Evaluation of Two Biotypes of Euseius scuta lis (: ) as Predators of Bemisia tabaci (Homoptera: Aleyrodidae)

DALE E. MEYERDIRK AND DONALD L. COUDRIET Boyden Fruit and Vegetable Insects Research Unit, Agricultural Research Service, U.S. Department of Agriculture, University of California, Riverside, California 92521 Downloaded from https://academic.oup.com/jee/article/79/3/659/2214652 by guest on 01 October 2021 J. Econ. Entomol. 79: 659-663 (1986) ABSTRACT Two predaceous biotypes of Eusetus scutalts (Athias-Henriot) were eval- uated as biological control agents of Bemtsta tabact (Gennadius). One biotype was originally collected on citrus in Morocco; the other was collected on lantana in Jordan. Both biotypes survived well on ice plant pollen, but their survival varied when fed various stages of B. tabact. The Jordanian mite had longer survival when fed eggs or first or second instars of the whitefly. Eggs, followed by first instars, were the most suitable whitefly host stage fed to the ; the least suitable stage was the second instar. Egg consumption by both mites showed preference for freshly laid eggs. Although the mean survival rate was 22.9 days, one Jordanian biotype survived 69 days when fed whitefly eggs. Oviposition periods did not extend beyond 16.6 days for either biotype. The Jordanian biotype showed higher fecundity, longer ovipositional period, and longer survival when fed various stages of B. tabact than the Moroccan biotype. Potential use of the Jordanian mite for biological control purposes appears promising for regulation of B. tabact in California.

Euseius scutalis (Athias-Henriot) is a common the world (Costa 1976) and recently has become a phytoseiid mite with a cosmopolitan distribution serious vector of three virus disease agents (squash in the Middle East and North Africa on a variety leaf curl, lettuce infectious yellows, and cotton leaf of host plants including Citrus sp. (Porath & Swir- crumple viruses) in Southern California (Duffus & ski 1965), Vitis sp. (Daneshvar 1980), Hibiscus es- Flock 1982). Chemical control is limited because culentus L. and Gossypium sp. (Narayanan & Kaur of the whitefly's behavior-i.e., adult feeding, 1960), and Gossypium herbaceum L. (Swirski & mating, oviposition, and larval development oc- Amitai 1965). It is considered synonymous with curring on the underside of its host's leaves. Thus, Typhlodromous scutalis (Athias-Henriot 1958), canopy penetration of aerially applied pesticides Amblyseius rubini Swirski & Amitai, A. gossipi El- has not been effective (Johnson et al. 1982). Pes- badry, and A. delhiensis Narayanan & Kaur (Wy- ticide resistance to organophosphates and pyre- soki & Bolland 1983, Bounfour 1985) according to throids has also developed (Prabhaker et al. 1985). Bounfour (1985). The biology and ecology of E. This pesticide resistance plus the evidence of re- scutalis from Morocco was studied by Bounfour productive stimulation by pesticides (Dittrich et (1985). E. scutalis has been reported (as E. rubini) al. 1985) has prompted research on biological con- feeding not only on spider mites, but also on trol of B. tabaci. whiteflies (Aleyrodidae) and other foods (Swirski The purpose of our investigation was to evaluate et al. 1967a, Wysoki & Cohen 1983). This phe- two predaceous mite biotypes of E. scutalis from nomenon of phytoseiid mites feeding on whiteflies different geographical locations and different host is not uncommon. The sweet potato whitefly, Be- plants as predators of B. tabaci, and to determine misia tabaci (Gennadius), has been reported as prey if either could serve as a potential biological con- of Amblyseius swirski (Athias-Henriot) (Swirski et trol agent of this whitefly species. al. 1967a), E. scutalis (as E. rubini) (Teich 1966, Swirski et al. 1967a), Euseius aleyrodis (Elbadry) Materials and Methods (Elbadry 1967, 1968, Gameel1971), A. limonicus (Garman & McGregor) (Swirski & Dorzia 1968), One of the biotypes of E. scutalis was collected A. chilenensis Dosse and Eusieus hibisci (Chant) from citrus in Marrakech, Morocco, by James (Swirski et al. 1970, Meyerdirk & Coudriet 1985), McMurtry (Division of Biological Control, Uni- T. sudanicus Elbadry (Gameel1971), T. medani- versity of California, Riverside, Calif.). No obser- cus Elbadry (Elbadry 1967), T. athiasae (Swirski vations were made to determine associations with et al. 1967b), and T. occidentalis Nesbitt (Swirski whiteflies. The other biotype was collected from & Dorzia 1969). lantana in association with B. tabaci in the Jordan B. tabaci is reported to be the most economi- Valley of Jordan by D.E.M. cally important whitefly vector of plant viruses in Laboratory rearing techniques described by

