Effect of fallows on population dynamics of Cosmopolites sordidus: toward integrated management of banana fields with pheromone mass trapping

• 1 The banana weevil Cosmopolites sordidus Germar (Coleoptera: Curculionidae) is the most serious pest of banana and plantain in most production areas, including the West Indies.
• 2 During a period of 2 years, we assessed the efficacy of a pheromone mass‐trapping control strategy of C. sordidus in field conditions in Guadeloupe at different cropping stages, both in sanitation fallows and in different ratoon banana crops.
• 3 In the fallows, catches peaked 3 months after beginning trapping and then decreased to zero after 9 months. By contrast, for the new plantations, the catches of C. sordidus increased after the 11th month and, in the older banana fields, there was no decrease in C. sordidus catches. The C. sordidus catches increased in the neighbouring banana plots, whereas they decreased in the fallows, and these catches decreased with the distance from fallow.
• 4 In conclusion, mass trapping with synergized pheromone traps within fallows should allow better sanitation of banana plantations. Yet, within the farms, fallows must not be located next to new plantations to avoid massive damage to the young plants. More generally, the present study emphasizes that the control of this insect should be managed at the farm scale and not at the field scale, with special attention being paid to the location of fallows.

     

Banana defence responses to Cosmopolites sordidus feeding and methyl jasmonate application

Each year 25–75% of banana and plantain yields are lost because of rhizome damages caused by banana weevil (Cosmopolites sordidus) in growing regions of sub‐Saharan Africa. However, the specific plant defence response of the rhizome tissue in relation to the C. sordidus attack is unknown. Consequently, in this study, we evaluated whether plant defence substances in the rhizome are correlated with the degree of larval damage and whether applications of methyl jasmonate (MJ) elicit a greater induction of the plant defence potential against C. sordidus. Moreover, we attempted to reveal cellular modifications in response to the root feeding herbivore through histochemical staining. The banana cultivars “Km5” and “Mbwazirume” with tolerance and susceptibility to C. sordidus, respectively, were used in a pot experiment to evaluate percent rhizome damage, leaf chlorophyll content, total phenolic content (TPC), antioxidant capacity and cell morphology in response to C. sordidus attack and/or MJ applications compared to untreated control plants. We found that C. sordidus‐induced rhizome damage was 30% in the susceptible cultivar but less than 5% in the tolerant cultivar. The percent rhizome damage was not related to leaf chlorophyll content but showed a significant negative linear relationship to both TPC and antioxidant capacity. Larvae feeding induced a considerably greater increase of polyphenolic defence compounds in Km5 than in Mbwazirume; however, this response was opposite in the MJ treatment, suggesting that the phytohormone induced the susceptible plant to invest more into the synthesis of defence chemicals that in turn lead to reduced C. sordidus damage. Tissue staining demonstrated a greater deposition of lignin and suberin in C. sordidus challenged rhizome, presumably to seal off healthy tissue with a physical barrier from continued pest attack. It is concluded that MJ induces polyphenolics in susceptible Mbwazirume banana that reduced C. sordidus damage.     

The use of aggregation pheromone to enhance dissemination of Beauveria bassiana for the control of the banana weevil in Uganda

Candidate strains of Beauveria bassiana were identified for use in integrated pest management of the banana weevil Cosmopolites sordidus. Horizontal field transmission of B. bassiana between banana weevils using different delivery systems, including aggregation pheromones, was investigated. We observed that infected weevils could transmit the fungal pathogen to healthy individuals. Most dead weevils (52%) due to B. bassiana infection were found at the base of banana plants in the leaf sheath or in the soil near banana plants. Significantly more weevils died from the pathogen in plots where B. bassiana was applied in combination with the pheromone than where it was applied alone. Our data demonstrate that C. sordidus aggregation pheromone can be a valuable tool to enhance the dissemination of B. bassiana for the control of C. sordidus.     

