The challenge of biological control of Cosmopolites sordidus Germar (Col. Curculionidae): A review

The banana weevil (also known as banana root borer) Cosmopolites sordidus Germar (Coleoptera Curculionidae) is the major pest of banana and plantain. Because banana ranks 2nd in fruit production worldwide, this pest has substantial social and economic importance. The biological control of the C. sordidus remains challenging because of its behaviour and resistance to parasitism and predation. The last review concerning the biological control of C. sordidus was published two decades ago, and relevant knowledge and methods have developed in the interim. The present paper provides an update of that knowledge and summarizes past and current challenges as well as providing perspectives on achieving sustainable control of C. sordidus. We first discuss studies on the classical biological control of C. sordidus, underlining the limits of classical biological control methods such as the importation of predators, parasitoids or pathogens. Next, we consider conservation biological control of C. sordidus, with a focus on ants. We also highlight an ‘arthropod bias’ that has led to a lack of information on the role of vertebrates in the regulation of C. sordidus.     

Potential of Beauveria bassiana (Hyphomycetes: Moniliales) for controlling the white pine weevil, Pissodes strobi (Col., Curculionidae)

Abstract:  Studies were conducted under laboratory conditions to document the potential of Beauveria bassiana conidia applications for controlling the white pine weevil, Pissodes strobi (Peck). A screening test including six B. bassiana isolates allowed us to demonstrate that CFL (Centre de Foresterie des Laurentides) and IP-CPB (Île Perrault-charançon du pin blanc) were the most virulent isolates among the ones tested, with percentages of mortality after 3 weeks of 73% and 85.5%, respectively. These two B. basiana isolates were applied either onto soil or branch sections to compare the effectiveness of these potential control strategies. Greater than 75% mortality was observed within 3 weeks for both modes of application using suspensions of B. bassiana at a concentration of 1.0 × 10⁸ (soil application) and 1.0 × 10⁹ conidia/ml (branch application). The results demonstrate for the first time that B. bassiana is an effective entomopathogen against P. strobi .     

Attractant for the sugar-beet weevil Conorrhynchus (Cleonus) mendicus (Col.: Curculionidae)

Abstract:  Traps baited with a 1 : 1 : 1 mixture of Grandlure I [ cis -1-methyl-2-(1-methylenethenyl)-cyclobutaneethanol], Grandlure II [( Z )-2-ochtoden-1-ol; ( Z )-2-(3,3-dimethylcyclohexylidene)ethanol] and Grandlure III–IV [( Z )- and ( E )-2-ochtodenal; ( Z )- and ( E )-(3,3-dimethyl)cyclohexylidene)acetaldehyde] caught significantly more Conorrhynchus (Cleonus) mendicus Germar (Col.: Curculionidae) weevils than traps without bait. Later tests revealed that only Grandlure III–IV was responsible for attractivity. Both sexes were attracted according to a random sample of captures. C. mendicus appeared to be very similar in its responses to the synthetic aggregation attractant as the closely related Bothynoderes (Cleonus) punctiventris (Germar), in which species, the attraction to Grandluree III–IV has recently been published. Doses from 500 to 5000  μ g of Grandlure III–IV on rubber dispensers performed satisfactorily in monitoring trials and can be recommended for use in practical trapping applications for C. mendicus .     

The nematode Neoaplectana carpocapsae and the beet armyworm Spodoptera exigua: Infectivity of prepupae and pupae in soil and of adults during emergence from soil

The nematode, Neoaplectana carpocapsae, infected >90% of the prepupae of Spodoptera exigua in soil even at concentrations as low as five nematodes/cm² of soil surface. Pupae were less susceptible to nematode infection in soil than prepupae, with mortality ranging from 10 to 24% and 10 to 83% for pupae exposed 3–5 days and 6–8 days to the nematode, respectively. Longer exposure (6–8 days) of the pupae to the nematode resulted in higher mortality with a positive relationship with increasing concentrations. Adults of S. exigua were susceptible to nematode infections as they emerged from the soil. The higher nematode concentrations (25 and 50 nematodes/cm²) resulted in higher adult mortality. The majority of nematode-induced mortality occurred within 24 hr after emergence. The susceptibility of emerging S. exigua adults to N. carpocapsae offers a new dimension for insect control.     

