Experimental evaluation of the efficiency of Epidinocarsis lopezi, a parasitoid introduced into Africa against the cassava mealybug Phenacoccus manihoti

The capability of Epidinocarsis lopezi (De Santis) (Hymenoptera: Encyrtidae) to control the cassava mealybug (CM) Phenacoccus manihoti Mat.-Ferr. (Homoptera: Pseudococcidae) was investigated in Nigeria using physical and chemical exclusion experiments. In two sleeve cage experiments CM populations, about 2 months after artificial infestation, were 7.0 and 2.3 x lower on artificially infested cassava tips covered with open cages than on tips in closed cages which excluded most parasitoids. On similarly infested but uncovered tips, CM populations were 24.3 and 37.5 x lower, and parasitisation rates were higher. In an artificially infested field which was treated weekly with carbaryl, parasitisation rates were below 10% and CM populations exceeded 200 per tip. In the chemically untreated plot, parasitisation rates were up to 25% and CM densities were mostly below 10 per tip. This study demonstrates the efficiency of E. lopezi in controlling its host under the experimental conditions.

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Résumé La capacité d'E. lopezi de contrôler la cochenille farineuse du manioc a été évaluée au Nigéria en excluant le parasitoïde de son hôte par des moyens physiques et chimiques. Dans deux expériences utilisants des manchons les populations de la cochenille deux mois après l'infestation artificielle étaient 7.0 et 2.3 fois plus basses sur les branches couvertes d'un manchon ouvert que sur les branches couvertes par un manchon fermé, qui excluait la plupart des parasitoïdes. Sur les apex sans manchons, également infestés artificiellement, les populations de la cochenille étaient 24.3 et 37.5 fois plus bas tandis que le degré de parasitisme était plus élevé. Dans un champ infesté artificiellement et partiellement traité chaque semaine avec du carbaryl, le pourcentage de parasitisme restait au-dessous de 10%, et les populations de la cochenille dépassaient 200 par apex. Dans la partie non-traitée, le parasitisme atteignait 25% et la densité de la cochenille restait pour la plupart du temps au-dessous de 10 cochenilles par apex. Ces expériences démontrent la capacité d'E. lopezi de maintenir son hôte à un bas niveau dans des conditions expérimentales.

     

Interspecific interference between Apoanagyrus lopezi and A. diversicornis, parasitoids of the cassava mealybug Phenacoccus manihoti

The parasitoids Apoanagyrus lopezi De Santis and A. diversicornis (Howard) (Hymenoptera: Encyrtidae) have been introduced into Africa for the biological control of the cassava mealybug Phenacoccus manihoti Matile-Ferrero (Homoptera: Pseudococcidae). We have studied competition between these species to investigate if they can coexist. Here we report on the influence of the simultaneous presence of non-conspecific adult females on searching efficiency on patches. Wasps of either species foraged on discs of cassava leaf with mealybugs, while at the same time different numbers of non-conspecifics were also depleting the patch. Patch area per parasitoid and number of hosts available to each parasitoid were equal in all treatments.In both species, the presence of other foragers clearly affected several aspects of the parasitoids' behaviour. Patch residence time increased with the number of non-conspecifics in A. diversicornis. In both parasitoid species, the proportion of hosts left unparasitized after the patch visit decreased with increasing numbers of females on the patch. The proportions of super- and multiparasitism did not change with the number of females. Both species produced more offspring during a patch visit in the presence of more non-conspecifics. These behavioural changes did not, however, lead to a change in the offspring production rate on patches. A. diversicornis produced offspring at a rate three times that of A. lopezi when one A. lopezi and one A. diversicornis foraged simultaneously. This is the first report of an aspect of interspecific competition where A. diversicornis has an advantage over A. lopezi. Interference between adult females thus promotes coexistence of the two species on P. manihoti.     

Biological control of the cassava mealybug Phenacoccus manihoti (Hom., Pseudococcidae) by Epidinocarsis lopezi (Hym., Encyrtidae) in Malawi

From 1985 to 1989 five large scale surveys were made to document the spread of the cassava mealybug (CM) Phenacoccus manihoti Matile‐Ferrero (Hom., Pseudococcidae) and the releases and successful establishment of its exotic parasitoid Epidinocarsis lopezi (De Santis) (Hym., Encyrtidae) through most cassava‐growing areas of Malawi. In a multiple regression analysis involving 29 meteorological, agronomic and plant variables from 476 fields, the duration of E. lopezi's presence was the major factor influencing CM population densities. In the first year the CM was recorded in a particular place, 25% of all tips had more than 100 CM. Wherever E. lopezi had been present for two years or more, CM populations were reduced on average seven times and tips infested with more than 100 CM became rare (1%). In parallel, damage on cassava tips stabilized at a low level. Similarly, along Lake Malawi, 84.9% of all tips had more than 10 CM in 1986; this value stabilized at 3.3%‐4.0% in 1988–1989. Indigenous coccinellids were often abundant in the first year of the CM infestation, but their populations collapsed later, while the frequency of fields with E. lopezi increased. In 1987, farmers abandoned 28.4% of all fields where E. lopezi was just introduced as compared with 2.7% where the parasitoid had been present for two years or more. Overall, satisfactory control was achieved by E. lopezi in all but a few fields concentrated on extremely poor soils characterized by sand dune vegetation. The socioeconomic implications of this ongoing and apparently successful biological control program are discussed.     

