Jorge Toledo's research while affiliated with El Colegio de la Frontera Sur and other places

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Publications (104)


Functional response and mutual interference in the parasitoid Coptera haywardi (Oglobin) (Hymenoptera: Diapriidae) attacking Anastrepha ludens (Loew) (Diptera: Tephritidae) pupae
  • Article

January 2024

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37 Reads

Bulletin of Entomological Research

Gibran Clemente

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Jorge Toledo

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[...]

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Functional response and mutual interference are important attributes of natural enemies that should be analysed in species with the potential to be used as biological control agents in order to increase the predictive power of the possible benefits and/or consequences of their release in the field. Our main objective was to determine the functional response and mutual interference of Coptera haywardi (Oglobin), a pupal parasitoid of economically important fruit flies (Diptera: Tephritidae). The functional response of C. haywardi on A. ludens pupae corresponded to a type II model, with an attack rate of 0.0134 host pupa/h and a handling time of 1.843 h, which reveals a meticulous selection process of pupal hosts. The effect of mutual interference among foraging females was negatively correlated with increased parasitoid density in the experimental arena, showing a gradual decline in attack rate per individual female. The increase in the number of foraging females also had an impact on the number of oviposition scars per pupa and the number of immature parasitoids per dissected pupa, but not on the percentage of adult emergence or the sex ratio. Our results suggest that C. haywardi could act as a complementary parasitoid in the control of fruit fly pupae, since the random distribution of these pupae in the soil would decrease the possibility of aggregation and mutual interference between foraging females.

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Can Entomopathogenic Nematodes and Their Symbiotic Bacteria Suppress Fruit Fly Pests? A Review
  • Literature Review
  • Full-text available

June 2023

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192 Reads

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2 Citations

Microorganisms

Fruit flies (Diptera: Tephritidae) are serious pests that affect fruit production and marketing. Both third instar larvae and pupae are biological stages that persist in the soil until adult emergence. Entomopathogenic nematodes (ENs) are biological control agents that are used to control agricultural pests in greenhouse or field conditions. Several studies have been carried out under laboratory and field conditions showing how ENs can be applied within an area-wide integrated pest management approach to control fruit fly species in orchards and backyard fruit trees. In this review, we analyze how soil physical characteristics and biotic factors affect the performance of these biological control agents. Of the reviewed papers, more than half evaluated the influence of soil texture, humidity, temperature, and other factors on the performance of infective juveniles (IJs). Abiotic factors that significantly influence the performance of IJs are temperature, humidity, and texture. Among the biotic factors that affect IJs are fungi, bacteria, mites, insects, and earthworms. We conclude that ENs have the potential to be applied in the drip area of fruit trees that are infested by fruit flies and contribute to their suppression. This approach, in conjunction with an area-wide pest management approach, may contribute to pest suppression and increase the sustainability of agroecosystems.

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Bulletin of Entomological Research

September 2021

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81 Reads

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2 Citations

Bulletin of Entomological Research

Knowledge on reproductive strategies and host use in insect parasitoids is fundamental for biological control purposes. Superparasitism and multiparasitism, oviposition in a previously parasitized host by a female of the same or different species, respectively, may impact pest management decisions. Our objective was to determine the occurrence of superparasitism and multiparasitism in three species of native larval−pupal solitary endoparasitoids that attack Anastrepha Shiner species (Diptera: Tephritidae) in the Neotropical region, and the possible effect on offspring fitness parameters. Doryctobracon crawfordi (Viereck), Utetes anastrephae (Viereck), and Opius hirtus (Fischer) occur in sympatry in Mexico, and are currently under consideration for use as biocontrol agents. Experiments were conducted under laboratory conditions with females acting alone (self-superparasitism), females in groups of the same species (conspecific superparasitism), and females in mixed groups (multiparasitism). Our results showed that self-superparasitism is an uncommon strategy in the three native species and is rare under conditions of intraspecific competition. In the case of multiparasitism, a higher number of immature stages of U. anastrephae was observed, compared to those of D. craw-fordi and O. hirtus. However, it is not clear yet if this was due to some adult female trait or to the competitive ability of the larvae. We conclude that most females of the native species studied appeared to avoid superparasitism, specifically when acting alone, suggesting a high discrimination ability, which is probably a result of a close relationship and evolutionary history with Anastrepha hosts.


