PROC. ENTOMOL. SOC. WASH. 101(3). 1999. pp. 640-644 HYPERPARASITISM BY ABLERUS CLISIOCAMPAE ASHMEAD (HYMENOPTERA: APHELINIDAE) David Kattari, George E. Heimpel, Paul J. Ode, and Jay A. Rosenheim Department of Entomology, University of California, One Shields Avenue, Davis, CA 95616, U.S.A.; (GEH) current address: Department of Entomology, University of Min- nesota, St. Paul, MN 55108, U.S.A. (e-mail: [email protected]): (PJO) current ad- dress: Department of Entomology, Biological Control Facility, Texas A&M University, College Station, TX 77843-2475, U.S.A. Abstract. —Ablerus clisiocampae (Hymenoptera: Aphelinidae) is known as a parasitoid both of diaspidid scale insects and lepidopteran eggs. Although it has been suspected that A. clisiocampae is a secondary (hyper) parasitoid of diaspidid scale insects, direct evidence of hyperparasitism has been lacking. We used observation and rearing data from field- collected material to demonstrate hyperparasitism of three species of diaspidid scale in- sects, and primary parasitism of two species of parasitoid wasps by A. clisiocampae. Ablerus clisiocampae was found feeding on Aphytis aonidiae (Hymenoptera: Aphelinidae) attacking San Jose scale {Quadraspidiotiis perniciosus) and Comperiella bifasciata (Hy- menoptera: Encyrtidae) attacking California red scale {Aonidiella aurantii) and yellow scale (A. citrina). Ablerus clisiocampae were associated with pupal Aphytis aonidiae and pupal and pharate adult C. bifasciata. All Ablerus clisiocampae reared for this study were females. Key Words: Ablerus clisiocampae, Aphytis aonidiae, Comperiella bifasciata, hyperpar- asitism, parasitoids, Quadraspidiotus perniciosus, San Jose scale, Aonidiella aurantii, California red scale, Aonidiella citrina, yellow scale The aphelinid parasitoid Ablerus clisio- scure scale, Melanaspis obscura (Com- campae Ashmead has been reared both stock) (Homoptera: Diaspididae), and that from lepidopteran eggs and diaspidid scale its phenology was consistent with a hyper- insect hosts (Darling and Johnson 1984, Po- parasitic life history. Although these lines laszek 1991). There has been confusion, of reasoning are consistent with hyperpar- however, regarding the exact host relation- asitism, the information required to distin- ships exhibited by this species. The genus guish between primary and secondary par- Ablerus has historically been considered asitism in this species has not been avail- largely or exclusively hyperparasitic (Vig- able to date. Here, we provide direct evi- giani 1984, 1990), and some authors have dence that A. clisiocampae hyperparasitizes assumed that A. clisiocampae attacks pri- primary parasitoids of three armored scale mary parasitoids of the hosts from which it insects (Homoptera: Diaspididae): the San has been reared (Muma 1959, Hughes Jose scale, Quadraspidiotus perniciosus 1960, Viggiani 1981). Also, Ehler (1995) (Comstock); the California red scale, Aon- found that A. clisiocampae was the smallest idiella aurantii (Maskell); and the yellow of a guild of parasitoids associated with ob- scale, A. citrina (Coquillet). VOLUME 101. NUMBER 3 641 San Jose Scale System resented a small fraction of the total number sampled. Between August and October of San Jose scale is a pest of fruit, nut, and 1994, we examined 1,462 adult female ornamental trees. Its most important natural scale insects, 19.7% of which were parasit- enemy in California is the parasitoid Aphy- ized by Aphytis aonidiae (GEH and JAR, tis aonidiae (Mercet) (Hymenoptera: unpublished data). Aphelinidae) (Gulmahamad and DeBach 1978a, Heimpel et al. 1996). Aphytis aoni- California Red Scale and Yellow diae lays eggs singly on the external surface Scale System of the scale insect under the scale cover, and The California red scale (CRS) and yel- larvae and pupae develop ectoparasitically low scale are important pests of citrus (Gulmahamad and DeBach 1978b, Heimpel worldwide, including California. Comper- et al. 1996). We encountered AZ?/^n/.9 clisio- iella bifasciata Howard (Hymenoptera: En- campae underneath San Jose scale covers cyrtidae) is a solitary parasitoid of both during a study aimed at quantifying para- CRS and the yellow scale, although it is sitism of San Jose scale by A. aonidiae on generally considered to be of secondary im- almonds. portance to Aphytis melinus DeBach as a We collected 20-cm twig samples from a control agent in many citrus growing re- 4 ha section of an organically managed al- gions (Flaherty et al. 1973, Blumberg and mond orchard in Sutter County, California, Luck 1990). Comperiella bifasciata is an that supported a moderate infestation of San endoparasitoid, laying one or a few eggs Jose scale (Heimpel et al. 1996). Samples inside the bodies of armored scales (Rosen- were taken to the