Interactions Among the Entomopathogenic Fungus, Paecilomyces Fumosoroseus (Deuteromycotina: Hyphomycetes), the Parasitoid, Aphel
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Biological Control 22, 51–59 (2001) doi:10.1006/bcon.2001.0950, available online at http://www.idealibrary.com on Interactions among the Entomopathogenic Fungus, Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes), the Parasitoid, Aphelinus asychis (Hymenoptera: Aphelinidae), and Their Aphid Host Antonio L. M. Mesquita*,† and Lawrence A. Lacey*,‡,1 *European Biological Control Laboratory, USDA/ARS, Campus International de Baillarguet, CS 90013, Montferrier sur Lez, 34980 St. Gely du Fesc, Cedex, France; †EMBRAPA/CNPAT, Rua Dra. Sara Mesquita, N 2270, Bairro Pici, Cx. Postal 3761, 60511-110 Fortaleza, Ceara´, Brazil; and ‡USDA-ARS-Yakima Agricultural Research Laboratory, 5230 Konnowac Pass Road, Wapato, Washington 98951 Received August 16, 2000; accepted April 2, 2001 posure varied from 20.3 to 23.0 and was not signifi- The interactions among the hyphomycete, Paecilo- cantly different when the aphids were first exposed to myces fumosoroseus, the Russian wheat aphid, Diura- the parasitoids and then treated with P. fumosoroseus phis noxia, and its common parasitoid, Aphelinus asy- 24, 48, 72, and 96 h after exposure. No difference in chis, were investigated under laboratory conditions to time between oviposition and emergence of the F1 determine if fungal infection of the aphid host had an generation of the parasitoid for groups treated with effect on oviposition and feeding behavior of the fe- the fungus and the untreated groups was noted, but male parasitoid and on development of parasitoid the percentage of emergence of the F1 generation of A. progeny. Aphids were first treated with 2 times the asychis was significantly lower among the aphids ex- ؋ LD95 of P. fumosoroseus for D. noxia third instars (5.2 posed to the parasitoid and treated with the fungus 4 2 10 conidia/cm ). At various intervals afterward they 24 h afterward than for the untreated aphids. Various were exposed to 4- to 5-day-old mated parasitoid fe- findings of this study demonstrate the potential of syn- males for 1 h. Various combinations of treatments ergistic interaction of P. fumosoroseus and A. asychis were examined: exposure to P. fumosoroseus and par- for the biological control of D. noxia. asitization simultaneously; exposure to parasitoids Key Words: Paecilomyces fumosoroseus; Diuraphis 24–96 h after treatment with fungus; exposure to the noxia; Aphelinus asychis; Russian wheat aphid; micro- parasitoid alone; and fungal treatment alone. The av- bial control; interaction. erage number of aphids probed by the parasitoids was not significantly influenced by host infection with P. fumosoroseus, but duration of ovipositor insertion was Competition between microorganisms and multicel- influenced by the length of the time interval between lular animals for nutrition and other requisites is per- exposure to P. fumosoroseus and subsequent exposure vasive throughout nature (Hochberg and Lawton, to the parasitoid. Parasitoid females spent consider- ably less time with their ovipositor inserted in dead 1990). Despite the competition, there is evidence for aphids and in aphids that had been exposed to P. mechanisms that reduce antagonistic interaction be- fumosoroseus 72 h prior to contact with the parasi- tween natural enemies vying for common insect hosts toids. The number of dead aphids fed upon by parasi- (Hochberg and Lawton, 1990; Brooks, 1993). Several toids was significantly less than in the other treatment studies on fungal pathogens and parasitoids of ho- groups. The percentage of successfully parasitized D. mopterous insects have revealed the avoidance of fun- noxia was significantly reduced as a function of the gal-infected hosts by ovipositing wasps and a degree of time between treatment with P. fumosoroseus and host immunity to fungal infection induced by parasi- parasitoid oviposition. The effect of previous parasit- toid larvae within the host (Milner et al., 1984; Powell ization on the ability of the fungus to infect aphids and et al., 1986; Brobyn et al., 1988; Poprawski et al., 1992; interfere with parasitoid development within host Fransen and van Lenteren, 1994). aphids was also investigated. The number of mummies Aphelinus asychis Walker (Hymenoptera: Aphelini- produced by two female A. asychis during 24 h of ex- dae) is a common parasitoid of the Russian wheat aphid Diuraphis noxia (Mordvilko) (Homoptera: Aphi- 1 didae) and other aphids. In addition to ovipositing into To whom correspondence should be addressed at USDA-ARS- YARL, 5230 Konnowac Pass Road, Wapato, WA 98951. Fax: (509) aphids, A. asychis females immobilize aphids by sting- 454-5646. E-mail: [email protected]. ing and subsequently feed upon their hemolymph and 51 1049-9644/01 52 MESQUITA AND LACEY other tissues for longevity and production of eggs (Bai two times the LD95 of P. fumosoroseus for third instar and Mackauer, 1990b). The proportion of aphids killed D. noxia. by host feeding at times exceeds that due to parasit- Insects. Colonies