Classical biological control program for the mealybug Oracella acuta in Guangdong Province,China

Abstract The mealybug Oracella acuta, native to the southeastern US, was accidentally introduced into slash pine plantations in Guangdong Province in China in 1988. A classical biological control program was initiated in 1995, and the parasitoids Allotropa oracellae, Acerophaus coccois, and Zarhopalus debarri were imported from the US. A total of 19 972 parasitized mealybugs were shipped to China from 1996–2004, from which 15 430 wasps emerged, 12 933 of which were the three target species. Efforts to establish a mass-rearing program for the parasitoids in China failed. Five field release sites were established, and 6 020 parasitoids were released. Only 118 individuals of the three imported species were collected during establishment checks, although several wasps were collected 1–2 years after the last parasitoid release. Over 2 000 Anagyrus dactylopii, a cosmopolitan parasitoid, emerged from the parasitized mealybugs collected, a majority from the Taishan area near the site of the original introduction of O. acuta. To date the imported parasitoids have failed to establish, and natural enemies have not noticeably reduced mealybug populations.     

Egg production in response to combined alternative foods by the predator Coccinella transversalis

The peformance of the parasitoid Anagyrus kamali Moursi [Hymenoptera: Encyrtidae], as a function of host density, temperature, and photoperiod was investigated with the objective to optimize a mass-rearing system in the context of a biological control program. The number of hosts parasitized at densities varying from 2–100 hibiscus mealybug (HMB), Maconellicoccus hirsutus Green [Homoptera: Pseudococcidae], corresponded to a type II-III functional response in fixed-time conditions and a type III in variable-time conditions. Twenty-six percent of the oviposited eggs led to progeny emergence with a sex ratio of 0.49±0.102 (M/F), regardless of host density. Fecundity and oviposition period under six abiotic combinations (i.e., two temperatures (26±2 °C and 32±2 °C) and three photoperiods (L0:D24, L12:D12, L24:D0)) were measured. Lifetime fecundity and reproductive life were significantly affected by temperature and photoperiod conditions. Optimum female parasitoid lifetime fecundity was attained at 26±2 °C, L0:D24 with an average of 116.1±17.43 eggs. At 32±2 °C, L24:D0 and L12:D12, an average of 79.4±34.57 and 85.8±35.81 eggs were laid, respectively. Reproductive longevity was maximal at 26±2 °C, L0:D24 with 12±4.85 days of oviposition. Because the parasite A. kamali can be reared optimally without light, this may save tremendous energy costs.     

Importation,colonization and establishment ofAnagyrus indicus [Hym.: Encyrtidae] onNipaecoccus viridis [Hom.: Pseudococcidae] in Jordan

Anagyrus indicus Shafeeet al. was collected on the island of Guam and released in the Jordan River Valley of Jordan in order to regulateNipaecoccus viridis (Newstead) on citrus.A. indicus was originally released in February 1984 and became colonized by April of the same year. It also dispersed by natural means up to 61 km following the original release and colonized that same year on infestedZizyphus sp. By spring of 1985 it became the dominant parasitoid attackingN. viridis. Another parasitoid,Anagyrus kamali Moursi, was collected in Jordan in June of 1985 for the first time. This latter parasitoid apparently moved into the Jordan River Valley by means of natural dispersal from a neighboring country. Infestations ofN. viridis have been greatly reduced in areas whereA. indicus became established. This paper reports the results of research only. Mention of a proprietary product does not constitute an endorsement for its use by USDA.     

Field and laboratory studies on the fungus Aspergillus parasiticus, a pathogen of the pink sugar cane mealybug Saccharicoccus sacchari

Infestation of sugar cane nodes by the mealybug Saccharicoccus sacchari (Cockerell) was studied in two commercial fields over a 7-month period in 1987. Natural enemies associated with S. sacchari were fungi Aspergillus parasiticus Speare, Metarhizium anisopliae (Metschnikoff) Sorokin, and Penicillium spp.; the dipteran Cacoxenus perspicax Knab; and the hymenopteran parasitoid Anagyrus saccharicola Timberlake. A. parasiticus was the predominent natural enemy of S. sacchari whereas all other natural enemies showed a low level of activity. The highest prevalence of A. parasiticus was in March when it occurred on 84% of S. sacchari-infested nodes. The prevalence of A. parasiticus declined rapidly during April and May and was absent in the winter months during which nodal infestation of S. sacchari increased. In laboratory bioassays all fungal isolates originating from S. sacchari were more virulent at 28°C than at 24°C. Laboratory studies supported the hypothesis based on field observations that temperature highly influenced the efficacy of A. parasiticus against S. sacchari.     