Sexual performance and survival of males of Ceratitis capitata VIENNA 8 (Diptera: Tephritidae) inoculated with a commercial formulation of Beauveria bassiana

September 2021

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56 Reads

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7 Citations

Journal of Applied Entomology

The Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), is a polyphagous pest that feeds upon more than 300 host plants, including fruits and vegetables. To eradicate this pest, the Mexican program (Programa Moscamed) targeting fruit flies applied a novel approach that works with the sterile insect technique (SIT) by inoculating sterile flies with fungal spores of a commercial formulation of Beauveria bassiana (Balsamo) Vuillemin. Dissemination occurs through contact with the sterile insect with wild populations. However, the fungus is known to reduce the homeostatic condition of the vector (sexual and aggressive interactions) to the point that it affects physical contact with the receptor. The objective was to evaluate the effect of B. bassiana on the sexual performance and survival of sterile males of the C. capitata strain VIENNA 8. Mating competition, induction of sterility, production of the sexual pheromone and survival were compared between inoculated and non‐inoculated sterile males. The parameters evaluated were fundamental to evaluate the success in the SIT. The results of the study indicated that the inoculated males with B. bassiana showed a gradual decrease in sexual performance (mating, induction of sterility and production of the sexual pheromone) and survival after treatment. We conclude that for SIT release programs, the effectiveness of targeted males is up to 5 days post‐inoculation. The implications of this biological control method in SIT are discussed.


Coptera haywardi females discriminate puparia of Anastrepha obliqua treated with Beauveria bassiana

August 2021

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37 Reads

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2 Citations

Entomologia Experimentalis et Applicata

The capacity of a parasitoid to discriminate hosts can favor the survival of its progeny as well as improve its efficacy as a biocontrol agent when it is used with another natural enemy, as this may result in greater control of the pest. Our aim was to characterize the discrimination ability of Coptera haywardi (Oglobin) (Hymenoptera: Diapriidae) females with respect to puparia of Anastrepha obliqua (Macquart) (Diptera: Tephritidae) treated with the fungus Beauveria bassiana (Balsamo) Vuillemin (Hypocreales: Cordycipitaceae), under three conditions: (1) no choice, separately exposing A. obliqua puparia treated 0, 24, 48, or 72 h prior to exposure to the parasitoid and without application of the fungus (absolute control); (2) with the possibility of choosing between untreated and treated puparia with the same times after fungus application; and (3) multiple choice, where parasitoids could select among puparia treated at different times. Observations were made to determine the discrimination behavior of the wasps as well the number of ovipositions by each female parasitoid; 14 observations were made. Coptera haywardi exhibited different levels of discrimination depending on the test. In the no‐choice test, discrimination was not observed; in the two‐choice test, females significantly discriminated the puparia treated 0, 24, and 72 h prior to exposure; and in the multiple‐choice test, females preferred the untreated puparia – behavior that was corroborated in the direct observations. Oviposition time ranged from 9 to 86 min and differences in average time among treatments were not significant. We conclude that the discrimination ability of C. haywardi allows the simultaneous use of B. bassiana, as females prefer healthy, untreated puparia without interfering with the fungus.


Efficacy of food-based attractants for monitoring Drosophila suzukii (Diptera: Drosophilidae) in berry crops

August 2021

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91 Reads

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9 Citations

Crop Protection

Spotted-Wing Drosophila (SWD), Drosophila suzukii Matsumura is an invasive fruit fly pest of soft-skinned fruits that causes serious economic losses in the berry growing areas of central Mexico. Effective attractants are necessary to detect its presence, to monitor populations where established, and to explore new strategies for pest control. The capture of D. suzukii in four food-based attractants was compared with apple cider vinegar (ACV) as the reference attractant in blackberry, raspberry, and blueberry crops. An active yeast-based lure, Fly Buster Powder®, resulted the most effective attractant capturing SWD flies in blackberry and blueberry. However, this attractant was similar to SuzukiiTrap® Max Captures, ACV and Pherocon® SWD, but less effective than a two-component attractant (2C trap) in raspberry. The specificity of attractants was variable among crops and experiments but Fly Buster Powder® tends to be highly selective in the capture of SWD with up to 70% of D. suzukii from all drosophilids captured. Fly Buster Powder® and 2C trap attractants were more effective trapping D. suzukii when aged for 7 days than when aged for 1 or 15 days. The specificity of both yeast-based attractants was significantly reduced when aged for 15 days than when aged for 1 or 7 days.


