Biological control of citrus mealybug,Planococcus citri with an introduced parasite,Leptomastix dactylopii in India

Planococcus citri (Risso) is one of the major pests of citrus orchards in India. For the control ofP. citri, an encyrtid parasite,Leptomastix dactylopii How. was introduced from West Indies in 1983. The parasite was mass bred and inoculative releases were made in 2 selected citrus orchards where infestation of mealybug on fruits (sweet orange, seedless lime and acid lime) ranged from 38 to 65 per cent. Establishment of the parasite in the 2 release orchards resulted in complete control of the mealybug within 3 to 4 months. No insecticidal sprays were required subsequently for the control ofP. citri in the following seasons. Contribution No. 152/85 of the IIHR, Bangalore — 560089.     

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.     

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.     

Impacts of Argentine ants on mealybugs and their natural enemies in California's coastal vineyards

Abstract 1. The Argentine ant, Linepithema humile, tends honeydew‐excreting homopterans and can disrupt the activity of their natural enemies. This mutualism is often cited for increases in homopteran densities; however, the ant’s impact on natural enemies may be only one of several effects of ant tending that alters insect densities. To test for the variable impacts of ants, mealybug and natural enemy densities were monitored on ant‐tended and ant‐excluded vines in two California vineyard regions. 2. Ant tending increased densities of the obscure mealybug, Pseudococcus viburni, and lowered densities of its encyrtid parasitoids Pseudaphycus flavidulus and Leptomastix epona. Differences in parasitoid recovery rates suggest that P. flavidulus was better able to forage on ant‐tended vines than L. epona. 3. Densities of a coccinellid predator, Cryptolaemus montrouzieri, were higher on ant‐tended vines, where there were more mealybugs. Together with behavioural observations, the results showed that this predator can forage in patches of ant‐tended mealybugs, and that it effectively mimics mealybugs to avoid disturbance by ants. 4. Ant tending increased densities of the grape mealybug, Pseudococcus maritimus, by increasing the number of surviving first‐instar mealybugs. Parasitoids were nearly absent from the vineyard infested with P. maritimus. Therefore, ants improved either mealybug habitat or fitness. 5. There was no difference in mealybug distribution or seasonal development patterns on ant‐tended and ant‐excluded vines, indicating that ants did not move mealybugs to better feeding locations or create a spatial refuge from natural enemies. 6. Results showed that while Argentine ants were clearly associated with increased mealybug densities, it is not a simple matter of disrupting natural enemies. Instead, ant tending includes benefits independent of the effect on natural enemies. Moreover, the effects on different natural enemy species varied, as some species thrive in the presence of ants.     

Recovery of the indigenous Coccidoxenoides peregrinus and the exotic Leptomastix dactylopii on Planococcus citri in lemon and acid lime orchards

The citrus mealybug Planococcus citri was found in large numbers on lemon and acid lime in 1991 around Bangalore. It was attacked by two encyrtid parasitoids, the exotic Leptomastix dactylopii and the indigenous Coccidoxenoides peregrinus. L. dactylopii was recovered 7 years after a release in 1984 around Bangalore. However C. peregrinus was more abundant, and was responsible for the decline of P. citri both on lemon and acid lime. No other primary or hyper‐parasitoid or predator of P. citri was recorded in these citrus orchards during the study.     

Oviposition behaviour, influence of experience on host size selection, and niche overlap of the solitary Leptomastix epona and the gregarious Pseudaphycus flavidulus, two endoparasitoids of the mealybug Pseudococcus viburni