A new approach for mealybug management: recruiting an indigenous,but ‘non‐natural’ enemy for biological control using an attractant

We previously discovered that (2,4,4‐trimethyl‐2‐cyclohexenyl)‐methyl butyrate (cyclolavandulyl butyrate, CLB) is an attractant for the mealybug‐parasitic wasp Anagyrus sawadai Ishii (Hymenoptera: Encyrtidae: Anagyrini). This wasp is not likely to parasitize the Japanese mealybug, Planococcus kraunhiae (Kuwana) (Hemiptera: Pseudococcidae), under natural conditions. In this study, we showed that this ‘non‐natural’ enemy wasp can parasitize P. kraunhiae in the presence of CLB in field experiments. Laboratory‐reared mealybugs placed on persimmon trees with CLB‐impregnated rubber septa were parasitized significantly more often by endoparasitic wasps than those on non‐treatment trees (18.1–40.3 vs. 0–6.3%). Anagyrus sawadai accounted for 20% of the wasps that emerged from mealybugs placed on CLB‐treated trees. Moreover, CLB attracted another minor parasitoid, Leptomastix dactylopii Howard (Hymenoptera: Encyrtidae: Anagyrini), which also parasitized more P. kraunhiae in the presence of CLB. All wasps that emerged from the mealybugs on control trees were Anagyrus fujikona Tachikawa, a major parasitoid of P. kraunhiae around the test location. These results demonstrated that CLB can recruit an indigenous, but ‘non‐natural’ enemy that does not typically attack P. kraunhiae under natural conditions, as well as a minor natural enemy, for biological control of this mealybug species.     

Mutual Interference Among Female Anagyrus kamali Moursi (Hymenoptera: Encyrtidae) and its Impact on Fecundity, Progeny Production and Sex Ratio

The solitary endoparasitoid Anagyrus kamali Moursi was introduced to the Caribbean to control populations of Hibiscus Mealybug (HMB) Maconellicoccus hirsutus Green. As part of a biological control programme, mass rearing of A. kamali should produce a maximum of good quality female wasps, because only female parasitoids attack the mealybug. In laboratory experiments conducted at 27 +/- 2°C, mutual interference between female parasitoids on the total oviposition, progeny production and sex ratio was assessed at five parasitoid densities: i.e. 1, 2, 5, 10 and 20 female wasps per 50 mealybugs. Oviposition rates of females decreased with increasing female density, without significantly affecting the sex ratio (average across densities of 0.49 +/- 0.322) (male/female). Under mass-rearing conditions, an increase of the female density from 25 to 75 individuals per cage resulted in an increase of the progeny production from 266 +/- 70.1 to 877.5 +/- 393.3 parasitoids. From 75 to 100 females released per cages, the progeny production was not significantly different with 877.5 +/- 393.3 and 965.3 +/- 608.3 parasitoids produced, respectively. Regardless of the female density, progeny sex ratio remained stable at an average of 0.45 +/- 0.095. As a result, the best efficiency of the mass-production system was obtained at a density of 75 females per cage. However, parasitoid production at this density was inferior to singly caged females by about 50%.     

Competition between Gyranusoidea tebygi and Anagyrus mangicola, parasitoids of the mango mealybug, Rastrococcus invadens: interspecific host discrimination and larval competition

The competition between Gyranusoidea tebygi Noyes and Anagyrus mangicola Noyes (both Hymenoptera: Encyrtidae), exotic parasitoids of the mango mealybug, Rastrococcus invadens Williams (Homoptera: Pseudococcidae) was studied in the laboratory. No significant differences were found in the way each parasitoid species examined, attacked, stung, and oviposited into hosts, unparasitized, or previously parasitized by the other species. This suggests that neither species discriminates against each other. The total number of parasitoids of either species emerging did not significantly differ between competition experiments. When A. mangicola was the first parasitoid to attack a host, it had no significant advantage over G. tebygi. However, when A. mangicola followed G. tebygi by either 4 or 24 h, it clearly won. Overall A. mangicola won the competition in 70.9% of all cases. The level of the competition, either at the egg or larval stage, and factors responsible for the elimination of older larvae by younger ones could not be assessed in these experiments. The coexistence of the two parasitoids as complementary for the biological control of the mango mealybug is discussed.     