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plant pollen, Malephora crocea Jacques, and fresh eggs of Pacific spider mite, Tetranychus pacificus McGregor, were used as the main food source in the stock culture and were added every 3 or 4 days. The experimental arenas consisted of one set of cotton-leaf disks free of B. tabaci and others con- taining either freshly laid eggs (<24 h old) or first > or second instars of the whitefly. Whitefly host ma- I- ...J terial was changed every 3 days. M. crocea pollen c( I- was added every 3 days to whitefly-free cotton a: disks. Disks were also placed with the upper leaf o ::E surface down on the water-saturated polyurethane Downloaded from https://academic.oup.com/jee/article/79/3/659/2214652 by guest on 01 October 2021

I- MOROCCO pads and labeled. A disk (6 mm diam) of dark ~ 100 green blotter paper, placed on each cotton leaf u a: disk, served as the ovipositional site for E. scutalis. ~ 80 E. scutalis adult females from each biotype were individually isolated and held for mating with one 60 or two males for 24 h without a food source. One E. scutalis female of each biotype was then iso-

40 Food Supply lated on each of 25 cotton leaf disks with either 8 Pollen b ~lllllW Eggs pollen, eggs, or first or second instars of B. tabaci, 20 c !i.l..iL.b..A&.l 1 sl inst8r or no food. An abundant supply of host material d ~tabaci 2nd inslsr e No Food was available to each adult mite for a 3-day pe- a riod. Laboratory observations were made every 24 5 10 15 20 25 30 35 40 h; number of eggs laid per female mite and mor- DAYS AFTER MATING tality were recorded. When mites were fed only Fig. 1. Accumulative mortality curves of adult fe- on whitefly eggs, the number of eggs consumed males of two E. scutalis biotypes fed different host ma- per day was recorded. When pollen or first or sec- terial. ond instars of the whitefly were provided as food material, only the total number of eggs laid by each biotype of E. scutalis plus mortality were Tanigoshi et al. (1981) were used. Excised cotton recorded. E. scuta/is eggs were randomly collected leaf disks (2 cm diam) were placed with upper from each feeding group and monitored to deter- leaf surfaces down on a water-saturated polyure- mine their viability. thane pad in a stainless steel pan (20 cm square E. scutalis survival rates were determined by by 2.5 cm deep). A cellucotton barrier (ca. 1.25 transferring 25-50 protonymphs (1 day old) pre- cm wide) saturated with water was placed along viously fed pollen to cotton leaf disks (five nymphs the periphery of each leaf to prevent escape of per disk) containing either eggs or first or second mites from the leaf arena. Ovipositional sites for instars of B. tabaci or pollen. Leaf disks and food the stock culture consisted of several cotton fiber sources were changed every 3 or 4 days until the strands beneath a plastic coverslip (22 mm). Ice mites died. Those mites that wandered off the sub-

UJ 26 ...J « 24 :::l: ~ 22 JORDAN I , 20 MOROCCO 0 Cl Morocco strain UJ 18 :::l: discontinued :J Ul 16 Z 0 14 U Ul 12 CJ CJ 10 UJ 0 8 z 6 z « UJ ::!"

Fig. 2. B. tabaci egg consumption by adult females of two E. scutalis biotypes. June 1986 MEYERDIRK & COUDRIET: E. scutalis PREDATION ON B. tabaci 661

Table 1. Oviposition period and fecundity of two biotypes of E. scutalis when fed different host materials

f no. of days Parameter Biotype B. tabacl Pollen No food Eggs 1st instar 2nd instar Oviposition period (days) Jordan 14.5a 15.6a 12.4a 2.7a 0.3a Morocco 16.6a 9.2b 4.0b 2.0a 0.5a % eggs laid ~14 days Jordan 84.1a 87.8a 9l.6a 100a l00a Morocco 80.2a 97.9b 98.0a 100a l00a Total no. eggs laid/9 Jordan 15.0a 16.8a 9.5a l.6a 0.3a Morocco 35.7b 12.4b 5.9b 2.3a 0.8a No. eggs/9/day Jordan l.Oa Ua 0.6a 0.5a 0.3a Morocco 2.2b l.3a l.3b l.Oa 0.2a Downloaded from https://academic.oup.com/jee/article/79/3/659/2214652 by guest on 01 October 2021