laboratory, and scale in- heim and Hongkham 1996). At most, only sects were individually examined at 40 X. one egg survives to adulthood, and many Each scale insect was noted as being eggs become encapsulated by the host healthy, dead from causes, or par- unknown (Blumberg and Luck 1990, Ode and Rosen- asitized, and the identity and stage of each heim 1998). In a study examining host en- parasitoid was recorded. capsulation rates in the field, we encoun- were Samples taken during 1992, 1993 tered Ablerus clisiocampae along with the and 1994. Between August and October remains of C. bifasciata pupae and pharate 1994, we recovered twelve specimens of adults that had parasitized both CRS and Ablerus clisiocampae, all fe- of which were yellow scale (PJO, unpublished data). male. These individuals were discovered as Leaf samples infested with both species = = larvae (n 9) or pupae (n 3) and reared of armored scale were collected weekly to adulthood in glass vials. Two of the 9 from an organic mandarin orange grove in larvae were observed feeding ectoparasiti- Glenn County, California, between June cally on Aphytis aonidiae pupae, providing and October 1995. Scales were examined direct evidence of hyperparasitism (Fig. under a dissecting microscope at 40 X and la). In both of these cases, remains of the their condition was scored as described scale insect and the A. aonidiae pupa were above for the San Jose scale. When A. cli- clearly visible underneath the scale cover. siocampae individuals were found, they We did not find A. aonidiae or scale insect were always in association with the remains remains associated with the other 10 Able- of C. bifasciata. Overall, 2,391 female CRS rus clisiocampae. We were unable to clas- and yellow scales were examined, 875 of sify these cases as either primary or sec- which were parasitized by C bifasciata, ondary parasitism, and suspect that scale in- and approximately 400 of which were par- sect and/or Aphytis remains were lost dur- asitized by Aphytis (probably A. melinus). ing handling of the samples. Scale insects Ablerus clisiocampae was found to have associated with Ablerus clisiocampae rep- hyperparasitized C. bifasciata in 213 cases; 642 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON Fig. \. Ablerus cUsiocampae. a. Larva feeding on Aphytis aonidiae pupa, b. Larva feeding on a female Comperiella bifasciata pharate adult. VOLUME 101, NUMBER 3 643 in 27 of these cases, we clearly saw an A. AcKNOWLEDGMENTS clisiocampae larva feeding ectoparastically Thanks go out to Edward Sills and Ri- on C. bifasciata pharate adults (Fig. lb; chard Johansen for allowing us to use their PJO, unpublished data). We successfully land for this work. Aphytis aonidiae was these individuals to adulthood, and reared identified by David Rosen, Department of all A. clisiocampae were females. Voucher Entomology, Hebrew University of Jerusa- specimens of A. clisiocampae reared from lem, Rehovot, Israel, and Ablerus clisio- San Jose scale, and yellow scale have CRS campae was identified by Michael Schauff, deposited at the Bohart Insect Muse- been USDA Systematic Entomology Laboratory, um, University of California, Davis. Washington D.C. We thank Jane Adams and Francisco Hernandez for field and lab- Discussion oratory assistance. For advice on the man- rearing data and dissections of ar- Our uscript, we thank Les Ehler, Brook Murphy, developing parasitoids mored scales with and two anonymous reviewers. This work demonstrate that A. clisiocampae develops was supported in part by USDA grant as an obligate hyperparasitoid. Ableriis cli- #9202397 to J. A. Rosenheim, a University observed feeding on the pu- siocampae was of California Statewide IPM Project grant pae or pharate adults of ectoparasitic and to G. E. Heimpel and J. A. Rosenheim, and endoparasitic primary parasitoids, and no USDA NRIGCP award #94-37312-0960 to primary parasitism was observed despite R J. Ode. extensive sampling of primary host mate- rial. Literature Cited All of the Ablerus clisiocampae individ- Blumberg, D. and R. E Luck. 1990. Differences in the uals that we reared were females. Although rates of superparasitism between two strains of female-biased sex ratios are known in this ComperieUa bifasciata (Howard) (Hymenoptera: Encyrtidae) parasitizing California Red Scale (Ho- species (Smith and Goyer 1985, Ehler moptera: Diaspididae): An adaptation to circum- 1995), a complete lack of males has not vent encapsulation? Annals of the Entomological been reported. An all-female sex ratio in Society of America 83: 591-597. our samples could be explained in at least Darling, D. C. and N. F. Johnson. 1984. Synopsis of two ways. First, the populations could be Nearctic Azotinae (Hymenoptera: Aphelinidae). Proceedings of the Entomological