Oviposition behaviour and host size selection of the solitary parasitoid Leptomastix epona(Walker) and the gregarious Pseudaphycus flavidulus(Brèthes) [both Hymenoptera: Encyrtidae] were examined on five size classes of the mealybug Pseudococcus viburni(Signoret) [Hemiptera: Pseudococcidae]. The host size classes mostly consisted of one stage (first, second, third instar nymph, young adult and preovipositing adult) and were presented together to wasps of either parasitoid species. Both parasitoid species locate the host by drumming the surface of the patch with the antennae. Leptomastix eponaseems to use mainly the antennae to examine the host but P. flavidulusmay accept or reject a host for oviposition after antennation or insertion of the ovipositor. Leptomastix eponaattempts oviposition in all the host stages from second instar nymphs but P. flavidulusincludes first instar. Both parasitoid species select mainly larger hosts (>1 mm, third instar nymphs) to oviposit but P. flavidulusis able to parasitize more second instar nymphs compared to L. epona. Female wasps of L. eponamay host feed on small mealybugs (second and third instar nymphs) that they do not use for oviposition. Oviposition experience of either parasitoid species for 24 hours does not influence host size selection on patches with hosts of similar mixed sizes. Oviposition decisions are independent of the host sizes of the preceding ovipositions. Implications about stability of a single parasitoid – host system and the success of biological control of the mealybug were discussed in respect of the developmental refugia of the two parasitoid species. Niche overlap of the two parasitoid species was discussed with a view to giving an insight into a single or multiple introduction.     

Interactions between the ant Tapinoma nigerrimum (Hymenoptera: Formicidae) and the main natural enemies of the vine and citrus mealybugs (Hemiptera: Pseudococcidae)

Honeydew-excreting hemipterans, such as mealybug pests, can be protected from their natural enemies by tending ants in return for honeydew, thereby compromising the aims of biological control. In this respect, antagonistic interactions between the ant Tapinoma nigerrimum, native to the Mediterranean basin, and the main natural enemies of both the vine mealybug (VMB), Planococcus ficus, and the citrus mealybug (CM), Planococcus citri, were assessed in laboratory conditions. Parasitism of vine and CMs by their respective parasitoids, Anagyrus sp. nr. pseudococci and Leptomastix dactylopii, was negatively affected by the ant T. nigerrimum. Similarly, T. nigerrimum was shown to significantly disrupt the predatory potential of ladybird larvae, Cryptolaemus montrouzieri, when foraging on host CMs. By contrast, the presence of the ant did not negatively influence the predatory activity of C. montrouzieri adults when feeding on CMs. Consequently, the encyrtid parasitoids A. sp. nr. pseudococci and L. dactylopii and the larval stage of the predator C. montrouzieri may be considered as T. nigerrimum-sensitive, whereas the adults of C. montrouzieri may be regarded as T. nigerrimum-resistant predators. Accordingly, the ant T. nigerrimum constitutes a threat to the biological control of mealybugs by either the encyrtids A. sp. nr. pseudococci and L. dactylopii or the larval stage of the ladybird C. montrouzieri. Hence, adequate control of T. nigerrimum is highly recommended before any release of these mealybugs' natural enemies.     

Predicting development of the mealybug parasitoids Anagyrus pseudococci, Leptomastix dactylopii and Leptomastidae abnormis under glasshouse conditions

Developmental rates of three encyrtid mealybug parasitoids were examined under constant, cycling and glasshouse temperatures. Under constant conditions the rate of development increased with rising temperature up to 35°C, but a constant 40°C was lethal. Under cycling conditions, 12 h periods at 40°C could be tolerated. Developmental rates under cycling conditions could be calculated from constant temperature data, by incrementing development on an h/h basis. A new technique was developed to determine the lower thresholds for development, using cycling regimes and to calculate the rates of development over short periods at high temperature. A previously untested polynomial regression technique was used to predict mean developmental periods under glasshouse conditions. These predictions were considerably more accurate than day-degree (D^o) predictions when substantial periods at extreme temperatures were involved, but not significantly different from day-degree predictions under hot-house conditions. In addition a method was developed to calculate a 95% range for emergence, which gave consistently good estimates of first and last eclosion observed under fluctuating conditions.