Means within a column and parameter followed by the same letter are not significantly different (P < 0.01; Duncan's [1951] multiple range test). strate and could not be found were not included extended periods of time, which may be attributed in calculating the percentage of survival. to its association with this whitefly species on lan- B. tabaci used in these studies were collected as tana. Both biotypes were short-lived when no food adults from Lantana camara L. in the Imperial source was offered. The whitefly second instar was Valley, Calif., in 1982 and subsequently reared on not readily fed upon by either biotype, as denoted cotton in a greenhouse at Riverside, Calif. Seasonal by the high mortality early in the test. Whitefly greenhouse temperatures ranged from 16 to 38°C. eggs or first or second instars appeared more ac- Additional fluorescent lighting was supplied on a ceptable to the Jordanian biotype. At 22 days, only 12:12 (L:D) photoperiod throughout the year. B. 8% of the Moroccan biotype were still alive when tabaci eggs were obtained by confining 25-30 fed on whitefly eggs compared with 36% of the adults on cotton foliage for 24 h with leaf-clip adult mites from Jordan. cages (2.5 cm diam by 2.5 cm high). The cages The consumption of eggs per adult female on a limited the leaf area available for egg deposition, daily basis showed a definite trend for both bio- thereby reducing the time required to obtain suf- types: a high consumption of 1-day-old eggs and ficient numbers of eggs on a leaf disk before ex- reduced feeding as the eggs aged (Fig. 2). The posure to E. scutalis biotypes. First instars were high peak of consumption every 3 or 4 days rep- obtained from eggs collected in the same manner resents the first day of feeding after the introduc- and then held at 26.7 ± 1°C and 60 ± 5% RH with tion of freshly laid whitefly eggs. This difference a photoperiod of 12:12 (L:D) until hatching (5-7 in predaceous mite feeding behavior on whitefly days). This temperature and relative humidity were eggs has been observed in other predaceous mites maintained for all tests conducted. First-instar (GameeI1971, Meyerdirk & Coudriet 1985). The crawlers were allowed to settle before being eval- hardening of the egg's chorion may make it diffi- uated as prey. Second instars were obtained from cult for the mites to feed. During the first 10 days, eggs 8-10 days after oviposition using these same the Moroccan biotype consumed approximately rearing conditions. two more eggs per day than the Jordanian biotype. Data were analyzed by analysis of variance; The study of the Moroccan biotype fed eggs was Duncan's (1951) multiple range test was used for terminated on the 22nd day of observation; two mean separation. adults were still alive. The Jordanian biotype was allowed to feed until all mites had died. One Jor- danian adult female that fed on eggs lived for 69 Results and Discussion days, although the mean longevity for that biotype The cumulative mortality curves of the adult was 22.9 days. The egg consumption tests for the females of E. scutalis biotypes when fed pollen two biotypes were run on different dates, which versus different stages of B. tabaci varied substan- accounts for the misalignment of peak feeding be- tially (Fig. 1). Both the Jordanian and Moroccan tween the two biotypes. biotypes survived well on pollen alone, with 50% The oviposition periods did not extend beyond mortality occurring at 18 and 21 days, respective- a mean of 16.6 days for either biotype (Table 1). ly. The Jordanian biotype survived longer when The Jordanian E. scutalis had a significantly (P < fed on the different stages of B. tabaci (50% mor- 0.01) longer ovipositional period when fed B. ta- tality at 22, 13, and 6 days when fed whitefly eggs, baci eggs and first instars; overall, this biotype pro- first instars, or second instars, respectively, com- duced more eggs on the same whitefly stages. The pared with the Moroccan biotype with 50% mor- Moroccan biotype performed significantly (P < tality at 11, 3, and 2.5 days, respectively). E. scu- 0.01) better on pollen; a mean total of 35.7 eggs talis from Jordan appeared more capable of was produced compared with 15.0 eggs laid by preying on the different stages of B. tabaci for the Jordanian E. scutalis. The mean number of 662 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 79, no. 3

POllEN lsi INSTAR lARVAE W 3.6 3.0 !!:~ -l Morocco·-. < Jordan ._-. ~ 3.0 2.5 . W u.. 2.4

