Combining Biological Control and Sterile Insect Technique to Enhance Invasive Pest Species Management

A special issue of Insects (ISSN 2075-4450). This special issue belongs to the section "Insect Pest and Vector Management".

Deadline for manuscript submissions: closed (30 June 2023) | Viewed by 13887

Special Issue Editors


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Guest Editor
Biotechnology and Biological Control Agency (BBCA), 00123 Rome, Italy
Interests: sterile insect technique; insect behavior; monitoring; bio-pesticides; integrated pest management; biological control of weeds; integrated weed management
Special Issues, Collections and Topics in MDPI journals

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Guest Editor
Center for Agriculture, Food Environment (C3A), University of Trento, 38010 San Michele all’Adige, Italy
Interests: semiochemicals; insect chemical ecology; mating disruption; biological control; IPM
Special Issues, Collections and Topics in MDPI journals

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Guest Editor
Plant & Food Research, Auckland, New Zealand
Interests: sterile insect technique; chemical ecology; population modelling; vibrational communication

Special Issue Information

Dear Colleagues,

Ongoing climate change and globalization-related phenomena are increasing the impact of harmful insects, both native and invasive alien, on multiple aspects of the environment and economy, such as biodiversity, human health, and agriculture. The development of biotechnologies for the sustainable, long-lasting, and large-scale control of such organisms is, therefore, crucial.

Area-wide integrated pest management (AW-IPM) actions involve the integration of background knowledge of the biology of the target pest, its distribution in the selected area to manage and the synergistic application of several control strategies, such as Sterile Insect Technique (SIT), biological control, and other pest suppression methods.  Among the control methods, SIT, and Biological Control have a peculiar importance, for their least toxic effects on the environment.

This Special Issue of Insects will include original research articles and reviews that are addressed to highlight the complementary relationships between sterile insect technique and biological control to improve the suppression or even the eradication of a given target pest species. Special emphasis must be given to the combination of these two strategies, looking for possible integrations in terms of monitoring, control, dispersal, and direct and indirect synergisms.

Dr. Massimo Cristofaro
Dr. Gianfranco Anfora
Dr. Lloyd Stringer
Guest Editors

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Keywords

  • sampling 
  • area-wide pest management 
  • biological control 
  • insect pests 
  • monitoring 
  • parasitoids 
  • predators 
  • sterile insect technique

Published Papers (8 papers)