The influence of temperature on the susceptibility of vine weevil, Otiorhynchus sulcatus (Fabricius) (Coleoptera: Curculionidae), larvae to Metarhizium anisopliae (Deuteromycotina: Hyphomycetes)

Mortality of Otiorhynchus sulcatus (Fabricius) larvae at 10^oC, 15^oC, 20^oC and 25^oC following treatment with 10⁷conidia ml“¹suspensions of six Metarhizium anisopliae (Metschnikoff) Sorokin isolates was temperature dependent. In all cases, the LT₅₀s were inversely related to temperature, but the nature of this response varied between isolates. Strain 101-82 was the most virulent isolate at 25^oC with an LT₅₀ of 3.7 days, but it was the least virulent isolate at 15^oC and it failed to kill any O. sulcatus larvae at 10^oC. In contrast, strain 159-83 had the lowest virulence at both 20^oC and 25^oC, whereas it was the most virulent isolate at 10^oC with an LT₅₀ of 20.0 days. The mortality rates followed a similar pattern and were positively related to temperature in all cases with the exception of strain 159-83 at 25^oC. Mycosis development was examined on larvae treated with strain 275-86 and significant differences were obtained between all four temperatures. Sporulation commenced after approximately 2.75 days at 25^oC, but took nearly 11 days at 10^oC. The infection rates also varied between temperatures; sporulation occurred on 98% of the treated larvae at 25^oC, but only on 93%, 87% and 49% of the larvae at 20^oC, 15^oC and 10^oC, respectively. The results of these bioassays demonstrate that temperature has a significant effect on the virulence of M. anisopliae. The differences between fungal strains also emphasises the importance of selecting isolates for specific situations on the basis of their temperature profiles.     

Host-size preference of the parasitoidAnisopteromalus calandrae [Hym: Pteromalidae] onSitophilus zeamais (Col.: Curculionidae) larvae with a uniform age distribution

First generationAnisopteromalus calandrae (Howard) collected from commercial stored maize in South Carolina were exposed to a mixture of all sizes of immatureSitophilus zeamais Motschulsky, representative of a uniform age distribution, in shelled maize. Eighty-seven percent of parasitism is expected on larvae with tunnel diameters of 0.9 to 1.8 mm and 6% on prepupae and pupae, given this host-size distribution. Preference was greatest for large host larvae (1.6 mm diameter), intermediate for other larvae in the range 0.9 to 1.8 mm, and least for pupae and small larvae. Host-stage preference is discussed with respect to Chesson's (1983) parameters for preference, α_i, probability of parasitism, P_i, and electivity index, ?_i.     

Response to host age of the egg parasitoid Anaphes n.sp. (Hymenoptera: Mymaridae)

The mymarid Anaphes n.sp. was observed to parasitize the eggs of the carrot weevil Listronotus oregonensis (LeConte) up to 138 h old at 23±1°C and 18L:6D. Adult emergence of the parasitoid was observed in 85%‐97.5% of the weevil eggs 42–138 h old and host embryogenesis was interrupted in nearly 100% of these eggs. In host eggs of 18 h old, parasitism was very high but not all parasitoids completed their development and their subsequent emergence was generally retarded. An.sp. could parasitize host eggs 162 h old, but such an attack rarely retarded the normal development of the host. The parasitoid was unable to complete its development in sterile carrot weevil eggs.     

Observations on the host specificity and biology of Lixus salsolae (Col., Curculionidae), a potential biological control agent of Russian thistle, Salsola tragus (Chenopodiaceae) in North America

Abstract:  No-choice host specificity tests were performed on Lixus salsolae Becker (Col., Curculionidae) in a quarantine green house near Montpellier, France. Several varieties of seven species of economic and ornamental plants from six genera of Chenopodiaceae were tested. Adult feeding was observed on almost all test plants and larvae successfully developed on nine of the eleven species/varieties tested. Sex ratio of field-collected overwintering adults was close to 1 : 1. While no-choice tests may indicate a wider host range under field conditions, we no longer consider L. salsolae as a potential biological control agent of Salsola tragus L. (Chenopodiaceae) in North America.     