of A. asychis and D. noxia derived ization (Mesquita et al., 1997). Poprawski et al. (1992) from collections in the vicinity of Montpellier, France, reported protection of D. noxia from infection by the were used for all tests. Detailed procedures for their entomophthoralean fungus Zoophthora radicans production in the laboratory were as described by Mes- (Brefeld) Batko after parasitization by A. asychis. The quita et al. (1996, 1997). Briefly, this involved rearing fungus, Paecilomyces fumosoroseus Brown and Smith D. noxia on barley plants (Hordeum vulgare L.) in (Deuteromycotina: Hyphomycetes), has been reported ventilated plastic cages in incubators at 22–24°C, 55– from whiteflies and over 40 other insects, but is not 65% relative humidity (RH), and photoperiod of 16:8 commonly reported from aphids (Samson, 1974; Smith, (L:D) until they matured to third instars and then 1993; Lacey et al., 1996). Laboratory and field studies exposing them to mated A. asychis females. Four- to revealed its potential for control of D. noxia in combi- 5-day-old A. asychis females were used for all experi- nation with A. asychis (Mesquita et al., 1996, 1997). ments except those to determine longevity. However, under conditions of high humidity, P. fu- P. fumosoroseus on development, longevity, and fe- mosoroseus can have direct negative impact on A. asy- cundity of A. asychis when the host was first exposed to chis (Lacey et al., 1997). the parasitoid and then treated with the fungus. Four The objective of this study was to determine if the replicate tests were conducted on separate dates, each same antiantagonistic mechanisms reported for hyme- using five groups of 30 third instar aphids. Each group nopterous parasitoids and fungal pathogens of a com- of aphids was placed on three barley leaves (5 cm long) mon host would also occur with a fungal pathogen and the bases of which were inserted in pieces of moist parasitoid that are not commonly found in nature as- cotton and exposed to two 4- to 5-day-old female A. sociated with the same host. Specifically, we present asychis for 24 h. The exposure took place in a rectan- information on the influence that the stage of infection gular plastic box (9 ϫ 6 ϫ 2 cm) with a 2.5-cm-diameter of D. noxia by P. fumosoroseus can have on oviposition, hole in the lid covered with screen (0.1 mm mesh) for feeding behavior, development time, percentage of ventilation. After 24 h, the parasitoids were removed emergence, sex ratio, longevity, and size of female A. and the leaves bearing live aphids were transferred to asychis. We also investigated the effect of prior para- petri dishes that had each been lined with a 9-cm- sitization by the wasp on the ability of the fungus to diameter filter paper. Parafilm (5 ϫ 2.5 cm) prevented produce subsequent infection and interfere with para- contact between the moist cotton and the filter paper. sitoid development within host aphids. The petri dish covers were also ventilated with a screened hole. For each replicate test, one group of MATERIALS AND METHODS parasitized aphids (23–24 individuals) was sprayed with 2 ϫ LD95 P. fumosoroseus either 24, 48, 72, or 96 h Fungus. The strain of P. fumosoroseus (ARSEF after exposure to the parasitoids. The fifth group of 3877) used for bioassays was isolated from Bemisia parasitized aphids was treated with distilled water tabaci (Gennadius) in Multan, Pakistan (Lacey et al., only. Additionally, four replicate dishes with 30 aphids 1993). After passage of the fungus through D. noxia, it each that were not exposed to parasitoids were sprayed was grown on Sabouraud maltose-dextrose agar with with fungus only, and an equal number of dishes were yeast extract (SMDAY) and subsequently prepared for treated with distilled water only. In the two latter bioassay using the procedures described by Mesquita et cases, the insects from each repetition were sprayed al. (1996). The average viability of conidia used in the over 4 consecutive days, coinciding with the treatment various tests was 94.7% as determined on SMDAY of aphids that had been parasitized and subsequently using standard techniques (Goettel and Inglis, 1997). treated with the fungus. During the first 24 h following This involved inoculating a 9-cm petri plate containing fungal treatment, the petri dishes were hermetically SMDAY medium with 100 l of a suspension contain- sealed with parafilm to maintain saturated humidity ing 106 conidia/ml and counting the number of germi- and enable germination. The covers were then replaced nated conidia/100 conidia in four separate areas on the by others with mesh-covered apertures as described plate after incubation at 24°C for 18–20 h. This process above to allow aeration and prevent condensation. The was performed for each separate batch of P. fumosoro- barley leaves were replaced with fresh ones every 3 seus. Applications of P. fumosoroseus were made with 2 days. Dead aphids were recorded daily for 1 week and ml aqueous suspensions of 12- to 14-day-old conidia were placed on water agar (3 g of agar/liter of water) to (1.4 ϫ 108 conidia/ml) as described by Mesquita et al.