Temperature-dependent growth rates for the cassava mealybug, Phenacoccus herreni, and two of its encyrtid parasitoids, Epidinocarsis diversicornis and Acerophagus coccois in Colombia

Developmental rates for Phenacoccus herreni Cox & Williams were determined at 18°, 20°, 22°, 25°, 30° and 35°C for the egg, all juvenile male and all juvenile female stadia. Longevity was determined for adult females and adult males. Developmental rates for the P. herreni parasitoid Epidinocarsis diversicornis (Howard) were determined at 18°, 20°, 25° and 30°C for the oviposition-to-mummy-formation period and the mummy-formation-to-adult-eclosion period. Developmental rates were determined for the P. herreni parasitoid Acerophagus coccois Smith for the same two life stages at 20°, 25° and 30°C. Least-squares-derived polynomial equations or logistic equations were fitted to each data set (except for A. coccois) so that rates could be interpolated for temperatures between observed points for use in an analysis of the impact of these parasitoids on population dynamics of P. herreni. Results of this analysis are presented separately.

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Résumé Les vitesses de développement des oeufs et de tous les stades larvaires mâles et femelles de P. herreni Cox & Williams ont été déterminées à 18°, 20°, 22°, 25°, 30° et 35°C. La longévité des adultes mâles et femelles a été déterminée. Les vitesses de développement de la ponte à la formation du cocon et de celleci à l'émergence de E. diversicornis Howard, encyrtide parasite de P. herreni ont été déterminées à 18°, 20°, 25° et 30°C. Il en a été de même pour un second encyrtide parasite A. coccois Smith à 20°, 25° et 30°C. Les équations polynomiales des derniers carrés dérivés et les équations logistiques ont été ajustées pour chaque lot de données (à l'exception de A. coccois) de façon à ce qu'elles aient pu être interpolées pour analyser l'impact de ces parasites sur la dynamique de population de P. herreni. Les résultats de cette analyse sont présentés à part.

     

Sustained biological control of the cassava mealybugPhenacoccus manihoti [Hom.: Pseudococcidae] byEpidinocarsis lopezi [Hym.: Encyrtidae] in Nigeria

Following the successful introduction ofEpidinocarsis lopezi (De Santis) for biological control of the cassava mealybug (CM)Phenacoccus manihoti Mat.-Ferr. in southwestern Nigeria in 1981 and 1982, 11 groups of cassava fields were sampled every 2 weeks up to 1988 for impact assessment. After 1984, CM populations remained mostly below 10 per tip despite the presence of native hyperparasitoids, demonstrating the long-term success of biological control byE. lopezi in the region. Indigenous polyphagous coccinellids were found only during peak host densities, whereas the specificE. lopezi was common throughout the year. During some periods, percentage parasitism indicated delayed density dependence. Since 89% of all sampled cassava tips had no CM at all and the parasitisme is very mobile, parasitization rates were also calculated for individual infested tips (N=4,878). Parasitism increased slightly with host density on tips having between 1 and 10 CM of the 3^rd and 4^th instars, indicating positive density dependence. Such tips comprised 64% of all infested tips. At higher host densities, parasitism rates fell rapidly. The results are discussed in view of different theories on population regulation by biological control agents.      

The role of host- and host-plant odours in the attraction of a parasitoid, Epidinocarsis lopezi, to the habitat of its host, the cassava mealybug, Phenacoccus manihoti

In the field, the encyrtid wasp, Epidinocarsis lopezi (DeSantis) can find its host, the cassava mealybug (Phenacoccus manihoti Matile-Ferrero) on cassave plants when the host is scarce. As a step towards understanding the parasitoid's effectiveness we investigated the cues with which it locates its host-habitat. Using a fourarmed olfactometer, we determined the attactivity of various host-and host-plant odours to female E. lopezi which had been previously exposed to infested plants. Attractivity or preference of an odour was determined from the proportion of 50 choices made between the odour and a blank, or between two odours. Female E. lopezi were attracted by mealybug-infested cassava leaves (CML), but not by the odour of cassava mealybugs (CMB) alone or by uninfested plants (ULU). An artificial combination of CMB and ULU was also not attractive. CML was preferred over ULU and CMB + ULU. These results suggest that the attractive element arises from the cassava plant itself in response to CMB infestation. We therefore tested the attractivity of uninfested leaves from partly infested plants, and found that these were indeed attractive. E. lopezi probably uses the odour which is emitted from infested cassava plants to guide it to its host in the field.