Predation of Clitostethus arcuatus (Col.: Coccinellidae) on Trialeurodes vaporariorum (Hem.: Aleyrodidae)

Greenhouse whitefly, Trialeurodes vaporariorum, is a serious pest of glasshouse crops. It shows resistance to different insecticides and growers are interested in finding other useful control methods. This research was carried out to study the predation potential and biology of Clitostethus arcuatus (Rossi) as one of the most important predators of this pest. Adult C. arcuatus were reared on tobacco leaves bearing colonies of greenhouse whitefly eggs under controlled conditions (25±2°C, 65±5% RH and 16 h L:8 h D). Results showed that the average developmental time of the egg, first through fourth instar larva and pupa were 2.82±0.12, 4.47±0.14, 4.54±0.1, 6.3±0.2, 7±0.22 and 3.8±0.13 days, respectively; and longevity of female and male were 66.4±2.6 and 54.9±2.5 days, respectively. The average feeding rates of female, male and larvae (first through fourth) were 61.4±0.7, 27.6±0.9 eggs/day and 12±1.03, 30.3±2.4, 41.3±2, 68.04±2 eggs/day, respectively. The larvae consumed an average of 992.2±36 eggs during the total larval developmental period with a daily mean of 45.8±0.5. A significant difference was shown between the feeding rate of fourth instar larval stages and between sexes. Females, males and one pair of C. arcuatus (♀,♂) consumed an average of 17.2±0.4, 10.6±0.8, 23.1±0.5 nymph/day; 28.5±0.9, 20.3±0.6, 47.2±0.6 pupa/day and 8±0.3, 6.5±0.54, 13.6±0.4 adult/day, respectively. The feeding rate was significantly different among whitefly life stages. Females laid an average of 3±0.23 eggs/day.     

Suppression of Anthonomus eugenii (Coleoptera: Curculionidae) pepper fruit infestation with releases of Catolaccus hunteri (Hymenoptera: Pteromalidae)

The pepper weevil, Anthonomus eugenii Cano, is an important pest of Capsicum spp. pepper in Florida, Puerto Rico, and Central America. Catolaccus hunteri Crawford is the most abundant parasitoid attacking pepper weevil larvae in Florida. Weekly releases of C. hunteri at a rate of 1600 adults per 0.2-ha plot in organically-grown bell pepper, C. annuum L., beginning at first bloom resulted in fewer weevil infested fruit compared to 0.2-ha plots where no parasitoids were released. Weekly releases of C. hunteri adults on nightshade, Solanum americanum Mill, during the fall/winter off-season followed by weekly releases of the same parasitoid in adjacent bell pepper during the spring in-season resulted in fewer infested pepper fruit compared to off-season nightshade and in-season pepper where no parasitoids were released. The results of these experiments demonstrate the potential of augmentative releases of C. hunteri for suppressing infestations of pepper fruit by pepper weevil larvae.     

Host stage preference, functional response and mutual interference of Aphidius matricariae (Hym.: Braconidae: Aphidiinae) on Aphis fabae (Hom.: Aphididae)

Host stage preference, functional response and mutual interference of Aphidius matricariae (Haliday) (Hym.: Braconidae: Aphidiinae), parasitoid of the black bean aphid, Aphis fabae Scopoli (Hom.: Aphididae) were investigated in a growth chamber at a temperature of 25°C, 65% relative humidity and a photoperiod of 16 h light : 8 h dark on the PP8 variety of sugar beet. Nicholson's model and linear regression were used to determine per capita searching efficiency and interference coefficient, respectively. The highest parasitism percentage was observed on the third instar nymphs of A. fabae in both choice and no‐choice preference tests. There was significant difference between rates of parasitism on different stages of A. fabae (P < 0.01). Using logistic regression, a type II functional response was determined for A. matricariae. The Holling and Rogers models were used for estimating searching efficiency (a) and handling time (T_h). The data was fitted by the Rogers equation better than by the Holling disc equation based on the R² values. The estimated values of searching efficiency and handling time were 0.040 ± 0.013/h and 3.439 ± 0.383 h, respectively. The per capita searching efficiency decreased significantly from 0.272 to 0.139 as parasitoid densities increased from one to five. Therefore, different host‐parasitoid ratios could affect the efficacy of A. matricariae.     