Sex separation of Aedes spp. mosquitoes for sterile insect technique application: a review

July 2021

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145 Reads

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3 Citations

Entomologia Experimentalis et Applicata

Separation of the sexes is necessary for the application of the sterile insect technique (SIT) in mosquitoes due to the hematophagous habits and disease vector activity of the females. In this review we analyze the history, current status, and future perspectives for the development of genetic sexing strains (GSS) of Aedes mosquitoes (Diptera: Culicidae). Various genetic control methods for mosquitoes are reviewed, as are their need for sex-separation methods. We focus on areas of opportunity where GSS developed with classical genetic methods can be used. Regulatory restrictions and social acceptance of various control methods are analyzed. We conclude that the development of GSS by classical methods represents the most viable option for separation of the sexes and the application of large-scale SIT programs within an area-wide integrated vector management (AW-IVM) approach.


Figure 1. Weekly field monitoring of Anastrepha fraterculus populations in commercial apple orchards with McPhail traps baited with fruit juice or hydrolysed proteins.
Figure 1. Stable flies on leg of steer (left, photographer David Cook) and damage from stable fly bites in Costa Rica (right, photographer Jose Solórzano).
Figure 1. Suggested research and implementation framework toward sustainable area-wide integrated tick management to prevent tick-borne diseases in the context of global change and the One Health approach (*adapted from Pérez de León et al. 2012).
Figure 1. Map top left: Distribution of Glossina palpalis gambiensis in West Africa and location of the Niayes area around Dakar in Senegal. The red area represents suitable habitats predicted from a Maxent model. Map right: The project area indicating the suitability of the vegetation for harbouring G. p. gambiensis after a phytosociological study, and the "wet areas" as obtained from a supervised classification (modified after Bouyer et al. 2010, 2015b).
Figure 2. Sticky traps used for stable fly control in Costa Rica.

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Area-Wide Integrated Pest Management: Development and Field Application

February 2021

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479 Reads

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19 Citations

The Sterile Insect Technique (SIT) has been successfully used for the control of fruit flies in a number of places in the world. One requirement for its successful application is that wild populations should be at low densities to achieve effective sterile to wild fly overflooding ratios. This has been an important reason that has limited its integration in fruit fly management in tropical fruit growing areas, where climate conditions and the availability of hosts all year-round results in high population densities. Here we report the results of a project where SIT integration into fruit fly management was evaluated under the tropical conditions of the mango growing area in the Soconusco region of Chiapas, Mexico. The basis for the area-wide integrated pest management (AW-IPM) approach was the knowledge of the population dynamics of the pest fruit flies in the region and of the fruit phenology. The main commercial mango growing areas are in the lowlands, where fruit fly populations are very low outside of the mango production season. Population densities are higher in the midlands and highlands, where alternate hosts are common in backyards and as part of the natural vegetation. We call these refuge areas, and the AW-IPM approach aimed at establishing a biological barrier with releases of parasitoids and sterile male fruit flies to suppress the fruit fly populations and prevent or minimize the dispersal of wild flies from the refuge areas to the mango orchards. In 2014, after two years of releases, fruit fly population densities were suppressed more than 70% in the release area and 65% in the entire area, including the lowlands with the mango orchards. With the support of fruit growers, state and federal governments, this project was continued and established as an operational AW-IPM programme. In 2016, after 4 years of programme implementation, the detection of wild flies was significantly reduced, and the number of batches of fruit that were rejected at the packing houses due to the detection of infested fruits was the lowest in the past 12 years, since the recording of these data was initiated. These indicators declined even further in 2017. The results obtained demonstrate that AW-IPM integrating the SIT can be applied successfully against fruit flies under tropical conditions with naturally high pest densities, providing there is adequate knowledge on the population dynamics of the fruit fly species present in the region.