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Zusammenfassung Epidinocarsis lopezi ist imstande, seine Wirte auf den Cassavapflanzen zu finden, auch wenn die Wirte nur in geringer Dichte vorkommen. Die Reaktion der Schlupfwespe auf Gerüche der Wirte und der Wirtspflanzen wurde untersucht. Weibchen der Schlupfwespe, die vorher mit Schmierläusen auf Cassavapflanzen zusammengebracht worden waren, wurden individuell in einem vierarmigen Olfaktometer verschiedenen Kombinationen dieser Gerüche ausgesetzt. Die relative Attraktivität jedes Geruchs wurde bestimmt anhand von 50 Entscheiden zwischen dem Geruch und einer Kontrolle oder zwischen zwei Gerüchen. E. lopezi Weibchen wurden von schmierlausinfizierten Blättern angezogen, aber nicht von Cassavaschmierläusen (CMB), oder von uninfizierten Cassavapflanzen (ULU). Die künstliche Mischung von CMN und ULU wurde auch nicht anlockend. CML war relativ mehr attraktiv als ULU und als die Mischung. Die Vermutung liegt vor dass E. lopezi von einem Pflanzenduft angezogen wird, der von mit Schmierläusen infizierten Cassavapflanzen ausgeschieden wird. Die Parasitoide wurden auch von uninfizierte Blättern teilweise infizierter Pflanzen angezogen. Wahrscheinlich wird im Freiland der Geruch infizierter Cassavapflanzen durch E. lopezi zur Auffindung weiterer wirtstragenden Cassavapflanzen gebraucht.

     

Sex ratios in field populations of Epidinocarsis lopezi, an exotic parasitoid of the cassava mealybug, in Africa

Abstract.

• 1 In cassava fields in Africa, population sex ratios of Epidinocarsis fopezi vaned from 0.44 (males to total parasitoids) at low host densities to highly male-biased ratios of 0.70 at high host densities.
• 2 This variability is caused by the difference in allocation of sons and daughters to hosts of different sizes, through the following mechanisms: (a) small, i.e. second instar, hosts are mainly used for the production of male offspring, whereas in large, i.e. third instar, hosts a variable, female-biased sex ratio is produced; (b) E.fopezi does not selectively oviposit into large hosts but always accepts both small and large hosts for oviposition upon encountering; (c) in the field, this parasitoid is time-limited, and not egg-limited. On the basis of an optimal diet model, such general host acceptance is shown to be the best strategy.
• 3 Thus, sex ratio increases with host density for three reasons: the proportion of small hosts encountered in the field increases with increasing host density, small hosts are used for male production, and hosts are always accepted when encountered.

     

Influence de l'hyperparasitisme sur les populations d'un hymenoptère encyrtidae,Epidinocarsis lopezi,parasitoide de la cochenille du manioc Phenacoccus manihoti introduit au Congo

Résumé Une étude au champ de la dynamique des populations de la cochenille du manioc Phenacoccus manihoti Matt.-Ferr. (Hom. Pseudococcidae) et des agents biologiques qui lui sont associés a été entreprise dans 4 parcelles de manioc Manihot esculenta Crantz (Euphorbiacée) situées dans 2 localités différents du Congo. Elle a essentiellement montré que les 7 à 16% de parasitisme développés par le parasitoïde exotique Epidinocarsis lopezi (De Santis) (Hym. Encyrtidae), 4 ans après son introduction, n'affectent pas significativement la dynamique des populations du ravageur. Les taux importants d'hyperparasitisme (67 à 100%) dont le parasitoïde primaire est l'objet limitent la reproduction de ses populations. Toutefois il est difficile de conclure quant à l'impact réel des hyperparasites sur l'efficacité de l'auxiliaire dans la lutte contre la cochenille.

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A field study of cassava mealybug Phenacoccus manihoti Mat.-Ferr. (Hom. Pseudococcidae) population dynamics, together with that of associated biological agents was made on 4 sample plots in cultivated manioc Manihot esculenta Crantz (Euphorbiacée) in two different areas of the Congo. It showed that four years after introduction, the 7 to 16% of parasitism attributable to the exotic parasitoid Epidinocarsis lopezi (De Santis) (Hym. Encyrtidae), did not significantly affect pest population dynamics. High levels of hyperparasitism (67% to 100%) to which the parasitoid is itself subject limits its population levels. It is, however, impossible to determine the real effect of hyperparasites on the efficiency of the auxiliary in the biological control of the mealybug.

