High host specificity in Encarsia diaspidicola (Hymenoptera: Aphelinidae), a biological control candidate against the white peach scale in Hawaii

Abstract

Pre-introductory host specificity tests were performed with Encarsia diaspidicola, a biological control candidate against the invasive white peach scale, Pseudaulacaspis pentagona. False oleander scale, P. cockerelli, coconut scale, Aspidiotus destructor, cycad scale, Aulacaspis yasumatsui, greenhouse whitefly, Trialeurodes vaporariorum, green scale, Coccus viridis, and long-tailed mealybug, Pseudococcus longispinus were tested in quarantine using traditional no-choice tests and examined for wasp emergence. The Hawaiian endemic palm scale, Colobopyga pritchardiae was also tested using no-choice tests and evaluated using species-specific molecular markers. All tests used unexposed non-target cohorts and no-choice exposure of white peach scale to the parasitoid as controls. None of the non-target exotic species yielded wasp emergence, and exposure to wasps had no effect on the mortality of the non-target species examined. Molecular tests with the endemic palm scale showed no evidence of parasitism by E. diaspidicola. These results strongly support that E. diaspidicola has a narrow host range and that its release in Hawaii will have negligible risk of non-target effects.

Introduction

White peach scale, Pseudaulacaspis pentagona Targioni-Tozzetti (Hemiptera: Diaspididae), is one of the most polyphagous armored scale insects in the world (Miller and Davidson, 2005), but so far in Hawaii it is only known as a crop pest in papaya, Carica papaya L. Infestation can rapidly increase to levels where large areas of the trunks of papaya trees are completely covered by white peach scales. Overcrowding causes scales to spread up the trunk, and in heavily infested trees scales move up onto fruit, preferring to settle in the calyx and peduncle regions. White peach scale on the fruit is a quarantine problem. Infested fruit shipments may be rejected in California, and Japan, a very important market for Hawaii papayas, has zero tolerance for white peach scale. Infested fruits may be brushed to physically remove scales at considerable cost. In papayas grown for the Japan market, fields may be abandoned after 5% of the trees are infested. White peach scale can also decrease plant vigor and yield. Control with available chemical insecticides is not effective (Follett, 2000). The advancing infestation, which is at outbreak levels in some areas of the Big Island (Island of Hawaii), where the largest Hawaii papaya orchards are located, and the inefficiency of chemical control necessitated the development of a biological control program.

Female white peach scales deposit all their eggs (≈100–150 total/female) in about a week. Eggs hatch in 3–4 days and the young scales (“crawlers”) settle on the host plants within 2 days after hatching. Crawlers do not actively disperse far from the point of hatching but can be spread by the wind. Once crawlers settle they remain attached to the host plant throughout their lives. Two subsequent molts requiring about three weeks time produces adult females. Females form a slightly oval waxy cover (scale) during development. Second instar males form an oblong cover and after three molts emerge as adults 19–22 days later. Adult males are winged and immediately start inseminating females. Oviposition by females begins 14–16 days after mating. A generation is completed in 36–40 days at 25 °C (Miller and Davidson, 2005).

Encarsia diaspidicola Silvestri (Hymenoptera: Aphelinidae) is a thelytokous solitary endoparasite. The adult females deposit eggs singly in immature stages of white peach scale. The development time of the parasitoid at approximately 23 °C is 30–35 days. In the scientific literature, E. diaspidicola is reported from white peach scale (Huang and Polaszek, 1998) and Quadraspidiotus pernicious Comstock, San Jose scale (Peck, 1963). The Universal Chalcidoidea Database (Noyes, 2003) lists other primary hosts but those records may have been based on misidentifications. Later workers (Heraty et al., 2007) only list white peach scale and San Jose scale as primary hosts with a single reference to San Jose scale (Peck, 1963). As there have been no reports since 1963 of E. diaspidicola attacking San Jose scale, the Peck record may be questionable.

Several biological control programs have targeted white peach scale worldwide (Collins and Whitcomb, 1975, Waterhouse and Norris, 1987, Liebregts et al., 1989). Encarsia berlesei Howard (Hymenoptera: Aphelinidae) and E. diaspidicola were released in Samoa as biological control agents to control white peach scale on passion fruit, Passiflora edulis L. Over time, E. diaspidicola displaced E. berlesei in Samoa and lowered white peach scale population numbers significantly (Liebregts et al., 1989). Because of its successful establishment and control of white peach scale populations in Samoa, which has a similar climate to Hawaii, E. diaspidicola was selected as the preferred biological agent and was imported into Hawaii from Samoa in 2006. A colony was established at the USDA Forestry Service Quarantine Facility in Hawaii Volcanoes National Park.

Parasitoid wasps in the genus Encarsia Foerster mostly attack whiteflies (Aleyrodidae) and armored scale insects (Diaspididae) (Huang and Polaszek, 1998), with four species recorded from aphids in the family Hormaphididae (Evans et al., 1995). Females of most Encarsia species develop as primary internal parasitoids of diaspidid armored scales or whiteflies, but the males of the same species develop as parasitoids of female parasitoid larvae or pupae, often of their own species (Viggiani, 1984, Hunter and Woolley, 2001). In the case of E. porteri, females develop as primary parasitoids of whiteflies and males are obligate parasitoids of lepidopteran eggs (Hunter et al., 1996).

The Hawaiian insect fauna has a high rate of endemism, and biological control programs must show a high degree of host specificity for candidate agents and minimal risk to non-target native species before permission to release will be granted. E. diapidicola is known to attack only diaspidid scales and there are no native diaspidid scale insects in Hawaii, making it a promising candidate. Nevertheless, host specificity testing was required by state and federal regulatory agencies to demonstrate minimal risk of non-target effects. The native Hawaiian insect fauna includes three species of scale insects in the family Halimococcidae or pupillarial palm scales; these halimococcids were at one time classified as diaspidid scales (Beardsley, 1963). One of the species, Colobopyga pritchardiae, an endemic palm scale found only on Pritchardia palms and recently recorded for the first time on the island of Hawaii (Neumann et al., 2007), was included in host testing as a representative of the Hawaiian Halimococcidae. Encarsia diaspidicola was also tested for its ability to parasitize several invasive, economically important diaspidid scales and close relatives: the false oleander scale, P. cockerelli Cooley (Diaspididae), the coconut scale, Aspidiotus destructor Signoret (Diaspididae), the cycad scale, Aulacaspis yasumatsui Takagi (Diaspididae), the greenhouse whitefly, Trialeurodes vaporariorum Westwood (Aleyrodidae), the green scale, Coccus viridis Green (Coccidae), and the long-tailed mealybug, Pseudococcus longispinus Targioni-Tozzetti (Pseudococcidae).