Experimental evaluation of the impacts of two ant species on banana weevil in Uganda

The banana weevil, Cosmopolites sordidus (Germar), is an important pest of bananas. Predatory ants are increasingly being viewed as possible biological control agents of this pest because they are capable of entering banana plants and soil in search of prey. We studied ant predation on banana weevil in Uganda in crop residues and live plants in both laboratory and field experiments. Field studies with live plants used chemical ant exclusion in some plots and ant enhancement via colony transfer in others to measure effects of Pheidole sp. 2 and Odontomachus troglodytes Santschi on plant damage and densities of immature banana weevils.In crop residues, an important pest breeding site, twice as many larvae were removed from ant-enhanced plots as in control plots. In young (2 month) potted suckers held in shade houses, ant ability to reduce densities of banana weevil life stages varied with the weevil inoculation rate. At the lowest density (2 female weevils per pot), densities of eggs, larvae, and pupae were reduced by ants. At higher rates there was no effect. In older suckers (5–11 months) grown in larger containers, banana weevil densities were not affected by ants, but damage levels were reduced. In a field trial lasting a full crop cycle (30 months), we found that the ants tested reduced the density of banana weevil eggs in suckers during the crop, but did not affect larval densities in the sampled suckers. However, most larvae occur in the main banana plants, rather than associated suckers. Nevertheless, levels of damage in mature plants at harvest did not differ between Amdro-treated and ant-enhanced plots, suggesting the ant species studied were not able to provide economic control of banana weevil under our test conditions.     

New primary resource increases predation on a pest in a banana agroecosystem

• 1 Primary resources may affect the structure of species assemblages in upper trophic levels of food webs. These bottom‐up effects may involve important ecological processes that affect pest control. For example, population densities of natural enemies may increase when alternative preys are favoured by a new resource.
• 2 Ants, particularly Solenopsis geminata Forel (Myrmicinae), are recognized as effective predators of herbivores eggs. In the present study, we tested the hypothesis that the addition of a primary resource in a banana agroecosystem will increase pest control of the banana weevil Cosmopolites sordidus Germar (Coleoptera, Curculionidae) by ants.
• 3 Using stable isotope analyses, we showed that S. geminata used the new resource pathway provided by the addition of a cover crop. This change was revealed by increased δ¹³C values (¹³C/¹²C) in a cover crop treatment (C4 plant) compared with a banana (C3 plant) in bare soil treatment.
• 4 We also showed that the abundance of S. geminata, as measured with pitfall traps, was 4.8–5.4‐fold higher in the cover crop treatment than in the bare soil treatment. Estimation of egg predation rates was in the range 7.8–70.3%, which occurred in plots with the lowest and highest S. geminata numbers, respectively.
• 5 The addition of a new primary resource in this system changed the origin of the carbon consumed by predators and increased their densities. The increased ant abundance resulted in increased predation of weevil eggs, which was consistent with our hypothesis. These results will be useful for the design of cropping systems that enhance the biological regulation of pests.

     

Cover Cropping Alters the Diet of Arthropods in a Banana Plantation: A Metabarcoding Approach

Plant diversification using cover crops may promote natural regulation of agricultural pests by supporting alternative prey that enable the increase of arthropod predator densities. However, the changes in the specific composition of predator diet induced by cover cropping are poorly understood. Here, we hypothesized that the cover crop can significantly alter the diet of predators in agroecosystems. The cover crop Brachiaria decumbens is increasingly used in banana plantations to control weeds and improve physical soil properties. In this paper, we used a DNA metabarcoding approach for the molecular analysis of the gut contents of predators (based on mini-COI) to identify 1) the DNA sequences of their prey, 2) the predators of Cosmopolites sordidus (a major pest of banana crops), and 3) the difference in the specific composition of predator diets between a bare soil plot (BSP) and a cover cropped plot (CCP) in a banana plantation. The earwig Euborellia caraibea, the carpenter ant Camponotus sexguttatus, and the fire ant Solenopsis geminata were found to contain C. sordidus DNA at frequencies ranging from 1 to 7%. While the frequencies of predators positive for C. sordidus DNA did not significantly differ between BSP and CCP, the frequency at which E. caraibea was positive for Diptera was 26% in BSP and 80% in CCP; the frequency at which C. sexguttatus was positive for Jalysus spinosus was 14% in BSP and 0% in CCP; and the frequency at which S. geminata was positive for Polytus mellerborgi was 21% in BSP and 3% in CCP. E. caraibea, C. sexguttatus and S. geminata were identified as possible biological agents for the regulation of C. sordidus. The detection of the diet changes of these predators when a cover crop is planted indicates the possible negative effects on pest regulation if predators switch to forage on alternative prey.     