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Research

13 pages, 1560 KiB  
Article
Effect of the Sterile Insect Technique and Augmentative Parasitoid Releases in a Fruit Fly Suppression Program in Mango-Producing Areas of Southeast Mexico
by Jorge Cancino, Pablo Montoya, Fredy Orlando Gálvez, Cesar Gálvez and Pablo Liedo
Insects 2023, 14(9), 719; https://doi.org/10.3390/insects14090719 - 22 Aug 2023
Viewed by 1367
Abstract
The Sterile Insect Technique (SIT), by means of sterile male releases of Anastrepha ludens (Loew), coupled with Augmentative Biological Control (ABC), by releasing the parasitoid Diachasmimorpha longicaudata (Ashmead), was evaluated in a commercial mango production area for one year. The obtained results were [...] Read more.
The Sterile Insect Technique (SIT), by means of sterile male releases of Anastrepha ludens (Loew), coupled with Augmentative Biological Control (ABC), by releasing the parasitoid Diachasmimorpha longicaudata (Ashmead), was evaluated in a commercial mango production area for one year. The obtained results were compared with mean fruit fly population values from two previous years without the combined use of both techniques. The treatments were: SIT + ABC, SIT, ABC, and Control, and each treatment was established in blocks of 5000 Ha separated by distances of 5–10 km. The evaluations were carried out through fruit sampling to assess percent parasitism and trapping of adult flies to obtain Flies per Trap per Day (FTD) values. The mean percentage of parasitism increased from 0.59% in the control treatment to 19.38% in the block with ABC. The FTD values decreased from ~0.129 and ~0.012 in the control block to 0.0021 in the block with SIT and ABC, representing a 98% suppression. The difference between the two periods in the control block was not significant. We conclude that the integration of both techniques resulted in an additive suppression of the pest population, supporting the use of both control techniques in an area-wide pest management context. Full article
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17 pages, 2127 KiB  
Article
Combining Irradiation and Biological Control against Brown Marmorated Stink Bug: Are Sterile Eggs a Suitable Substrate for the Egg Parasitoid Trissolcus japonicus?
by Gerardo Roselli, Gianfranco Anfora, Raffaele Sasso, Livia Zapponi, Sergio Musmeci, Alessia Cemmi, David Maxwell Suckling, Kim Alan Hoelmer, Claudio Ioriatti and Massimo Cristofaro
Insects 2023, 14(7), 654; https://doi.org/10.3390/insects14070654 - 22 Jul 2023
Viewed by 1160
Abstract
The brown marmorated stink bug (BMSB), Halyomorpha halys, is a phytophagous invasive pest native to south-eastern Asia, and it is now distributed worldwide. This species is considered to be one of the most damaging insect pests in North America and in Europe. [...] Read more.
The brown marmorated stink bug (BMSB), Halyomorpha halys, is a phytophagous invasive pest native to south-eastern Asia, and it is now distributed worldwide. This species is considered to be one of the most damaging insect pests in North America and in Europe. In agriculture, the predominant approach to managing BMSB is based on the use of insecticides, specifically pyrethroids and neonicotinoids. Unfortunately, the biology of the species and its facility to develop mechanisms of resistance to available pesticides has induced farmers and scientists to develop different, least-toxic, and more effective strategies of control. In a territorial area-wide approach, the use of a classical biological control program in combination with other least-toxic strategies has been given prominent consideration. Following exploratory surveys in the native range, attention has focused on Trissolcus japonicus, a small scelionid egg parasitoid wasp that is able to oviposit and complete its larval development in a single egg of H. halys. A common method for detecting egg parasitoids in the native range involves the placement of so-called ‘sentinel’ egg masses of the pest in the environment for a short period, which are then returned to the laboratory to determine if any of them are parasitized. Outside of the area of origin, the use of fertile sentinel eggs of the alien species may lead to the further release of the pest species; an alternative is to use sterile sentinel eggs to record the presence of new indigenous egg parasitoids or to detect the dispersal of alien species (in this case, T. japonicus) released in a new environment to control the target insect pest species. This study evaluated the performance of three types of sterile sentinel eggs as a suitable substrate for the oviposition and larval development of the egg parasitoid T. japonicus in a context of combining classical biological control with a Sterile Insect Technique (SIT) approach. Full article
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13 pages, 3046 KiB  
Article
The Effect of the Sterile Insect Technique on Vibrational Communication: The Case of Bagrada hilaris (Hemiptera: Pentatomidae)
by Chiara Peccerillo, Chiara Elvira Mainardi, Rachele Nieri, Jalal Melhem Fouani, Alessia Cemmi, Massimo Cristofaro, Gianfranco Anfora and Valerio Mazzoni
Insects 2023, 14(4), 353; https://doi.org/10.3390/insects14040353 - 2 Apr 2023
Cited by 2 | Viewed by 1545
Abstract
The painted bug, Bagrada hilaris, is an agricultural pest in its original areas (Africa, South Asia, and the Middle East), and it has recently been recorded as an invasive species in southwestern part of the US, Chile, Mexico, and two islands in [...] Read more.