0 1.8 W , () , \ ::l 1.2 :~._.. ,...\ 0 0.5 /. . • .-... .' l 0 0.6 ::tv.~~~!• \,'\V\., .- .•••-~... ,,,, •• " "\I II: .•. ,' , ,;: '.1 " a.. 0.0 •. 0.0 . '-'-'-' (J') 2 4 6 8 10 12 14 16 18 20 22 24 2 4 6 8 10 12 14 16 18 20 22 24 26 (!) (!) ~ tabaci EGGS 1.4 ~ labaci 2nd INSTAR lARVAE W 2.0 Downloaded from https://academic.oup.com/jee/article/79/3/659/2214652 by guest on 01 October 2021 II: W ;\ m 1.5 \//\:.,. • I 1.0 . /" \-'- , \ ~ 0.81'2/'-'\ ::l ~ ,,,,,'\1 \'\\ ./\ \ Z 1.0 , , , .-- -'--'7-" ' 0.6 . ,', ,\ ~~' ~.\ Z i ,! / 'V'--:\j\," . « 0.5 W ~ I . '/·\A/\..·~::.-----/ "".,/ \.,-,,-.---'-""',,,,. ----..----. 0.0 0.0 2 4 6 8 10 12 14 16 18 20 22 2 4 6 8 10 DA YS AFTER MATING Fig. 3. Daily fecundity of two E. scutalis biotypes when fed different host materials.

eggs laid per day per female was significantly (P The Moroccan mite reached the adult stage in < 0.01) higher for the Moroccan mite when fed 5-6 days when fed pollen and 6-7 days when fed pollen and white£1y first instars (Fig. 3). The Mo- white£1y stages; the Jordanian mite required 7-8 roccan mite laid 97.9% of its egg complement dur- days when fed pollen as compared with 8-9 days ing the first 14 days when fed white£1y eggs; this when fed B. tabaci stages. At least 80% of the F, value was significantly (P < 0.01) greater than that eggs laid by both species of mites were viable when of the other biotype (87.8%), but no differences fed B. tabaci or pollen. were observed with other host material. Both biotypes may be potential biological con- Both E. scutalis biotypes, from I-day-old pro- trol agents of B. tabaci in the field, although the tonymphs, were able to complete development to Jordanian mite appears slightly better than the the adult stage when fed a combination of eggs or Moroccan biotype because of higher fecundity, first or second instars of the white£1y (Table 2). On longer ovipositional period, and longer survival this diet, 47% of the Jordanian mites survived to when feeding on B. tabaci. The Moroccan biotype maturity as compared with 64.7% for the other appears to have a higher reproductive potential if biotype (P > 0.05). Swirski & Dorzia (1968, 1969) pollen is present. Future testing should be con- reported survival rates of 86.9% for A. limonicus ducted with the biotypes to determine their feed- and 65.2% for T. occidentalis when these species ing preference for pollen compared with B. tabaci were fed a combination of B. tabaci stages. Mey- and evaluate their survival rate under field con- erdirk & Coudriet (1985) reported a 75% survival ditions. rate for E. hibisci fed the same white£1y stages. The Jordanian mite had a significantly (P < 0.05) higher survival rate (91.7%) when fed pollen as Acknowledgment compared with the Moroccan biotype (73.9%). We thank J. Fargerlund (Boyden Laboratory, ARS- USDA, Riverside, Calif.) and N. Prabhaker (Univ. of California, Riverside) for their assistance. Table 2. Survival of E. scutalis biotypes from first in- stars to adults when fed on different host material

Biotype Host" n % survival References Cited Jordan Pollen 50 91.7a Athias-Henriot, C. 1958. Contribution a la connais- Morocco Pollen 25 73.9b sance du genre Typhlodromus Sheuten (Acariens: Morocco B. tabaci 25 64.7bc Parasitjformes, Phytoseiidae). Description de deux Jordan B. tabaci 50 46.9c especes nouvelles d'algerie et de des especes du Means followed by the same letter in the column are not sig- groupe finlandicus.Rev. Pathol. Veg. Entomol. Agric. nificantly different (P < 0.05; Duncan's [1951] multiple range 37: 179-186. test). Bounfour, M. 1985. Biology and ecology of Euseius a B. tabaci: all life stages present except adults and renewed scutalis (Athias-Henriot)(Acarina:Phytoseiidae).M.S. every 3 to 4 days. thesis, University of California, Riverside. June 1986 MEYERDIRK & COUDRIET: E. scutalis PREDATION ON B. tabaci 663