Different bioassays for investigating orientation responses of the banana weevil, Cosmopolites sordidus, show additive effects of host plant volatiles and a synthetic male-produced aggregation pheromone

Abstract Three different bioassay methods to investigate the orientation behaviour of the banana weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae), to host plant volatiles and a synthetic pheromone (cosmolure+) were compared. A locomotion compensator was used to separately record walking tracks in response to three odour sources. The data show that C. sordidus uses odour‐conditioned anemotaxis in its orientation to the odour sources tested. Of the two olfactometers tested, a dual port olfactometer using a continuous airflow showed stronger discrimination by C. sordidus to the different odours compared with a double pitfall olfactometer. The results of all three bioassays indicate that C. sordidus responds in an additive way to the combination of fermentation plant volatiles and the synthetic pheromone.     

Preference of Cosmopolites sordidus for fusarium wilt-diseased banana plants

The objective of this study was to understand the role of Cosmopolites sordidus in the dispersal of Fusarium oxysporum f. sp. cubense race 1 (Foc) and more specifically to determine whether C. sordidus is preferentially attracted to Foc-contaminated banana plant material vs. Foc-free material. The attraction of C. sordidus to healthy and Foc-contaminated Gros Michel banana bulbs and pseudostems, as well as to pure cultures of Foc, was compared using four-choice olfactometers. Males and females were studied separately. After storage in a dark room, weevils were placed in the central chamber of olfactometers. After 15 min, the orientation of each of the weevil was determined according to the food source located in each of the four peripheral chambers of the olfactometer. Overall, 560 olfactometer assays were carried out. Weevils were found to prefer Foc-infected plant tissues. Weevil preference was not significantly affected by weevil sex. The attraction of C. sordidus to Foc-contaminated plant material suggests that this insect could be important for the dissemination of Foc, especially in early stages of epidemics, when Foc-infected plants are scarce.     

Partial characterization of the proteolytic enzymes in the gut of the banana weevil, Cosmopolites sordidus, and effects of soybean Kunitz trypsin inhibitor on larval performance

The proteolytic enzymes in the gut of the banana weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae), have been characterized. Both larvae and adults rely on a complex proteolytic system based on at least cathepsin D‐, cathepsin B‐, trypsin‐, chymotrypsin‐, leucine aminopeptidase‐, carboxypeptidase A‐, and carboxypeptidase B‐like activities. All endoproteolytic activities were higher in the anterior section of the gut, whereas the exopeptidases were evenly distributed in the anterior and middle sections, and almost no activity was detected in the posterior section. Gelatin‐containing gels confirmed the spatial organization of the proteolytic digestive process. According to this proteolytic profile, the STI (soybean Kunitz trypsin inhibitor) was tested in vivo to establish its potential as a resistance factor against C. sordidus. Newly hatched larvae fed on diets containing 0.2% (w/w) STI experience lower survival rates and display significant reductions in larval growth. Biochemical analysis carried out on guts of larvae reared on STI‐treated diet showed a reduction of trypsin‐like activity compared to that from larvae fed on control diet. This decrease was compensated with an induction of cathepsin B, whereas cathepsin D, chymotrypsin, and leucine aminopeptidase were not affected. These results are discussed as a basis for selecting appropriate inhibitors to obtain transgenic banana and plantain plants with enhanced resistance to this pest.     