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Résumé Les vitesses de développement de 3 parasitoïdes de cochenilles ont été étudiées dans les conditions de température de serre, avec thermopériode ou en température constante. En conditions constantes, la vitesse augmente jusqu'à 35°C, mais est létale à 40°C. Avec thermopériode, une thermophase de 40°C peut être tolérée pendant 12 heures. Les vitesses de développement sous thermopériodes pourraient être calculées à partir des données obtenues en conditions constantes, modifiées en fonction des durées respectives des cryophases et thermophases. Une méthode originale est présentée pour obtenir les seuils inférieurs de développement, en utilisant des thermopériodes, et pour calculer les vitesses de développement à températures élevées.Une méthode de régression polynomiale, non vérifiée préalablement, a été utilisée pour prévoir les durées moyennes des développements sous serre. Ces estimations sont beaucoup plus sûres que les prédictions basées sur le concept de degré-jour (D^o), lorsque les températures extrêmes durent longtemps, mais en serre chaude elles ne présentent aucune différence significative. De plus, une méthode d'évaluation des 95% d'émergences, a donné de bonnes estimations des premières et dermières émergences en conditions périodiques.

     

Progeny production and adult longevity of the mealybug parasitoidsAnagyrus pseudococci,Leptomastix dactylopii,andLeptomastidea abnormis [Hym.: Encyrtidae] in relation to temperature

Progeny production increased and adult longevity decreased with rising temperature within the range 18°C to 30°C for the 3 mealybug parasitoidsAnagyrus pseudococci (Girault),Leptomastix dactylopii Howard andLeptomastidea abnormis (Girault). The Weibull distribution gave a good fit to survival curves for the 3 parasitoids and statistical comparison of Weibullb andc parameters at different temperatures allowed changes in the scale and shape of the curves to be detected. In general, ♀♀ lived longer than ♂♂ for all 3 species, except at high temperature. FemaleL. abnormis attained their maximum progeny production at 24°C and maintained this level up to 34°C. They lived longer than the other 2 parasitoid species at 30°C and showed a type I survival curve throuhout the range of temperatures examined.A. pseudococci andL. dactylopii both required high temperatures (30°C) to attain their maximal progeny production, but werepseudococci tended towards type II, with a larger proportion of the population dying within the first few days.L. dactylopii lived longest at 26°C, with ♀♀ showing a type I survival curve at all temperatures and ♂ survival curves changing from type I to type II at 30°C. The implications of these findings for the population dynamics of the different parasitoids are briefly discussed.      

Host location and discrimination mediated through olfactory stimuli in two species of Encyrtidae

The role of olfactory stimuli in host detection and evaluation was studied in two encyrtid Hymenoptera. The first, Epidinocarsis lopezi De Santis, is a monophagous parasitoid of the cassava mealybug Phenacoccus manihoti Matile-Ferrero, itself feeding exclusively on cassava, Manihot esculenta Crantz. The second, Leptomastix dactylopii Howard, is a monophagous parasitoid of the Citrus mealybug, Planococcus citri Risso, but this latter is highly polyphagous. The behaviour of females of both parasitoids (attaction and locomotion) was compared in a tubular olfactometer for the odours of their respective hosts on cassava and poinsettia. Tests were made using: 1) healthy host-plant alone; 2) host-plant infested with unparasitized mealybugs; 3) unparasitized mealybugs only; 4) host-plant infested with parasitized mealybugs and 5) parasitized mealybugs only. Only E. lopezi was attracted by the odour of the host-plant alone, but both species were attracted by the odour of an infested host-plant and that of unparasitized mealybugs. The odour of parasitized mealybugs, alone or on host-plant, induced an undirected activity. The attraction of E. lopezi to the odour of the host-plant alone could be linked to the monophagous diet of its host, whereas the attraction of the two species of parasitoids to the odours of infested host-plants and unparasitized mealybugs could be due to the fact that both parasitoids are specialists. The behavioural response of both species to the odour of parasitized mealybugs revealed a new aspect in host discrimination: the identification of parasitized hosts could be partly mediated through olfactory stimuli, and not only through gustatory stimuli.