Effects of Purpureocillium lilacinum (Hypocreales: Ophiocordycipitaceae) on food consumption and sexual behavior of Anastrepha ludens (Diptera: Tephritidae) fruit flies

January 2021

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71 Reads

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6 Citations

International Journal of Tropical Insect Science

Purpureocillium lilacinum is an entomopathogenic fungus. An experiment was conducted to see the sublethal effects of P. lilacinum on Anastrepha ludens adults. The infection of P. lilacinum reduced daily food consumption per fly ranging from 4.25 ± 0.28 to 6.44 ± 0.27 µl for infected flies, and from 6.30 ± 0.28 to 7.81 ± 0.22 µl for non-infected control flies. The age of treatment in males showed a significant effect on their ability to mate (χ2 = 5.32, P < 0.02). Early stage infection (4 days-old), reduced the male mating propensity significantly (10 ± 0.46 treated to 15.4 ± 0.26 untreated, F 8, 5.94 = 5.592, P < 0.01), compared to later stage (8 days-old) insignificant effect. No effect of fungal infection on an ability of male to inseminate the females was noticed, as fertility of the females mated with infected males was not declined. An inoculated single female (mixture of talc and P. lilacinum) was able to transmit conidia to four groups of 10 males within four days. Males exposed to females on the first day acquired in average 1.7 ⋅ 106, on the second day 1.7 ⋅ 105, on the third day 7.3 × 104 and the fourth day 3.5 ⋅ 104 conidia/ male; which resulted 67.5, 55.0, 20.0, and 7.5 % male mortality, respectively. Our study demonstrated that horizontal transmission through copulation could be used to suppress A. ludens populations.


Citations (83)


... Successful use requires that the ecology of the target is matched to the activity of infective juveniles; as the target pests are protected from environmental extremes, applications are timed to coincide with susceptible host stages and favourable weather conditions and nematodes are able to rapidly locate and infect hosts [71]. In addition to performance, factors including cost, availability, compatibility within integrated strategies and alternative options for organic growers will ultimately determine the extent to which nematodes are used against Dipteran insect pests [72,[78][79][80]. To make entomopathogenic nematodes more successful, realistic strategies through genetic engineering [81], IPM programs, and new delivery systems and/or training programs to overcome their inherent cost, formulation instability, and limited field efficacy toward the Dipteran pests are needed [82,83]. ...

Reference:

Management of Dipteran Pests Through Entomopathogenic Nematodes
Can Entomopathogenic Nematodes and Their Symbiotic Bacteria Suppress Fruit Fly Pests? A Review

Microorganisms

... The integrated management of the fruit fly pest caused by Anastrepha has been implemented since 1992 through the National Program and the National Campaign Against Fruit Flies (NCFF), under an international agreement between Mexico, Guatemala, and the United States (Montoya et al., 2010). The program is based on the implementation of phytosanitary measures to control, suppress, and eradicate fruit flies. ...

MOSCAS DE LA FRUTA: FUNDAMENTOS Y PROCEDIMIENTOS PARA SU MANEJO

... Inoculated males probably started being sick during the three days of observation (Zimmermann 2007), then becoming less and less competitive until death (Armsworth et al. 2006;Thaochan and Ngampongsai. 2018;Ramírez y Ramírez et al. 2022). As a result, the males that were both sterile and inoculated had the lowest mating success. ...

Sexual performance and survival of males of Ceratitis capitata VIENNA 8 (Diptera: Tephritidae) inoculated with a commercial formulation of Beauveria bassiana
  • Citing Article
  • September 2021

Journal of Applied Entomology

... The commercial lures evaluated in this study showed different performance in catching D. suzukii. FLYBUSTER ® Powder was developed to attract Musca domestica L. (Diptera: Muscidae); however, Toledo-Hernández et al. (2021) reported it to be highly attractive to D. suzukii, which contrasts with our results. Z-Kinol ® is a product developed from studies conducted by Cha et al. (2017), with the compounds contained in polyethylene tubes to permit a controlled emission, making them independent of the drowning solution (soapy water). ...