Costa, A. S. 1976. Whitefly transmitted plant dis- Swirski, E. & N. Donia. 1968. Studies on the feed- eases. Annu. Rev. Phytopathol. 14: 429-449. ing, development, and oviposition of the predaceous Daveshvar, H. 1980. Some predatory mites from mite Amblyseius limonicus Garman and McGregor northern and western Iran. Entomol. Phytopathol. (Acarina: Phytoseiidae) on various kinds of food sub- Appliq. 48: 15-87. stances. Isr. J. Agric. Res. 18: 71-75. Dittrich, V., S. O. Hasson & G. H. Ernst. 1985. Su- 1969. Laboratory studies on the feeding, develop- danese cotton and the whitefly: a case study of the ment, and fecundity of the predacious mite Typh- emergence of a new primary pest. Crop Prot. 4: 161- lodromus occidentalis Nesbitt (Acarina: Phytosei- 176. idae) on various kinds of food substances. Isr. J. Agric. Duffus, J. E. & R. A. Flock. 1982. The whitefly trans- Res. 19: 143-145. mitted disease complex of the desert Southwest. Cal- Swirski, E., S. Amitai & N. Donia. 1967a. Labora- if. Agric. 36: 4, 6. tory studies on the feeding, development and repro- Duncan, D. B. 1951. A significant test for differences duction of predaceous mites Amblyseius rubini Swir-

between ranked treatments in an analysis of vari- ski and Amitai and Amblyseius swirski Athias Downloaded from https://academic.oup.com/jee/article/79/3/659/2214652 by guest on 01 October 2021 ance. Va. J. Sci. 2: 171-189. (Acarina: Phytoseiidae] on various food substances. Elbadry, E. A. 1967. Three new species of phytoseiid Isr. J. Agric. Res. 17: 101-119. mites preying on the cotton whitefly, Bemisia tabaci, 1967b. Laboratory studies on the feeding, develop- in the Sudan (Acarina: Phytoseiidae). Entomologist ment and oviposition of the predaceous mite Ty- 100: 106-111. phliodromus athiasae P. and S. [Acarina: Phytosei- 1968. Biological studies on Amblyseius aleyrodis, a idae] on various kinds of food substances. Isr. J. Agric. predator of the cotton whitefly (Acarina: Phytosei- Res. 17: 213-218. idae). Entomophaga 13: 323-329. 1970. Laboratory studies on the feeding habits, post- Gameel, O. I. 1971. The whitefly eggs and first larval embryonic survival, and oviposition of the preda- stages as prey for certain phytoseiid mites. Rev. ZooI. ceous mites, Amblyseius chilenensis Dosse and Am- Bot. Afr. 84: 79-82. blyseius hibisci Chant (Acarina: Phytoseiidae) on Johnson, W., N. Toscano, H. T. Reynolds, E. S. Sylves- various kinds of food substances. Entomophaga 15: ter, K. Kido & E. T. Natwick. 1982. Whiteflies 93-106. cause problems for Southern California growers. Cal- Tanigoshi, L. K., J. Fargerlund & J. T. Nishio-Wong. if. Agric. 36: 24-26. 1981. Significance of temperature and food re- Meyerdirk, D. E. & D. L. Coudriet. 1985. Predation sources to the developmental biology of Amblyseius and developmental studies of (Chant) hibisci (Chant) (Acarina: Phytoseiidae). Z. Angew. (Acarina: Phytoseiidae) feeding on Bemisia tabaci Entomol. 92: 409-419. (Gennadius) (Homoptera: Aleyrodidae). Environ. Teich, Y. 1966. Mites of the family Phytoseiidae as Entomol. 14: 24-27. predators of the tobacco whitefly, Bemisia tabact Narayanan, E. S. & R. B. Kaur. 1960. Two new Gennadius. Isr. J. Agric. Res. 16: 141-142. species of the genus Typhlodromus Scheuten from Wysoki, M. & H. R. Bolland. 1983. Chromosome India (Acarina: Phytoseiidae). Proc. Indian Acad. Sci. studies of phytoseiid mites (Acari: Gamasida). Int. J. 51: 1-8. Acarol. 9: 91-94. Porath, A. & E. Swirski. 1965. A survey of phyto- Wysoki, M. & M. Cohen. 1983. Mites of the Family seiid mites (Acarina: Phytoseiidae) on citrus, with a Phytoseiidae (Acarina: ) as predators of description of one new species. Isr. J. Agric. Res. 15: the Japanese bayberry whitefly, Parabemisia myri- 87-100. cae Kuwana (Hom., Aleyrodidae). Agronomie 3: 823- Prabhaker, N., D. L. Coudriet & D. E. Meyerdirk. 825. 1985. Insecticide resistance in the sweetpotato whitefly, Bemisia tahaci (Homoptera: Aleyrodidae). Received for publication 30 October 1985; accepted J. Econ. Entomol. 78: 748-752. 25 February 1986. Swirski, E. & S. Amitai. 1961. Some phytoseiid mites of Israel with a description of two new species. Isr. J. Agric. Res. 11: 193-202.