Identification and laboratory behavioral test of the alarm pheromone of Acanthocoris sordidus Thunberg (Hemiptera: Coreidae)

The winter cherry bug, Acanthocoris sordidus Thunberg (Hemiptera: Coreidae), widely spread in South Korea, Japan and Taiwan, is becoming an economic pest in these regions. Its elevated pest status in pepper plant, Capsicum annuum, is a trigger for eco‐friendly management tactics. In order to use its pheromone for pest management, the cuticular components of adult A. sordidus were identified and a behavioral bioassay on the functions of the components was conducted. From the whole‐body extracts of male and female A. sordidus, 13 compounds (hexanal, 1‐hexanol, 2‐hexanol, 3‐hexanol, hexanoic acid, hexyl acetate, heptyl acetate, octyl acetate, tetradecane, 2‐butyl‐2‐octenal, hexyl hexanoate and (2α,4α,6β)‐2,4,6‐tripentyl‐1,3,5‐trioxane (hexanal trimer, cis‐ and trans‐forms) were identified. In addition to these, two unidentified compounds, a male‐specific and a male‐rich compound, were also found. Hexanal provoked clear escaping behavior. 1‐Hexanol, hexyl acetate and hexanoic acid evoked weaker behavior than hexanal. We concluded that hexanal worked as an alarm pheromone and could be used as a pushing signal for a control program for A. sordidus.     

Interaction between the predator Xylocoris sordidus and Bacillus thuringiensis bioinsecticides

Xylocoris species (Hemiptera: Anthocoridae) are known to occur in various habitats and attack a diversity of agriculturally important prey. Other groups of organisms, such as strains of Bacillus thuringiensis Berliner (Bt) bacteria, also have been extensively studied and applied as biological control agents. The use of these Bt-bioinsecticides in association with predators may be a good strategy in integrated pest management. This work had the objective to study predator behaviour, predatory capacity, and functional response of fifth-instar nymphs of Xylocoris sordidus (Reuter) to eggs of Plutella xylostella (L.) (Lepidoptera: Plutellidae) and Corcyra cephalonica (Stainton) (Lepidoptera: Pyralidae) treated with one of three commercial Bt-bioinsecticides. The predator presented a type II functional response to untreated P. xylostella eggs (control) and to eggs treated with Agree, whereas the response was type III to P. xylostella eggs treated with Xentari and Dipel. However, on a diet of C. cephalonica eggs the predator displayed a type II response curve on eggs treated with each of the three bioinsecticides, and a type III response on untreated eggs. Bioinsecticides based on B. thuringiensis may be used in association with X. sordidus predators to control lepidopterous pest species.     

Acoustic recording as a non‐invasive method to detect larval infestation of Cosmopolites sordidus

The banana weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae), is a major pest of banana cropping systems, as larvae bore into the corm of banana plants and damage the insertion points of primary roots, leading to plant snapping and toppling. Plant infestation by the banana weevil is assessed only via invasive techniques, such as plant cutting that highlights larval tunnels. We present here a non‐invasive technique based on a bioacoustic sensor with a band‐pass filter to detect larval activity inside banana corm. On the basis of a test under controlled conditions, we observed that the range of larval activity was between 1.4 and 2.6 kHz. Pulses lasted ca. 168 ms and were separated by intervals of 300 ms. The technique enables detection of more than 90% of infested suckers. The use of this technique to understand larval development of banana weevil is discussed.     

Deleterious effects of plant cystatins against the banana weevil Cosmopolites sordidus

The general potential of plant cystatins for the development of insect‐resistant transgenic plants still remains to be established given the natural ability of several insects to compensate for the loss of digestive cysteine protease activities. Here we assessed the potential of cystatins for the development of banana lines resistant to the banana weevil Cosmopolites sordidus, a major pest of banana and plantain in Africa. Protease inhibitory assays were conducted with protein and methylcoumarin (MCA) peptide substrates to measure the inhibitory efficiency of different cystatins in vitro, followed by a diet assay with cystatin‐infiltrated banana stem disks to monitor the impact of two plant cystatins, oryzacystatin I (OC‐I, or OsCYS1) and papaya cystatin (CpCYS1), on the overall growth rate of weevil larvae. As observed earlier for other Coleoptera, banana weevils produce a variety of proteases for dietary protein digestion, including in particular Z‐Phe‐Arg‐MCA‐hydrolyzing (cathepsin L–like) and Z‐Arg‐Arg‐MCA‐hydrolyzing (cathepsin B–like) proteases active in mildly acidic conditions. Both enzyme populations were sensitive to the cysteine protease inhibitor E‐64 and to different plant cystatins including OsCYS1. In line with the broad inhibitory effects of cystatins, OsCYS1 and CpCYS1 caused an important growth delay in young larvae developing for 10 days in cystatin‐infiltrated banana stem disks. These promising results, which illustrate the susceptibility of C. sordidus to plant cystatins, are discussed in the light of recent hypotheses suggesting a key role for cathepsin B–like enzymes as a determinant for resistance or susceptibility to plant cystatins in Coleoptera. © 2009 Wiley Periodicals, Inc.     