     

The influence of constant temperature on population growth rates of the cassava mealybug, Phenacoccus manihoti

Life table studies were conducted to assess the effect of constant temperature on the rate of population growth of the cassava mealybug, Phenacoccus manihoti Matile-Ferrero. Four temperatures, between 20 and 30.5°C, were tested. An inverse relationship was observed between temperature and most demographic parameters.The intrinsic rate of natural increase (r_m) increased from 0.1 at 20°C to 0.2 at 27°C and 30.5°C. The net reproductive rate varied between 426.3 at 30.5°C and 584.7 at 20°C. The mealybug population reached 50% mortality after 37.5, 21.5, 19.0 and 19.0 days respectively at 20, 23.5, 27 and 30.5°C. The results indicate that P. manihoti can persist and increase in numbers within the range between 20 and 30.5°C.

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Influence de températures constantes sur les taux de croissance de populations de la cochenille du manioc Phenococcus manihoti

Résumé Des tables de vie ont été établies pour déterminer l'effet de températures constantes sur les taux de croissance de populations de la cochenille du manioc, Phenacoccus manihoti Mat.-Ferr., et ainsi comprendre les changements au sein des populations du ravageur dans les champs et mener à bien le programme de lutte biologique organisé à l'I.I.T.A. contre cette cochenille. P. manihoti, introduit à partir de l'Amérique latine en Afrique, y menace la production du manioc (Manihot esculenta Crantz).Le taux intrinsèque d'accroissement natural (r_m) a augmenté de 0.114 à 20°C, à 0.185 à 27°C, avant de descendre à 0.182 à 30.5°C. Le taux net de reproduction (R_o) a été relativement élevé (426–584 oeufs femelles/génération). Dans nos conditions expérimentales, la mortalité a atteint 50% au bout de 37.5, 21.5, 19.0 jours respectivement à 20, 23.5, 27 et 30.5°C. La durée du cycle et le coefficient d'accroissement () étaient inversement liés à la température. Le ravageur possède la capacité de doubler sa population en 6.08 jours à 20°C alors que 3.81 jours seulement suffisent pour doubler la population à 30.5°C.Ces résultats nous ont permis de comprendre et d'expliquer l'énorme pouvoir de pullulation de la cochenille observé dans les champs pendant la saison sèche; il s'ensuit que les lâchers des entomophages produits en élevages doivent se faire très tôt au début de la saison sèche, afin de contrecarrer la grande fertilité et la capacité d'augmentation rapide des populations de P. manihoti.

     

Host feeding and ovipositor insertion as sources of mortality in the mealybug Phenacoccus herreni caused by two encyrtids, Epidinocarsis diversicornis and Acerophagus coccois

Females of Epidinocarsis diversicornis (Howard) killed cassava mealybugs, Phenacoccus herreni Cox & Williams, through host feeding and piercing (i.e. ovipositor insertion and its consequences). Parasitoids fed on 9% of 592 hosts in which ovipositor insertion was achieved. For hosts which were attacked but not fed on, mortality in the first 72 h was significantly greater than that of controls and was highest in the first nymphal instar. No host feeding by Acerophagus coccois Smith was observed in 494 attacks. Mortality due to piercing was significantly greater than control values, but did not differ between host life stages.

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Résumé La prise de nourriture et les piqûres (c'est-à-dire l'insertion de la tarière et ses conséquences) de Epidinocarsis diversicornis tuent Phenacoccus herreni. Les adultes s'alimentent sur 9% des 592 cochenilles dans lesquelles la tarière a pénétré. La mortalité au cours des 72 premières heures est beaucoup plus élevée chez les hôtes attaqués mais qui n'avaient pas subi une prise de nourriture, que chez les témoins; elle était particulièrement élevée chez les cochenilles du premier stade larvaire. Pour 494 attaques par Acerophagus coccois, aucune prise de nourriture n'a été observée; la mortalité était plus élevée que chez les temoins, sans qu'il y ait eu de différences suivant les stades.