Efficacy of food-based attractants for monitoring Drosophila suzukii (Diptera: Drosophilidae) in berry crops
  • Citing Article
  • August 2021

Crop Protection

... It has been documented that C. haywardi develops successfully in pupae of various species of the genus Anastrepha, such as A. serpentina, A. striata, and A. obliqua (García and Montilla, 2001), and that it can develop in wild and irradiated strains of Ceratitis capitata pupae (Wied) (Sivinski et al., 1998;Núñez-Campero et al., 2020). In addition, it has been suggested that C. haywardi can be used together with other biological control agents against both Anastrepha and Ceratitis flies due to its great discriminatory capacity (Cancino et al., 2014;Van Nieuwenhove et al., 2016;Martínez-Barrera et al., 2021). However, the use of C. haywardi (or any other species of parasitoid) in augmentative biological control programmes must be carefully planned and analysed in advance to avoid failure and/or harmful effects of their interaction (Montoya et al., 2019;Rezaei et al., 2019). ...

Coptera haywardi females discriminate puparia of Anastrepha obliqua treated with Beauveria bassiana
  • Citing Article
  • August 2021

Entomologia Experimentalis et Applicata

... However, these have only been developed in Aedes aegypti and require sorting at the fragile adult stage which is not ideal, slow, and difficult to scale. Alternatively, selectable markers have been genetically linked to sex chromosomes in Anopheles [33][34][35][36][37], or to sex-determining loci in Aedes [38][39][40]. However, genetic linkage is often broken by meiotic recombination, or translocations, making these strains less stable when scaled [17,41]. ...

Sex separation of Aedes spp. mosquitoes for sterile insect technique application: a review

Entomologia Experimentalis et Applicata

... Enterobacter sp. in treatment OB (XPS) and OB (EPS) with 6.46 ± 4.95% and 7.53 ± 4.10%, which increased by 5.28% and 6.35% as compared to treatment OB (only) with a relative abundance of 1.18 ± 0.22%. The symbiotic relationships between insects and Enterobacter species may be advantageous to the host as it has varied capacities to catalyze nitrogen fixation, hydrolyze and ferment carbohydrates, and synthesize vitamins and pheromones for the host (Hendrichs et al., 2021). Enterobacter sp. ...

Area-Wide Integrated Pest Management: Development and Field Application

... Collaboration and communication must remain an overall component of PROCEM. As an example, the successful application of SIT in combination with other eco-friendly control tools, such as biological control (Cladera et al. 2008;Liedo et al. 2021) and/or mass trapping, is an integrated strategy that, to be implemented on a large scale, requires continuous cooperation and consensus within the national PROCEM. ...

Area-Wide Management of Fruit Flies in a Tropical Mango Growing Area Integrating the Sterile Insect Technique and Biological Control: From a Research to an Operational Programme

... The genus Purpureocillium (Hypocreales: Ophiocordycipitaceae) consists of fungal species having pathogenicity against some dipteran pests, such as, Aedes aegypti (Luz et al. 2007), Musca domestica (Fernandes et al. 2013) and Anastrepha ludens (Toledo-Hernández et al. 2021). Among them, P. lilacinum has shown promising results for use as an effective biocontrol agent against Culicidae (Sani et al. 2017a(Sani et al. , 2017bHamama et al. 2021). ...

Effects of Purpureocillium lilacinum (Hypocreales: Ophiocordycipitaceae) on food consumption and sexual behavior of Anastrepha ludens (Diptera: Tephritidae) fruit flies
  • Citing Article
  • January 2021

International Journal of Tropical Insect Science

... There is evidence that high abundance of some Providencia species can have adverse effects on Ceratitis capitata (Wiedemann) [24]. However, it has been observed that the addition of P. rettgeri to the artificial diet of massreared A. obliqua can improve sterile male sexual competitiveness [25]. Our results confirmed the presence of the genus Wolbachia (Rickettsiaceae) in the midguts of mass-reared, irradiated, non-irradiated, and wild A. obliqua males. ...

Attractiveness and Sexual Competitiveness of Anastrepha obliqua Males (Diptera: Tephritidae) Fed on a Diet Enriched With Providencia rettgeri
Frontiers in Microbiology

Frontiers in Microbiology