Genetic Variability of Beauveria bassiana and a DNA Marker for Environmental Monitoring of a Highly Virulent Isolate Against Cosmopolites sordidus

The banana weevil Cosmopolites sordidus (Germar) is one of a number of pests that attack banana crops. The use of the entomopathogenic fungus Beauveria bassiana as a biological control agent for this pest may contribute towards reducing the application of chemical insecticides on banana crops. In this study, the genetic variability of a collection of Brazilian isolates of B. bassiana was evaluated. Samples were obtained from various geographic regions of Brazil, and from different hosts of the Curculionidae family. Based on the DNA fingerprints generated by RAPD and AFLP, we found that 92 and 88 % of the loci were polymorphic, respectively. The B. bassiana isolates were attributed to two genotypic clusters based on the RAPD data, and to three genotypic clusters, when analyzed with AFLP. The nucleotide sequences of nuclear ribosomal DNA intergenic spacers confirmed that all isolates are in fact B. bassiana. Analysis of molecular variance showed that variability among the isolates was not correlated with geographic origin or hosts. A RAPD-specific marker for isolate CG 1024, which is highly virulent to C. sordidus, was cloned and sequenced. Based on the sequences obtained, specific PCR primers BbasCG1024F (5′-TGC GGC TGA GGA GGA CT-3′) and BbasCG1024R (5′-TGC GGC TGA GTG TAG AAC-3′) were designed for detecting and monitoring this isolate in the field.

Electronic supplementary material

The online version of this article (doi:10.1007/s12088-012-0292-9) contains supplementary material, which is available to authorized users.     

Local and neighboring patch conditions alter sex‐specific movement in banana weevils

Understanding the mechanisms underlying the movements and spread of a species over time and space is a major concern of ecology. Here, we assessed the effects of an individual's sex and the density and sex ratio of conspecifics in the local and neighboring environment on the movement probability of the banana weevil, Cosmopolites sordidus. In a “two patches” experiment, we used radiofrequency identification tags to study the C. sordidus movement response to patch conditions. We showed that local and neighboring densities of conspecifics affect the movement rates of individuals but that the density‐dependent effect can be either positive or negative depending on the relative densities of conspecifics in local and neighboring patches. We demonstrated that sex ratio also influences the movement of C. sordidus, that is, the weevil exhibits nonfixed sex‐biased movement strategies. Sex‐biased movement may be the consequence of intrasexual competition for resources (i.e., oviposition sites) in females and for mates in males. We also detected a high individual variability in the propensity to move. Finally, we discuss the role of demographic stochasticity, sex‐biased movement, and individual heterogeneity in movement on the colonization process.     

Success evaluation of the biological control of Fusarium wilts of cucumber,banana, and tomato since 2000 and future research strategies

The Fusarium wilt caused by Fusarium oxysporum strains is the most devastating disease of cucumber, banana, and tomato. The biological control of this disease has become an attractive alternative to the chemical fungicides and other conventional control methods. In this review, the research trends and biological control efficiencies (BCE) of different microbial strains since 2000 are reviewed in detail, considering types of microbial genera, inoculum application methods, plant growth medium and conditions, inoculum application with amendments, and co-inoculation of different microbial strains and how those affect the BCE of Fusarium wilt. The data evaluation showed that the BCE of biocontrol agents was higher against the Fusarium wilt of cucumber compared to the Fusarium wilts of banana and tomato. Several biocontrol agents mainly Bacillus, Trichoderma, Pseudomonas, nonpathogenic Fusarium, and Penicillium strains were evaluated to control Fusarium wilt, but still this lethal disease could not be controlled completely. We have discussed different reasons of inconsistent results and recommendations for the betterment of BCE in the future. This review provides knowledge of the biotechnology of biological control of Fusarium wilt of cucumber, banana, and tomato in a nut shell that will provide researchers a beginning line to start and to organize and plan research for the future studies.     