     

Host preferences of two encyrtid parasitoids for the Columbian Phenacoccus spp. of cassava mealybugs

In a choice test among six life stages of Phenacoccus herreni Cox & Williams, Epidinocarsis diversicornis (Howard) used its antennae to examine adult and 3rd stadium females more than other stages and preferentially attempted to oviposit in these plus 2nd stadium females. Success of ovipositor insertion was unaffected by host stage. The outcome of these behaviors was preferential oviposition by E. diversicornis in the large female host stages. Acerophagus coccois Smith also preferentially examined larger female mealybugs (second and third stadium nymphs and adults) more than other stages and successfully inserted its ovipositor in these stages more often than in second stadium male nymphs and male cocoons, resulting in a similar preference in this species for larger female host stages. When given a choice between adult female hosts of two species, P. herreni and Phenacoccus gossypii Townsend & Cockerell, E. diversicornis exhibited a clear preference for P. herreni; whereas A. coccois preferred P. gossypii.

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Résumé Epidinocarsis diversicornis (Howard), ayant la possibilité de choisir entre six stades différents de Phenacoccus herreni Cox & Williams, examine avec ses antennes plus particulièrement les adultes et les larves femelles du 3ème stade, et essaie de pondre de préférence dans ces stades et les larves femelles de second stade. L'insertion de la tarière s'effectue aussi bien quel que soit le stade de l'hôte. Il résulte de ces différents aspects du comportement que E. diversicornis pond de préférence dans les femelles des stades les plus avancés. Acerophagus coccois Smith préfère aussi examiner les cochenilles femelles les plus grosses (second et 3ème stade larvaires et adulte), et introduit sa tarière avec succès dans ces stades plus souvent que dans les larves mâles de second stade ou les cocons mâles; il en résulte aussi pour cette espèce une préférence pour les femelles des stades les plus gros.Quand on leur a donné le choix entre des femelles des deux espèces de cochenilles (P. herreni et Phenacoccus gossypii Towsend & Cockerell), E. diversicornis manifestait une nette préférence pour P. herreni, tandis que A. coccois préférait P. gossypii.

     

Comparative life table statistics of Apoanagyrus lopezi reared on the cassava mealybug Phenacoccus manihoti fed on four host plants

The demographic statistics of Apoanagyrus lopezi De Santis (Hymenoptera: Encyrtidae) were studied in the laboratory on its host, the cassava mealybug Phenacoccus manihoti Matile-Ferrero (Homoptera: Pseudococcidae), reared on four host plants characterized by different levels of antibiotic resistance to the mealybug: two cassava varieties, Incoza and Zanaga (Manihot esculenta Crantz: Euphorbiaceae), the faux-caoutchouc (hybrid of M. esculenta × M. glaziovii Muel. Arg.) and Talinum (Talinum triangulare Jack:Portulacaceae).Total and daily mean fecundities of female parasitoids were strongly influenced by the host plant but there was no link with antibiotic resistance. The mean duration of the oviposition period was also significantly modified by the host plant and was again not correlated to the level of antibiotic resistance. Net reproduction rates of female parasitoids were nearly 2 times higher on hosts fed on Zanaga and Talinum than on Incoza and Faux-caoutchouc, and were not related to the total fecundities. The generation time was significantly longer on Faux-caoutchouc than on the other three plants. The intrinsic rate of increase varied significantly with host plants and was higher on Talinum and Zanaga than on Incoza and Faux-caoutchouc. With the varieties of cassava, Incoza and Zanaga, it was observed that antibiosis had a significant negative effect on the survival of A. lopezi, which would influence the effectiveness of the parasitoid.     

Host stage selection of the mealybug parasitoid Anagyrus spec. nov near sinope

The mealybug parasitoid Anagyrus spec. nov near sinope (Hymenoptera: Encyrtidae) is an undescribed parasitoid of the Madeira mealybug, Phenacoccus madeirensis Green (Homoptera: Pseudococcidae). We investigated the preference of Anagyrus spec. nov near sinope for six developmental stadia (first‐ and second‐instar nymphs, third‐instar immature females, third‐ or fourth‐instar immature males, pre‐reproductive adult females, and ovipositing adult females) of P. madeirensis and the fitness consequences of the host stage selection behavior. In the no‐choice test, Anagyrus spec. nov near sinope parasitized and completed development in all host stadia except third‐instar immature males. When all host stadia were offered simultaneously, the parasitoids preferred third‐instar immature and pre‐reproductive adult females. Dissection of the stung mealybugs revealed that the clutch size (number of eggs per host) was approximately four and three in the third‐instar and pre‐reproductive females, respectively, and one egg per first‐instar nymph. Parasitoids emerged from P. madeirensis parasitized at third‐instar or pre‐reproductive adult female completed development in the shortest duration, achieved a higher progeny survival rate, larger brood and body size, and the lowest proportion of males. We showed that the continued development of mealybugs had significant influence on the fitness of the parasitoids. Although deposited as eggs in first‐ or second‐instar nymphs, parasitoids emerged from mummies that had attained third‐instar or adult development achieved similar progeny survival rate, brood size, body size, and sex ratio as those parasitoids deposited and developed in third‐instar or adult mealybugs. By delaying larval development in young mealybugs, Anagyrus spec. nov near sinope achieved higher fitness by allowing the parasitized mealybugs to grow and accumulate body size and resources. We suggest that the fitness consequence of host stage selection of a koinobiont parasitoid should be evaluated on both the time of parasitism and the time of mummification.     