Application of Metarhizium anisopliae (Metsch.) Sor. conidia to control Otiorhynchus sulcatus (F.) (Coleoptera: Curculionidae) larvae on glasshouse pot plants

The efficacy of the entomogenous fungus Metarhizium anisopliae was assessed against vine weevil (Otiorhynchus sulcatus) larvae in the glasshouse. Prophylactic application of M. anisopliae conidia to begonia resulted in total larval control, but curative applications were less effective with only 65% control when conidial application was delayed until 8 weeks after egg infestation. Prophylactic applications also provided effective larval control on begonia plants which received multiple egg applications over a six week period. Larval mortality was monitored on cyclamen plants which had received a prophylactic drench of M. anisopliae conidia. The population was reduced by 78% within 5 weeks of egg application and control rose to 90% after 17 weeks, although the increase was not significant. Prophylactic conidial drenches were compared with a similar number of compost incorporated conidia on cyclamen, but there was no significant difference between the two spore application strategies. Application of M. anisopliae conidia to impatiens modules before potting-on resulted in over 89% larval control compared to over 97% control when a similar number of conidia were applied to the plants after potting. Larval control was further reduced to 79% when the module drenches were reduced to one quarter of the highest dose (5 × 10⁷ compared to 2 × 10⁸ conidia per module). The persistence of three M. anisopliae strains was examined over a 20 week period on impatiens. There was no overall decline in efficacy over this period, although there was variability in the performance of the different strains and it was suggested that this was linked to temperature. The results of these experiments suggest that M. anisopliae has considerable potential as a microbial control agent for O. sulcatus on glasshouse ornamentals.     

Take-off capacity as a criterion for quality control in mass-produced predators,Rhizophagus grandis (Col.: Rhizophagidae) for the biocontrol of bark beetles,Dendroctonus micans (Col.: Scolytidae)

Time spent by adult beetles in cold storage at 3–7°C accounted for 81% of the loss of take-off capacity inRhizophagus grandis Gyllenhal in windtunnel experiments. At the age of three weeks, the insects were at their highest take-off capacity at about 80%. This was followed by a steady decrease, 7% of the insects failing to take-off each month. Changes in the fat reserves during cold storage could explain at least partly this reduction of flight capacity although there was no significant difference in fresh weight between insects that were able/unable to take-off. Sex had a significant influence on take-off rates, with an 8.7% higher take-off rate in females. Take-off capacity was further reduced when the insects were mass-produced in cultures using parent beetles submitted to a blend of synthetic oviposition stimulants instead of live prey larvae. Response to synthetic attractants by those insects which took-off, however, was not influenced by cold storage or by the use of synthetic stimulants in the culture medium.

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Résumé Le temps passé en conservation à basse température (3–7°C) depuis la métamorphose est intervenu pour 81% dans la perte de la capacité d'envol chez le coléoptère prédateurRhizophagus grandis Gyll. lors d'expériences en tunnel de vol. A l'age de trois semaines, les insectes sont à leur plus haut niveau d'envol (envol d'environ 80% des insectes). Par la suite, il y a un déclin constant de la capacité d'envol, à raison de 7% des insectes chaque mois. Des changements dans les réserves lipidiques peuvent partiellement expliquer cette réduction, bien qu'il n'y ait pas eu de différence entre le poids frais d'insectes capables de s'envoler et celui d'individus qui en étaient incapables. Le sexe a une influence sur le taux d'envol, avec un taux d'envol significativement plus élevé de 8.7% chez les femelles. La capacité d'envol est encore réduite chez des insectes qui ont été produits dans des élevages de masse où les parents étaient soumis à un mélange de stimuli de ponte de synthèse au lieu d'être mis en présence de larves deD. micans vivantes. Chez les insectes qui prennent leur vol, cependant, la réponse aux attractifs de synthèse est indépendante de l'age ainsi que des conditions d'élevage.