Field validation of senesced banana leaf extracts for trapping banana weevils on smallholder banana/plantain farms

Palm wine alcohol extract of senesced banana leaf material, Musa spp., was tested for its efficacy in open field trapping of the banana weevil, Cosmopolites sordidus in Ghana from June to August 2015. Modified pitfall and bottle traps were baited with either individual treatments, that is palm alcohol extract, C. sordidus aggregation pheromone or pseudostem or with combinations of extract plus aggregation pheromone or extract plus pseudostem. The combination of extract plus aggregation pheromone was able to lure more weevils into traps compared with the respective individual lures. There was a 2.1-fold increase in mean catch per week when the palm alcohol extract was used in combination with pheromone compared with using pheromone alone, and a corresponding 2.6-fold increase when the extract was used with pseudostem in traps. There was no statistically significant interaction between the palm alcohol extract (presence or absence) and treatment (pheromone or pseudostem), but the best combination for maximal catches of adult banana weevils was a combination of palm alcohol extract with aggregation pheromone. Management of banana weevils with attractive banana leaf extract has important practical applications in parts of the world where other management options are too expensive or commercial treatments are in short supply, but where leaf material is cheap and readily available for local use by smallholder farmers.     

Interactions between the winter cherry bug <Emphasis Type="Italic">Acanthocoris sordidus</Emphasis> (Hemiptera: Coreidae) and its egg parasitic wasps

Detailed research on the relative strength of the influence of parasitoids on hosts has contributed to the development of biological control techniques. Gryon philippinense (Ashmead) is a major egg parasitoid of the winter cherry bug, Acanthocoris sordidus (Thunberg). However, available data are insufficient to determine which egg parasitoids have the strongest effect on mortality of A. sordidus or why G. philippinense is the major egg parasitoid of A. sordidus. In this study, G. philippinense attained a much higher level of parasitism on A. sordidus eggs compared to four other parasitoid species. Mortality induced by G. philippinense on A. sordidus egg clusters occurred in an all-or-none manner, whereas mortality caused by the four other parasitoids occurred in a random manner. Compared to Ooencyrtus spp., G. philippinense required a significantly shorter time to parasitize an A. sordidus egg and also parasitized significantly more A. sordidus eggs within 24 h. These findings demonstrate that a short handling time allows G. philippinense to be the most significant egg parasitoid of A. sordidus.     

Molecular and morphological diagnoses of five species of Trichogramma: biological control agents of Chrysodeixis chalcites (Lepidoptera: Noctuidae) and Tuta absoluta (Lepidoptera: Gelechiidae) in the Canary Islands

Prospecting for potential natural enemies of the invasive lepidopteran tomato pest Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) and the banana pest Chrysodeixis chalcites (Esper) (Lepidoptera: Noctuidae) on the Canary Islands archipelago, where no Trichogramma species were previously recorded, has led to the discovery of five distinct species. T. achaeae Nagaraja & Nagarkatti, T. bourarachae Pintureau & Babault, T. euproctidis (Girault) and T. evanescens Westwood are relatively widespread species. The fifth is close to T. brassicae Bezdenko, but differs sufficiently in the sequence of the ITS2 region of ribosomal RNA to warrant further investigation as a species probably new to science. Each species is treated in detail in order to facilitate identification in future using molecular and/or morphological characters, or a combination of both. All species are newly recorded for the Canary Islands, and the distribution of each within the islands and elsewhere is provided. Known host records are given within the Canary Islands and elsewhere. The most common species found, T. achaeae, is already being used in biological control programmes against T. absoluta in mainland Spain and field trials are ongoing to evaluate its effectiveness as a biological control agent of C. chalcites in banana crops.