Field placement of mealybug-infested potted cassava plants for the study of parasitism of Phenacoccus herreni

During 4-day field exposure intervals, Phenacoccus herreni Cox & Williams, third-instar mealybugs on artificially infested potted cassava plants were reduced 73% from initial densities of 235.7–1100.2/infested plant to 63.7–314.2/plant due to dispersal, rain, and predation. Frequency of parasitoid attack did not differ between high and low mealybug densities. The same species of parasitoids, in approximately the same proportions, were reared from mealybugs on artificially infested potted plants as from field mealybugs (Acerophagus coccois) Smith, 88.1% and Epidinocarsis diversicornis (Howard), 11.3%. Parasitoid attack rates on artificially exposed mealybugs, when combined with a simulation model of parasitism, accurately predicted observed levels of stage-specific parasitism in the field population.

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Résumé Pendant des expositions de 4 jours dans la nature de plants en pots de M. esculenta contaminés artificiellement par des P. herreni du troisième stade, les densités de cochenilles ont été réduites de 73%: de 235.7–1100.2/par plant contaminé à 63.7–314.2/par plant, par suite des évasions, de la pluie et de la prédation. Les attaques de parasitoïdes ne changent pas suivant les densités de cochenilles. Les mêmes espèces de parasitoïdes, ont été élevées dans à peu près les mêmes proportions (Acerophagus coccois, 88.1%, et Epidinocaris diversicornis, 11.3%) à partir de cochenilles sur pots artificiellement contaminés ou de manioc de la nature. Les taux d'attaques par les parasitoïdes sur les cochenilles artificiellement exposées, associés à un modèle de simulation du parasitisme, ont permis de prévoir avec précision les niveaux de parasitisme observés pour chaque stade dans la population de la nature.

     

Interspecific host discrimination and competition in Apoanagyrus (Epidinocarsis) lopezi and A.(E.)diversicornis, parasitoids of the cassava mealybug Phenacoccus manihoti

Abstract.

• 1 Choice experiments on interspecific host discrimination in A.lopezi and A. diversicornis were carried out on discs of cassava leaf containing four hosts (P.manihoti) that had been parasitized by the other species and four unparasitized hosts.
• 2 A.lopezi accepted both host types equally for oviposition, whereas A.diversicornis accepted fewer hosts that had been parasitized by A.lopezi than unparasitized ones. A.diversicornis is therefore capable of interspecific host discrimination, but such a capability was not demonstrated for A.lopezi.
• 3 Survival probability in singly parasitized hosts was 0.85 for both parasitoid species. When the time interval between ovipositions was 2 h or less, survival in multiparasitized hosts was 0.68 for A.lopezi and 0.17 for A.diversicornis, irrespective of priority. Increasing A.lopezi priority to 24±2h did not increase A.lopezi survival. A.diversicornis survival, however, increased to 0.43 when A.diversicornis was given 24 ± 2 h priority. A.diversicornis eggs took 19 h longer than A.lopezi eggs to hatch. This could explain the difference in competitive abilities in multiparasitized hosts.
• 4 The observed difference in host selection behaviour between A.lopezi and A.diversicornis is in accordance with the different benefits of multiparasitism: A.lopezi gains more than A.diversicornis because of its superior within-host competitive abilities.
• 5 Neither species avoided multiparasitism completely. The low survival probability of A.diversicornis in multiparasitized hosts may partly explain its failure to establish when introduced into Africa as part of a biological control programme of P.manihoti.

     

The role of kairomones in prey finding by Diomus sp. and Exochomus sp., two coccinellid predators of the cassava mealybug, Phenacoccus manihoti

We studied searching behaviour of Diomus sp., a coccinellid predator introduced into Africa as a natural enemy of the cassava mealybug, when searching on cassava leaves, and compared its behaviour with the searching behaviour of Exochomus sp., an African predator of mealybugs (MB's). Female adults of Diomus and Exochomus spent more time searching on cassava leaves previously infested with cassava MB than on clean cassava leaves, in response to substances produced by MB's (wax and/or honeydew) still present on these leaves as kairomones after removal of the MB's. Both species were also arrested by wax and/or honeydew of the citrus mealybug, Planococcus citri. When offered a choice between kairomones of both MB species only experienced Diomus (reared on cassava MB) showed a clear preference for kairomone of cassava MB. Separate influences of wax and honeydew were tested. Wax from cassava MB was an arrestment stimulus for both coccinellid species. Honeydew produced by cassava MB arrested Exochomus and inexperienced Diomus.