     

Conservation of two predator species for biological control ofChrysophtharta bimaculata (Col.: Chrysomelidae) in tasmanian forests

Chrysophtharta bimaculata (Olivier) (Coleoptera: Chrysomelidae) is a major defoliator of regeneration eucalypt trees in Tasmania causing a significant reduction in height and diameter increment of trees which reduces wood volume per hectare. A study to conserve and enhance the efficiency of coccinellid species chieflyCleobora mellyi (Mulsant) (Coleoptera: Coccinellidae), and the cantharid,Chauliognathus pulchellus (Macleay) (Coleoptera: Cantharidae), for the biological control ofC. bimaculata was conducted in young regeneration forests in southern Tasmania from 1991–92. Cantharid adults and coccinellid adults and larvae feed onC. bimaculata eggs and, to a lesser extent, young larvae. The study found that coccinellids were more active throughout the egg and early (1^st and 2^nd) stage ofC. bimaculata. The cantharid, however was active only during the egg stage of the prey and then disappeared from the plantation. The coccinellids were therefore the most useful predators, but their population declined when the prey reached the 3^rd and 4^th stages. As shortage of food may account for this decline, supplementary food was provided in the form of sucrose sprays or sugar granules at a feeding station. This resulted in the retention of both predators and particularly the coccinellids and enhanced their efficacy.     

Control of the mushroom pests Lycoriella auripila (Diptera: Sciaridae) and Megaselia halterata (Diptera: Phoridae) by Steinernema feltiae (Nematoda: Steinernematidae) in field experiments

The nematode Steinernema feltiae (Nematoda: Steinemematidae) was tested for its ability to control two main mushroom pests i.e. the sciarid Lycoriella auripila (Diptera: Sciaridae) and the phorid Megaselia halterata (Diptera: Phoridae) in growing-rooms filled with spawned compost. A clear difference between female and male sciarid control was observed. A nematode application 1 day after casing preceded by an application 1 day before casing on the compost caused an almost complete control (97%) of the F1-generation of female sciarids. The F2-generation of females was similarly controlled (95%) by an application 7 days after casing. A dosage of 1 × 10⁶nematodes m^-2was found to be equally effective as higher dosages. Diflubenzuron remained active throughout entire the cropping period with high sciarid mortality rates varying from 72% to 99%. Phorid control was variable and seemed to depend on the presence of sciarids. In one occasion the control rate of F2-generation phorid larvae was 75% and was possibly caused by the presence of new infective juvenile nematodes recycled in F2-generation sciarid larvae. Diflubenzuron did not significantly reduce phorid numbers.     

Effects ofBacillus thuringiensis var.San diego on predation effectiveness,development and mortality ofColeomegilla maculata lengi (Col.: Coccinellidae) larvae

Laboratory experiments were conducted to determine the effects of M-One^™ (Bacillus thuringiensis var.san diego) on larval instars ofColeomegilla maculata lengi Timberlake. Coccinellid larval development (from egg hatch to adult), completed on pollen treated with suspensions of M-One^™ at 20 ml/litre (5.6×10⁸ CPBIU/litre) and 200 ml/litre, took respectively 29.3 and 38.5 days compared with 21.9 days for the control (water). M-One^™ did not cause larval mortality.C. maculata third instars did not show any preference between eggs ofLeptinotarsa decemlineata (Say) treated with water or with M-One^™ at 20 ml/litre. However, at 200 ml M-One^™/litre, the number of eggs attacked was 34.7% lower than the eggs treated with water only, 48 h after the beginning of the test. These results indicate that the use of M-One^™, at the manufacturer's recommended field rate of 20 ml/litre, does not cause a major threat to larvalC. maculata populations.