The painted bug, Bagrada hilaris, is an agricultural pest in its original areas (Africa, South Asia, and the Middle East), and it has recently been recorded as an invasive species in southwestern part of the US, Chile, Mexico, and two islands in the Mediterranean basin. Its polyphagous diet causes severe damage to economically important crops. The control of this pest is primarily achieved by means of synthetic pesticides, which are often expensive, ineffective, and harmful to the ecosystem. Recent physiological bioassays to assess its potential control through the sterile insect technique demonstrated that mating between untreated females and males irradiated at doses of 64 and 100 Gy, respectively, resulted in 90% and 100% sterility of the eggs produced by the females. In this study, the mating abilities of virgin males irradiated at 60 and 100 Gy with virgin females were measured through a study of short-range courtship mediated by vibrational communication. The results indicate that males irradiated at 100 Gy emit signals with lower peak frequencies, mate significantly less than unirradiated males do, and do not surpass the early stages of courtship. Conversely, males irradiated at 60 Gy present vibrational signal frequencies that are comparable to those of the control and successfully mated males. Our findings suggest that B. hilaris individuals irradiated at 60 Gy are good candidates for the control of this species, given that they retain sexual competitiveness regardless of their sterility, through an area-wide program that incorporates the sterile insect technique. Full article
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13 pages, 972 KiB  
Article
Additive Effect of Releasing Sterile Insects Plus Biocontrol Agents against Fruit Fly Pests (Diptera: Tephritidae) under Confined Conditions
by Pablo Montoya, Erick Flores-Sarmiento, Patricia López, Amanda Ayala and Jorge Cancino
Insects 2023, 14(4), 337; https://doi.org/10.3390/insects14040337 - 30 Mar 2023
Cited by 1 | Viewed by 1296
Abstract
Pest control models integrating the use of the sterile insect technique (SIT) and augmentative biological control (ABC) have postulated that it is possible to obtain a synergistic effect from the joint use of these technologies. This synergistic effect is attributed to the simultaneous [...] Read more.
Pest control models integrating the use of the sterile insect technique (SIT) and augmentative biological control (ABC) have postulated that it is possible to obtain a synergistic effect from the joint use of these technologies. This synergistic effect is attributed to the simultaneous attack on two different biological stages of the pest (immature and adult flies), which would produce higher suppression on the pest populations. Here we evaluated the effect of the joint application of sterile males of A. ludens of the genetic sexing strain Tap-7 along with two parasitoid species at the field cage level. The parasitoids D. longicaudata and C. haywardi were used separately to determine their effect on the suppression of the fly populations. Our results showed that egg hatching percentage was different between treatments, with the highest percentage in the control treatment and a gradual reduction in the treatments with only parasitoids or only sterile males. The greatest induction of sterility (i.e., the lowest egg hatching percentage) occurred with the joint use of ABC and SIT, demonstrating that the earlier parasitism caused by each parasitoid species was important reaching high levels of sterility. Gross fertility rate decreased up to 15 and 6 times when sterile flies were combined with D. longicaudata and C. haywardi, respectively. The higher parasitism by D. longicaudata was determinant in the decrease of this parameter and had a stronger effect when combined with the SIT. We conclude that the joint use of ABC and SIT on the A. ludens population had a direct additive effect, but a synergistic effect was observed in the parameters of population dynamics throughout the periodic releases of both types of insects. This effect can be of crucial importance in the suppression or eradication of fruit fly populations, with the added advantage of the low ecological impact that characterizes both techniques. Full article
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15 pages, 869 KiB  
Article
Paternity Analyses for the Planning of SIT Projects against the Red Palm Weevil
by Silvia Belvedere, Silvia Arnone, Massimo Cristofaro, Alessandra La Marca and Alessio De Biase
Insects 2023, 14(4), 326; https://doi.org/10.3390/insects14040326 - 28 Mar 2023
Cited by 2 | Viewed by 1023
Abstract
The red palm weevil Rhynchophorus ferrugineus is an invasive pest from southeastern Asia and Melanesia that has spread widely across the Middle East and the Mediterranean Basin over the last 30 years. Its endophagous larvae cause huge amounts of damage to several palm [...] Read more.
The red palm weevil Rhynchophorus ferrugineus is an invasive pest from southeastern Asia and Melanesia that has spread widely across the Middle East and the Mediterranean Basin over the last 30 years. Its endophagous larvae cause huge amounts of damage to several palm tree species from the Arecaceae family. Many of these palms are economically important for agricultural and ornamental purposes. Therefore, a lot of attention has recently been focused on studying this species with the aim of identifying sustainable and effective eradication strategies. Sterile insect techniques are biological control strategies that are currently being investigated for their potential to eradicate this pest in selected invasion areas. Mating system features (e.g., polyandry and related features) can affect the success and suitability of these approaches. The main goal of this research was to assess the performance of a previously developed microsatellite panel in terms of the paternity assignment of progeny from laboratory mating experiments. Using a simulation approach, we evaluated the reliability of the microsatellite markers in the paternity tests both in complex laboratory experiment scenarios and on the progeny of wild-caught gravid females to help future studies on the RPW mating system. As a case study of the simulation results, we performed two double-mating experiments, genotyped the progeny and estimated the P2 values to compare to the expected progeny genotypes according to the crossing scheme of each experiment. The results of our simulations on laboratory experiments showed that it was possible to carry out paternity assignments for all progeny with reliable statistical confidence using our 13 microsatellites set. On the contrary the low genetic variability measured in red palm weevil populations in invaded areas made the resolution power of our loci too low to carry out paternity analyses on natural populations. Results of laboratory crossing were completely congruent with the expectations from the Mendelian laws. Full article