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Zusammenfassung Das Suchverhalten auf Cassaveblätter des coccinelliden Raübers Diomus, eines aus Süd Amerika importierten natürlichen Feindes der Cassaveschmierlaus wurde studiert und verglichen mit dem Suchverhalten eines afrikanischen Räubers von Schmierläusen, Exochomus sp.. Weiblichen Adulten von Diomus un Exochomus verwendeten mehr Zeit auf Cassaveblätter wenn diese Blätter vorher mit Cassaveschmierläuse infiziert waren als auf uninfizierte Blätter, und gebrauchten Substanzen (Wachs und/oder Honigtau) die von Schmierläuse produziert wurden und nach der Entfernung der Schmierläuse auf die Blätter zugeblieben waren als Kairomonen.Beide Arten wurden auch von Wachs und/oder Honigtau der Citrusschmierlaus, Planococcus citri, auf den Blätter arretiert. Wenn die Tiere wahlen könnten zwischen Kairomone der beiden Schmierlausarten wurden die Kairomonen der Cassaveschmierlaus nur von erfahrenen Diomus-Individuen, die auf Cassaveschmierlaüse aufgezogen wurden, bevorzugt.Die Einflüsse von Wachs und Honigtau wurden separat geprüft. Wachs von Exuvien der Cassaveschmierlaus ist ein Arretierungsstimulus für beide Räuberarten. Von Cassaveschmierläusen produzierten Honigtau arretierte Exochomus-und unerfahrene Diomus-Individuen.

     

Electrically recorded feeding behaviour of cassava mealybug on host and non-host plants

The feeding behaviour of cassava mealybug (Phenacoccus manihoti) was analysed by the electrical penetration graph technique (EPG, DC-system) and by light microscopy. This study confirmed a typical phloem-feeding behaviour with an aphid-like predominance of extracellular pathways of stylets. Similarities of EPGs from mealybugs with those of aphids and whiteflies allowed adoption of standard pattern labelling. The main differences with aphid EPGs consisted of fewer but longer intracellular punctures (pd duration of 20 svs 5–7 s for aphids), longer times to the first phloem-ingestion period and a lower motility of stylets within the phloem searching process. Comparison of the feeding behaviour on 6 plant types, including two occasional hosts (Talinum and poinsettia), one cassava hybrid and three common cassava cultivars (Manihot esculenta), allowed differentiation of penetration profiles. Intracellular punctures were shorter on occasional hosts, on which phloem finding and subsequent ingestion were markedly delayed although a great variability within plants persisted. Chemical analysis of some secondary plant substances revealed that none of the plants tested contained detectable amounts of alkaloids, and that cyanides were restricted to true hosts (cassavas andManihot hybrid). Levels of total flavonoids did not differ between hosts and non-hosts, in contrast to those of phenolic acids. Preliminary correlations with EPG paterns are discussed.

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Résumé Le comportement alimentaire de la cochenille du manioc (Phenacoccus manihoti) a été étudié par électrographie de pénétration (EPG, analyse en courant continu) et par microscopie optique. Cette étude a permis de confirmer le caractère typiquement phloémophage de l'alimentation de cet Homoptère, présentant une large prédominance du trajet extracellulaire des stylets, comme cela est également observé chez les pucerons. Les similitudes des tracés EPG effectués sur cochenille et sur pucerons ou aleurodes ont permis d'adopter la même typologie du signal. Les principales différences avec les pucerons concernent le nombre moins important et la durée plus longue des ponctions intracellulaires (20 s en moyenne contre 5 à 7 s chez les pucerons), l'allongement du temps d'accès au phloème et une moins grande mobilité des stylets lors de la phase de recherche du phloème. La comparaison du comportement alimentaire sur 6 plantes, parmi lesquelles deux h?tes occasionnels (Talinum et poinsettia), un hybride et trois variétés courantes de manioc (Manihot esculenta), a permis de différencier plusieurs profils de pénétration. Les ponctions intracellulaires se sont révélées plus courtes sur h?tes occasionnels, qui induisent également, malgré la variabilité observée, un allongement net de la période de localisation du phloème et donc un retard à l'ingestion. Aucune des plantes testées ne contient d'alcalo?des, et les composés cyanés se restreignent au genreManihot, h?te naturel de la cochenille. Les flavono?des totaux ne permettent pas de distinguer plantes h?tes et non-h?tes, à la différence des acides phénoliques.