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Résumé Des bioessais en laboratoire ont été effectués afin de déterminer si les larves de la coccinelle maculée,Coleomegilla maculata lengi Timberlake (Col.: Coccinellidae), sont affectées par M-One^™, un insecticide biologique préparé à partir de la bactérieBacillus thuringiensis var.san diego Berliner et utilisé dans la lutte contre le doryphore de la pomme de terre,Leptinotarsa decemlineata (Say) (Col.: Chrysomelidae). Le développement larvaire, effectué sur du pollen traité avec des concentrations de 20 ml M-One^™/litre (5,6×10⁸ unités internationales de doryphore/litre) et 200 ml M-One^™/litre, a nécessité 29,3 et 38,5 jours respectivement, comparativement à 21,9 jours pour le témoin (eau). M-One^™ n'a pas causé de mortalité chez les larves. Au cours d'un test de 48 h, les larves de stade III n'ont montré aucune préférence entre des œufs traités avec 20 ml M-One^™/litre et des œufs traités avec de l'eau. Par contre avec 200 ml M-One^™/litre, le nombre d'œufs attaqués a diminué significativement de 34,7% par rapport au témoin, 48 h après le début du test. Ces résultats indiquent que l'utilisation de M-One^™ à la concentration recommandée de 20 ml/litre ne représente pas une menace pour les populations larvaires de la coccinelle maculée.

     

Effects of Application Rates of Steinernema feltiae (Nematoda: Steinernematidae) on Biological Control of the Mushroom Fly Lycoriella auripila (Diptera: Sciaridae)

The potential of Steinernema feltiae for the biological control of Lycoriella auripila was tested in commercial mushroom‐growing conditions. The nematodes, applied at rates of 1.5, 3, 6 or 12 x 10 ⁶ infective juveniles per 34 kg tray of spawn‐run compost, were mixed into the casing material before it was spread over the compost surface. When compared with untreated control trays, any rate of nematode application significantly reduced fly emergence. Insecticides significantly reduced mushroom yields; nematodes significantly increased them. At a rate of 3 x 10 ⁶ infectives/tray S. feltiae elicited mean total increases in the weight and numbers of mushrooms produced of 8% and 11% respectively. The nematodes also reduced the incidence of mushrooms spoiled by tunnelling sciarid larvae. The early decline in the numbers of nematodes persisting in casing was a trend that was reversed later, when evidence was obtained that S. feltiae was recycling in insects that had been killed. When applied at a rate of 3 ‐10⁶infectives/tray of compost S. feltiae should provide reliable and cost‐effective biological control of L. auripila.     

Efficacy of two entomopathogenic nematodes Heterorhabditis bacteriophora and Steinernema carpocapsae for control of the leopard moth borer Zeuzera pyrina (Lepidoptera: Cossidae) larvae under laboratory conditions

The biological traits of the entomopathogenic nematodes (EPNs), Steinernema carpocapsae and Heterorhabditis bacteriophora, against the larvae of the leopard moth, Zeuzera pyrina were evaluated in the laboratory. The traits included pathogenicity, penetration potential as well as foraging behaviour. Plate assays were performed using a range of EPN concentrations (5, 10, 20, 50 and 100 infective juveniles (IJs) per larva). The LC₅₀ values for S. carpocapsae and H. bacteriophora were 6.4 and 8.4 IJs larva^?1 after 72 h. Both EPN species caused high mortality in branch experiments. Significantly higher mortality rates occurred in the larger larvae after exposure to S. carpocapsae. Both EPN species successfully penetrated the Z. pyrina larvae as well as larvae of Galleria mellonella L. (Lepidoptera: Galleridae).The proportional response of H. bacteriophora to host-associated cues was strongly higher than S. carpocapsae in Petri dishes containing agar 1, 12 and 24 h after EPN application. These results highlight the efficiency of EPNs for the control of Z. pyrina larvae. However, due to the cryptic habitat of Z. pyrina larvae in their galleries in the trees, field trails need to be conducted to further evaluate this potential.