasps. Several biological costs average more than $23,000 per acre, mak- control options are available for aphid control. ing strawberry one of the most expensive crops in Lady beetles, such as Hippodamia convergens Florida to produce (FAFD 2002). The area of Guérin-Méneville (Rodriguez-Saona & Miller strawberry grown under protected cultivation in 1999) and Coleomegilla maculata DeGeer (Ron- Florida is less than 1 ha (NASS-USDA 2003). The don et al. 2004) are important aphid feeders. overall industry produces 15% of the total U.S. Lacewings such as Chysoperla rufilabris and C. crop and accounts for more than 17% of the total carnea Say, and the predatory midge A. aphi- dollar value generated from sales of fresh berries dimyza are voracious predators of aphids (Heinz in the U.S. (NASS-USDA 2003). If the strawberry 1998). Aphidoletes aphidimyza attacks many spe- aphid were to spread into commercial production cies of aphids; it can act alone or in combination areas of Florida, it could cause severe damage to with a parasite for rapid knockdown of aphid in- the strawberry industry, especially if viruses festations. This predator is most effective on were present. Strawberries require a highly inte- aphid “hot spots.” grated management system to control pests to in- If biological control is used, one should reduce sure profitability. In addition to C. fragaefolii (the or limit the use of broad-spectrum pesticides; pre- strawberry aphid), C. jacobi, C. minor (Forbes), ventive releases are recommended; monitor A. gossypii (the cotton aphid), A. forbesi Weed (the weekly to detect first sign of pest. If honey dew is strawberry root aphid also sometimes known as present, it may interfere with the search capabil- “the strawberry aphid”), Macrosiphon euphorbiae ity of the parasitoid, and the use of light soap is (Thomas) (the potato aphid), and Myzus persicae suggested. If insecticides are used to suppress the (Sulzer) (the green peach aphid) infest strawber- strawberry aphid, a full coverage is recom- ries (Table 1) (Blackman & Eastop 2000). Chaeto- mended. For greenhouse aphid control, Tanigoshi siphon fragaefolii and C. jacobi have not been & Bergen (2003) recommend Acatara® (thio- reported before in Florida strawberries. methoxam), Admire® (imidacloprid), Assail® (ac- Should the strawberry aphid become estab- etar) and Fulfill® (pymetorzine). Insecticidal soap lished in Florida, effective and timely control is (2.5 oz/gal water) can effectively reduce straw- essential in strawberry production due to the berry aphid population but may harm the crop aphid’s ability to develop large populations in a (personal observation); in addition, botanical in- short period. Cultural and mechanical control of secticides such as neem (Azatin™, Neemazad™, the strawberry aphid in the greenhouse or open and Nemix™) may be effective. Strains of the fun- field should include inspecting incoming trans- gus Beauveria bassiana, commercially available plants and eliminating infested crop material as Naturalis-O™ and BotaniGard™, may provide from the production site. Plant monitoring should good control of aphids. Insect growth regulators

614 Florida Entomologist 87(4) December 2004

TABLE 1. THE STRAWBERRY, Fragaria ananassa DUCH- approved for publication as Journal Series No. ESNE, APHID COMPLEX (MODIFIED FROM R-10270. BLACKMAN & EASTOP 2000).