     

Measuring host finding capacity and arrestment of natural enemies of the cassava mealybug,Phenacoccus manihoti, in the field

In unifested fields, 80 cassava tips were artificially infested with 0, 1, 2, 4, 8, 16, 32, or 64 third instars, and 20 or 100 eggs of cassava mealybug,Phenacoccus manihoti Matile-Ferrero (Hom., Pseudococcidae). Another 80 uninfested tips served as a control. Tips were arranged in a circle of 28 m diameter, in the centre of which the following exotic natural enemies ofP. manihoti were released:Apoanagyrus (Epidinocarsis) lopezi De Santis andA. diversicornis (Howard) (Hym., Encyrtidae),Hyperaspis notata (Mulsant) andDiomus hennesseyi Fürsch (Col., Coccinellidae), and others. This experiment was repeated six times. During the 4–14 days following release, all experimental tips were inspected at two-hour intervals during each day and the presence of exotic as well as indigenous natural enemies, likeExochomus troberti Mulsant (Col., Coccinellidae), ants and spiders was noted. The experiment was repeated six times measured the aggregative response by the natural enemies to different host densities, achieved through host attractance and arrestment. All exotic natural enemies, except the males ofApoanagyrus spp., were fast attracted to the host colonies. As compared to the control tips, they concentrated on the infested tips about 50-fold for the twoApoanagyrus spp. and 10 to 20-fold for the exotic coccinellids. By contrast, non-coevolved indigenous coccinellids, as well as generalist predators like ants and spiders were attracted to the infested tips only 2 to 5-fold.A. lopezi responded best to different host densities, followed byA. diversicornis and the coccinellids, followed by ants and spiders. None of the parasitoids or predators was particularly attracted to egg masses. These results correspond closely to the known efficiencies of these natural enemies,A. lopezi standing out among all candidates. The results of such aggregation studies are compared with those of life-table studies.     

Melanization and encapsulation of eggs and larvae of Epidinocarsis lopezi by its host Phenacoccus manihoti; effects of superparasitism and egg laying patterns

Encapsulation of Epidinocarsis lopezi (De Santis) (Hymenoptera, Encyrtidae) by the cassava mealybug Phenacoccus manihoti Matile-Ferrero (Homoptera, Pseudococcidae) was studied in the laboratory under controlled conditions (thermohygrometry and photoperiod as close as possible to field conditions): temperature, 26±1 °C; relative humidity, 80±10%; photoperiod, 12 h. Encapsulation began with melanin deposits forming on the parasitoid envelopes at different developmental stages: egg chorion and cuticle of L2 and L3 larvae. It led to the formation of an amorphous capsule from which parasitoids could occasionally escape. Encapsulation affected 26.7% of all parasitoids in solitary parasitism. There was a highly significant increase in the level of encapsulation (83.3%) in superparasitism. Encapsulation was more likely when egg laying occurred in the median body zone of host mealybugs but it was not related either to the sequence of eggs deposited or to the duration of egg laying. These results have significant implications for the assessment of E. lopezi parasitoid efficiency and should be considered in the current biological control program on P. manihoti in Africa.

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Mélanisation et encapsulement des ufs et des larves d'Epidinocarsis lopezi par son hôte Phenacoccus manihoti: effets du superparasitisme et des modalités de la ponte

Résumé L'encapsulement d'Epidinocarsis lopezi (De Santis) (Hyménoptère, Encyrtidae) par la cochenille du manioc Phenacoccus manihoti Matile-Ferrero (Homoptère, Pseudococcidae) a été étudié au laboratoire en conditions standardisées de thermohygrométrie et de photopériode aussi proches que possible de celle existant sur le terrain: température: 26±1 °C; hygrométrie relative: 80±10%; photopériode: 12 heures.Le phénomène débute par un dépot de mélanine sur les enveloppes du parasitoïde à différents stades de son développement: chorion de l'uf ou cuticule des larves L2 et L3. Il aboutit à la formation d'une capsule amorphe dont le parasitoïde parvient parfois à s'échapper. L'encapsulement affectant 26,7% des individus en situation de parasitisme solitaire est très significativement augmenté dans le cas de superparasitisme où ce taux concerne jusqu'à 83,3% des Hyménoptères en développement mais dans ces situations de superparasitisme, un Hyménoptère adulte est toujours obtenu d'une cochenille infestée.L'encapsulement est par ailleurs favorisé lorsque la ponte du parasitoïde s'effectue dans la région médiane de la cochenille mais ne dépend pas du rang de ponte des ufs et de la durée de la piqûre.Nos résultats, confirmés par des travaux de terrain au Congo, indiquent qu'un tel taux d'encapsulement a une incidence sur l'efficacité parasitaire d'Epidinocarsis lopezi et qu'il doit être pris en considération dans le progamme de lutte biologique en cours en Afrique contre Phenacoccus manihoti.