The effects of parasitism by an encyrtid parasitoid, Anagyrus pseudococci on the survival, reproduction and physiological changes of the mealybug, Planococcus citri

Survival, reproduction and some biochemical changes in the citrus mealybug, Planococcus citri (Risso) parasitized by the endoparasitoid, Anagyrus pseudococci (Girault) are reported. The parasitized younger mealybugs were more likely to die than be successfully parasitized. The mean duration (±SE) required for mortality other than mummification were 1.85 ± 0.06, 2.48 ± 0.14 and 2.89 ± 0.17 days for first, second and third instar P. citri respectively. Hosts parasitized in the first instar did not produce any mummies while the second and third instar nymphs and adult stages of the mealybugs were mummified on average 8 to 11 days after attack. Parasitization caused cessation of normal fecundity as well as induction of early egg maturation of the mealybugs. The mealybugs parasitized in the adult stage produced a few eggs but the fecundity of unparasitized mealybugs was about 40 fold higher than that of parasitized mature adults. Parasitized pre-ovipositing and mature adults laid eggs within 24 h of attack. SDS-PAGE analysis of the body content of the parasitized mealybugs after 24 h and 48 h of parasitization and before egg hatch revealed an increase in the concentration of some proteins. Response to wound reactions was not visible either as formation of extra protein bands or increased density of the existing bands. The possible effect of parasitism on the changes of the reproductive physiology of the host is discussed.     

Confirmation of the existence of alloparasitoids in nature – host relationships of an Australian Coccophagus species that parasitizes mealy bugs

Heteronomous hyperparasitoids are parasitic wasps with sex‐related host relationships that are unique to a group of genera in the chalcidoid family Aphelinidae. Females are primary parasitoids of various sedentary bugs (mainly, scale insects, mealy bugs, and whiteflies). Males, in contrast, are hyperparasitic, and they frequently develop at the expense of female conspecifics. Alloparasitoids constitute a special category of heteronomous hyperparasitoids, for their males never develop through female conspecifics. The existence of alloparasitic host relationships and the utility of the category ‘alloparasitoid’ have both been questioned. Here, we present results that confirm the existence of the alloparasitic way of life among heteronomous aphelinids. We investigated an undescribed species of Coccophagus (Hymenoptera: Aphelinidae), an Australian parasitoid that attacks the introduced lantana mealy bug, Phenacoccus parvus Morrison (Homoptera: Pseudococcidae), in Queensland. A year‐long field survey regularly returned large numbers of female Coccophagus spec. near gurneyi individuals from P. parvus (total n = 4212), but only few males (n = 11). Males emerged from samples only when the encyrtid parasitoid Anagyrus diversicornis (Howard) (Hymenoptera: Encyrtidae) was present in samples in relatively high numbers. Laboratory oviposition tests confirmed that A. diversicornis is a male host and showed that males do not develop at the expense of conspecific females. Other studies show that males are attracted in numbers to virgin females held in cages above mealy bug‐infested Lantana montevidensis (Spreng.) Briq. (Verbenaceae) in the field, demonstrating that they are common in the population as a whole. This confirms that the males need hosts other than conspecific females and that their usual hosts are present outside of the lantana/P. parvus system. The implications of these results for developing a realistic classification of heteronomous host relationships are discussed.     

Asymmetrical intraguild predation between natural enemies of the citrus mealybug

The ability of a predator to discriminate against parasitized prey determines the extent of asymmetrical intraguild predation, which is often crucial for the outcome of biological control. Anagyrus nr. pseudococci (Girault) (Hymenoptera: Encyrtidae), a parasitoid of the citrus mealybug, Planococcus citri (Risso) (Hemiptera: Pseudococcidae), suffers from intraguild predation by coccinellids occurring in the same habitat. The level of intraguild predation on A. nr. pseudococci by Nephus includens (Kirsch) (Coleoptera: Coccinellidae) at different immature stages has been investigated with and without simultaneous offer of extraguild prey. Larvae of A. nr. pseudococci appeared to face increased intraguild predation at early developmental stages, whereas mummification provided adequate protection against the predatory coccinellid. Different predation levels on unparasitized vs. parasitized hosts at various developmental stages in choice assays indicated that N. includens preferences might be determined not solely by palatability of the prey but also by its ability to protect itself.