Frequency SUMMARY in the strawberry During the spring 2003-2004 growing season, crop in the the strawberry aphid, Chaetosiphon fragaefolii Scientific name U.S.* (Cockerell) (Homoptera: Aphididae), appeared for the first time in damaging numbers on the straw- Acyrthosiphon rogersii (Theobald) 2 berry, Fragaria ananassa Duchesne, a high value Aphis forbesi Weed 1 commodity in Florida. Nymphs and adults of the Aphis gossypii Glover 1 strawberry aphid were found infesting ten differ- Aphis ruborum (Börner) 2 ent strawberry cultivars: ‘Treasure’, ‘Earlibrite’, Aulacorthum solani (Kaltenbach) 2 ‘Strawberry Festival’, ‘Sweet Charlie’, FL 97-39, Chaetosiphon fragaefolii (Cockerell) 1 ‘Camarosa’, ‘Carmine’, ‘Camino Real’, ‘Diamante’, Chaetosiphon jacobi Hille Ris Lambers 2 and ‘Ventana’. A brief description of the morphol- Chaetosiphon minor (Forbes) 2 ogy, biology, damage, and ecology of the pest is Ericaphis fimbriata (Richards) 2 presented. Correct identification, early detection Ericaphis wakibae (Hottes) 2 of the strawberry aphid, and adequate timely con- Macrosiphum euphorbiae (Thomas) 2 trol can prevent the spread of this pest. Macrosiphum rosae (Linnaeus) 2 Myzus ascalonicus (Doncaster) 2 REFERENCE CITED Myzus ornatus Lains 2 Rhodobium porosum (Sanderson) 2 BLACKMAN, R. L., AND V. F. EASTOP. 2000. Aphids on Sitobion fragariae (Walker) 2 the World’s Crops: An Identification and Informa- Aphis ichigocola Shinji 3 tion Guide. 2nd edition. Wiley, NY. 324 pp. Aphis maidiradicis Forbes 3 CONVERSE, R. H. 2002. Virus Diseases of Small Fruits. Aphis nasturtii Kaltenbach 3 U.S. Department of Agriculture, Agricultural Re- Aulacorthum circumflexum (Buckton) 3 search Service No. 631. 100 pp. DIXON, A. F. G., P. KINDLMANN, J. LEPS, AND J. HOL- Hyalomyzus fragaricola L.K. Ghosh 3 MAN. 1987. Why there are so few species of aphids espe- Hyperomyzus rhinanthi (Schouteden) 3 cially in the tropics. American Naturalist 129: 580-592. Macrosiphum pallidum (Oestlund) 3 FAFD (FLORIDA AGRICULTURAL FAST DIRECTORY). Myzaphis rosarum (Kaltenbach) 3 2002. FAOSTAT Agriculture database. Food and Ag- Myzus cymbalariae Stroyan 3 riculture Organization. http://apps.fao.org/page/col- Myzus persicae (Sulzer) 3 lection/subset-agriculture(08/20/03). Abstrusomyzus valuliae (Robinson) 3 FRAZIER, N. W. 1974. Strawberry crinkle virus, pp. 1-18 Paramyzus longirostris Miyazaki 3 In Plant Disease Report No. 58. Pemphigus bursarius (Linnaeus) 3 FRAZIER, N. W., AND F. C. MELLOW. 1970. Strawberry crinkle, pp. 18-23 In Virus Disease of Small Fruits Rophalosiphoninus latysiphon (Davidson) 3 and Grapevines. University of California Berkeley, Division of Plant Industry, CA. 186 pp. *1 Frequent, 2 Occasional, 3 Rare. HEINZ, K. M. 1998. Dispersal and dispersion of aphids and selected natural enemies in spatially subdivided greenhouse environments. Environ. Entomol. 27: (IGR) are another least toxic insecticide that can 1029-1038. be used. IGR kills by disrupting their de- KRCZAL, H. 1979. Transmission of the strawberry mild velopment, stopping the molting process (inter- yellow edge and strawberry crinkle virus by the fere with chitin production), and mimicking strawberry aphid Chaetosiphon fragaefolii. Acta juvenile hormone (insects never get into a repro- Horticulturae 95: 23-30. KRCZAL, H. 1982. Investigations on the biology of the ductive stage) (Sunderland 1992). strawberry aphid (Chaetosiphon fragaefolii), the Future information regarding biological and most important vector of strawberry viruses in west ecological aspects of the strawberry aphid will set Germany. Acta Horticulturae 129: 63-68. the basis of an effective integrated pest manage- MELLOW, F. C., AND N. W. FRAZIER. 1970. Strawberry ment program for the aphid if it becomes estab- mottle, pp. 4-8 In Viruses and Diseases of Small lished in Florida. Fruits and Grapevines. University of California, Ber- We thank Dr. Susan Halbert, Florida Depart- keley, Division of Agricultural Sciences, Ca. No. 290. ment of Agriculture for identification of the aphid. NASS-USDA (NATIONAL AGRICULTURAL STATISTICAL We thank Drs. David Voegtlin (University of Illi- SERVICE). 2003. Non-citrus fruits and nuts. 2002. Preliminary Summary, pp 28-31. nois), Margaret Smith-Kopperl (University of PARANJPE, A. V., D. J. CANTLIFFE, S. I. RONDON, C. K. Florida), and anonymous reviewers, who helped CHANDLER, AND E. J. BRECHT. 2003. Trends in fruit to improve the manuscript. This research was yield and quality, susceptibility to powdery mildew supported by the Florida Agricultural Station and (Sphaerotheca macularis), and aphid (Aphis gos- Scientific Notes 615

sypii) infestation for seven strawberry cultivars RONDON, S. I., D. J. CANTLIFFE, AND J. F. PRICE. 2004. grown without pesticides in a passively ventilated The feeding behavior of three generalist predators greenhouse using pinebark as soilless substrate. relative to main strawberry pests. Environ. Ento- Proc. Fla. State Hort. Soc. 116: 740-755. mol. 33: 1014-1019. POSTHUMA, K. I., A. N. ADAMS, Y. HONG, AND M. J. SUNDERLAND, K. 1992. Integrated pest management of KIRBY. 2002. Detection of strawberry crinkle virus in greenhouse crops in northern Europe, pp. 22-30 In plants and aphids by RT-PCR using conserved L J. Janick. [ed.], Aphids. John Wiley and Sons, Inc. NY. gene sequences. Plant. Path. 51: 266-274. TANIGOSHI, L. K., AND J. R. BERGEN. 2003. Evaluation RODRIGUEZ-SAONA, C., AND J. C. MILLER. 1999. Temper- of novel insecticides for the rational control of aphids ature-dependent effects on development, mortality, in strawberries 2002. Washington State University, and growth of Hippodamia convergens (Coleoptera: Vancouver Research and Extension Unit, Vancou- Coccinellidae). Environ. Entomol. 28: 518-522. ver, VA.