Journal of Economic Entomology Advance Access published January 24, 2015 HORTICULTURAL ENTOMOLOGY Evidence of Protaphorura fimata (Collembola: Poduromorpha: Onychiuridae) feeding on germinating lettuce in the Salinas Valley of California 1,2 1 1,3 SHIMAT V. JOSEPH, CHRISTOPHER BETTIGA, CHRISTIAN RAMIREZ, AND FELIPE N. SOTO-ADAMES4 J. Econ. Entomol. 1–9 (2015); DOI: 10.1093/jee/tou021 ABSTRACT A series of experiments were conducted to determine the impact of Protaphorura fimata Gisin (Family: Onychiuridae) feeding on seeds and germinating seedlings of lettuce, Lactuca sativa L. (Asteraceae). First, various densities of P. fimata were incubated with 25 lettuce seeds for 7 d and feeding injury was evaluated in three soilless arena experiments. As a second step, 100 P. fimata were incubated with 25 lettuce seeds in three arena experiments with soil media. Finally, in a commercial field the incidence and impact of P. fimata on recently planted lettuce was assessed following applications of pyre- throid–insecticides: 2 d before planting, at planting, and 20 d later. In experiments without soil, the num- ber of ungerminated seeds, feeding injury sites, and plants with injury were significantly greater in arenas with P. fimata than without. Similarly, the number of germinated seedlings, shoot fresh, and dry weights, and the length and width of fully opened-leaves were greater in arenas without than with P. fimata in as- says with soil. In the field, P. fimata densities were significantly lower in beds that received insecticides at 2 d before and at planting than in untreated beds. Also, the fresh and dry weights of lettuce plants were significantly greater in the beds that received insecticide than in untreated. The results clearly show that P. fimata is a pest of lettuce and can cause severe feeding injury to germinating seeds or seedlings, thereby reducing their growth rate. The potential implications of P. fimata feeding and feeding injury characteristics are discussed. KEY WORDS springtail, feeding injury, seed predation, Lactuca sativa, vegetable production, central coast of California Introduction spinach (Spinacia oleracea L.), and lima beans (Phaseo- A subterranean springtail, Protaphorura fimata Gisin lus lunatus L.) in the Salinas Valley; however, Scott (Family: Onychiuridae), was found associated with (1953, 1964) reported onychiurids as pests of vegeta- poor germination of lettuce, Lactuca sativa L. (Astera- bles in the Salinas Valley but did not present evidence ceae), particularly during February to May in the for Protaphorura spp. feeding damage on any of the northern part of Salinas Valley of California. The young crops. Greenslade and Ireson (1986) indicated that lettuce seedlings in fields with high densities of members of the family Onychiuridae could only be reli- P. fimata show retarded or stunted growth and do not ably identified to a group level such as P. armata group. emerge in a synchronous pattern. The value of lettuce P. fimata is less than 2.5 mm in length; lacks eyes, is estimated to be US$1.3 billion in the Salinas Valley pigmentation, and furcula; and carries 33/022/33333 (Monterey County Crop report 2012). Scott (1964) re- pseudocelli dorsally on the head and body (Fjellberg ported that Onychiurus armatus Tullberg (¼ Prota- 1998). Unlike other springtails, P. fimata lacks a furcula, phorura armata Tullberg) and Onychiurus and when disturbed does not jump but instead curls pseudarmatus Folsom were pests of a wide range of up. Many onychiurids primarily reproduce partheno- vegetable crops including lettuce (L. sativa), celery genically (Christiansen 1964); however, sexual repro- (Apium graveolens var. dulce Miller), broccoli (Brassica duction is also widespread (Larsen et al. 2009). The oleracea var. italica Plenck), cauliflower (Brassica species was originally described from Switzerland and oleracea L. var. botrytis), sugar beet (Beta vulgaris L.), seems to be widely distributed in Europe (Pomorski 1998, Fjellberg 1998), but has not been previously reported from the United States under the name P. fimata. Based on pseudocelli number, most records 1 University of California Cooperative Extension, 1432 Abbott of P. armata reported in Christiansen and Bellinger Street, Salinas, CA 93901. (1998) appear to refer to P. fimata, suggesting that the 2 Corresponding author, e-mail: [email protected]. species is widespread throughout the country. How- 3 Hartnell College, 411 Central Ave., Salinas, CA 93901. 4 Illinois Natural History Survey, Prairie Research Institute, ever, other members of the P. armata species group University of Illinois, 1816 S. Oak St., Champaign, IL 61820. with the same pseudocelli number might be present in VC The Authors 2015. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For Permissions, please email: [email protected] 2JOURNAL OF ECONOMIC ENTOMOLOGY other localities and species determination will require demonstrated. The major objectives of the present examination of individuals from different populations. study were to document 1) the ability of P. fimata to in- The taxonomy of North American members of the jure germinating seeds of lettuce in laboratory and P. armata species complex has not been fully worked field, and 2) to characterize the feeding injury of out. Christiansen and Bellinger (1998) follow Bo¨dvars- P. fimata on germinating seeds and seedlings of lettuce. son (1970) and include forms with at least four combi- Our hypothesis is that the subterranean springtail, nations of pseudocelli and chaetotaxy details under the P. fimata, which is detected in the lettuce and brassica name P. armata. fields of the Salinas Valley could affect crop stands Springtails occur in diverse habitats worldwide through feeding. (Hopkin 1997) and are generally considered as benefi- cial arthropods because they aid in the decomposition Materials and Methods of decaying plant material by feeding, thereby contrib- uting to the cycling of carbon and nitrogen, which in Species Identification. Individuals collected from turn improves soil health and structure (Coleman et al. the soil in the Salinas Valley in association with lettuce 1983, Hopkin 1997, Filser 2002). P. fimata is primarily were identified using the keys provided in Christiansen known to feed on soil fungi (Crist and Friese 1993, Jør- and Bellinger (1998), Fjellberg (1998),andPomorski gensen et al. 2003) but also feeds on live plant roots (1998). A subset of individuals of the same species (Endlweber et al. 2009). However, there are several re- were reared in the laboratory and used for all the stud- ports of springtails as pests of crops reducing yields ies presented in this manuscript. The voucher speci- and productivity. The onychiurids, especially P. fimata, mens were deposited in the University of California have been associated with feeding damage to germinat- Cooperative Extension, Entomology Laboratory in Sali- ing sugar beet seeds (Baker and Dunning 1975, Boetel nas, CA. et al. 2001, Brown 1983, Heijbroek et al. 1980, Hurej Springtail Rearing. P. fimata were collected from a et al. 1992)andsugarcane(Spencer and Stracener fieldinSalinas,CA,usingbeet(Be. vulgaris)rootsli- 1929, 1930). Folsomia candida Willem, a common soil ces. Beet root slices were placed 3-cm-deep subsur- springtail, has been reported feeding on poppy seeds, face of the soil for 2 d. The collected P. fimata were Papaver somniferum (L.) (Greenslade 2006), and weed reared in sealed plastic containers and were provided seeds such as Plantago major L. (Nietschke et al. with fish food (Wardley, The Hartz Mountain Corp., 2011). Foliage-feeding springtails such as lucerne flea, Secaucus, NJ) as nutrition at biweekly intervals. In the Sminthurus viridis (L.), and garden springtail, Bourle- container, a layer of clay soil (2 cm) was provided and liella hortensis (Fitch), attack several plant species in- covered with moist paper towel. The springtail contain- cluding Lucerne (Medicago sativa L.), clover (Trifolium ers were sprayed with tap water at biweekly intervals. sp.), and sugar beet (Be. vulgaris; Cleland 1955, Ireson The containers were maintained at 20C; 45% rela- 1984, 1993; Honma 1988). Thalassophorura encarpata tive humidity (RH), in complete darkness in the labora- (Denis) (identified as Onychiurus hortensis Gisin, in tory. A single colony of P. fimata was used in all the the original report) also is reported to feed on bean fo- laboratory experiments. liage (Edwards 1962). Laboratory Soilless Arena. Three soilless arena Growers in the Salinas Valley facing an irregular let- experiments were conducted in the laboratory. An tuce stand are usually uncertain about what caused the experiment unit or assay consisted of 4.5-cm-diameter problem and often blame the factors such as poor seed plastic petri dish (Fischer Scientific, Pittsburgh, PA) quality, planting error, irregular irrigation timing or dis- with a Whatman No.1 filter paper (GE healthcare UK tribution, high salt levels in the soil or water, soilborne Ltd., Little Chalsont, Buckinghamshire, United King- pathogens of seedlings, bulb mites, and garden sym- dom). The filter paper was soaked in 50 ml of distilled phylan (Scutigerella immaculata Newport) feeding for water for 5 s before being added to the petri dish. the losses. Also, several springtails were collected from Twenty-five uncoated and untreated ‘Bibb Heirloom’ the soil associated with lettuce and it is not clear if they lettuce seeds (L. sativa; Livingston Seed Co.,