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15 pages, 1896 KiB  
Article
Suitability of Raycell MK2 Blood X-ray Irradiator for the Use in the Sterile Insect Technique: Dose Response in Fruit Flies, Tsetse Flies and Mosquitoes
by Hanano Yamada, Bénéwendé Aristide Kaboré, Nanwintoum Séverin Bimbilé Somda, Nonhlanhla L. Ntoyi, Chantel Janet de Beer, Jérémy Bouyer, Carlos Caceres, Robert L. Mach and Yeudiel Gómez-Simuta
Insects 2023, 14(1), 92; https://doi.org/10.3390/insects14010092 - 15 Jan 2023
Cited by 5 | Viewed by 2744
Abstract
The sterile insect technique (SIT) is based on the inundatory field release of a target pest following their reproductive sterilization via exposure to radiation. Until recently, gamma irradiation from isotopic sources has been the most widely used in SIT programs. As isotopic sources [...] Read more.
The sterile insect technique (SIT) is based on the inundatory field release of a target pest following their reproductive sterilization via exposure to radiation. Until recently, gamma irradiation from isotopic sources has been the most widely used in SIT programs. As isotopic sources are becoming increasingly expensive, especially for small programs, and regulations surrounding their procurement and shipment increasingly strict, irradiation capacity is one of the limiting factors in smaller or newly developing SIT projects. For this reason, the possibility of using X-ray irradiators has been evaluated in the recent decade. The availability of “off-the-shelf” blood X-ray irradiators that meet the technical requirements for insect irradiation can provide irradiation capacity for those SIT projects in which the acquisition of gamma ray irradiators is not feasible. Following the recent technical characterization of a Raycell MK2 X-ray blood irradiator, it was found in this study, that MK2 instruments were suitable for the sterilization of fruit flies, tsetse flies and mosquitoes, inducing comparable, even slightly higher, sterility levels compared to those achieved by gamma ray irradiation. This, together with its estimated processing efficiency, shows that MK2 irradiators are suitable for small- to mid-sized SIT programs. Full article
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15 pages, 355 KiB  
Article
Aedes albopictus Sterile Male Production: Influence of Strains, Larval Diet and Mechanical Sexing Tools
by Marco Malfacini, Arianna Puggioli, Fabrizio Balestrino, Marco Carrieri, Maria Luisa Dindo and Romeo Bellini
Insects 2022, 13(10), 899; https://doi.org/10.3390/insects13100899 - 3 Oct 2022
Cited by 3 | Viewed by 1612
Abstract
The sterile insect technique (SIT) is a biologically based method of pest control, which relies on the mass production, sterilization, and release of sterile males of the target species. Since females can transmit viruses, it is important to develop a mass rearing system [...] Read more.
The sterile insect technique (SIT) is a biologically based method of pest control, which relies on the mass production, sterilization, and release of sterile males of the target species. Since females can transmit viruses, it is important to develop a mass rearing system to produce a large number of males with a low presence of females. We evaluated the effects of different strains, larval diets and sexing tools on male productivity and residual female presence for the application of SIT against Aedes albopictus. Strains coming from Italy, Germany, Greece, and Montenegro, with different levels of colonization, were reared with three larval diets: IAEA-BY, BLP-B and SLP-BY. Developed pupae were sexed using two different mechanical methods: sieve or Fay-Morlan separator. The results proved that adoption of the Fay-Morlan separator increased the productivity and limited the female presence. The IAEA-BY diet showed the lowest female contamination. Strains with a high number of breeding generations showed a decreased productivity and an increased female presence. Increased female presence was found only in extensively reared strains and only when the sorting operation was conducted with sieves. We hypothesize that extensive colonization may determine a size reduction which limits the sexing tool efficiency itself. Full article
17 pages, 1654 KiB  
Article
Effects of Gamma Irradiation on the Fecundity, Fertility, and Longevity of the Invasive Stink Bug Pest Bagrada hilaris (Burmeister) (Hemiptera: Pentatomidae)
by Massimo Cristofaro, René F. H. Sforza, Gerardo Roselli, Alessandra Paolini, Alessia Cemmi, Sergio Musmeci, Gianfranco Anfora, Valerio Mazzoni and Michael Grodowitz
Insects 2022, 13(9), 787; https://doi.org/10.3390/insects13090787 - 30 Aug 2022
Cited by 9 | Viewed by 2032
Abstract
The bagrada bug, Bagrada hilaris, is an invasive insect pest in the family Brassicaceae that causes economically important damage to crops. It was originally present in Asia, the Middle East, and Africa, and was reported as invasive in the southwestern part of [...] Read more.
The bagrada bug, Bagrada hilaris, is an invasive insect pest in the family Brassicaceae that causes economically important damage to crops. It was originally present in Asia, the Middle East, and Africa, and was reported as invasive in the southwestern part of the US, in Chile, and on a few islands in the Mediterranean Basin. In its native range, B. hilaris is controlled by several egg parasitoid species that are under consideration as potential biological control agents. This research evaluated the impact of gamma irradiation on life history parameters, e.g., the fecundity, fertility, and longevity of B. hilaris, as a critical step towards assessing the feasibility of using the sterile insect technique against this recent invasive pest. Newly emerged adults of a laboratory colony originally collected from the island of Pantelleria (Italy) were gamma-irradiated. Life history parameters were evaluated at nine different doses, ranging from 16 Gy to 140 Gy. The minimal dose to approach full sterility was 100 Gy. Irradiation up to a maximum of 140 Gy apparently did not negatively impact the longevity of the adults. Even if both genders are sensitive to irradiation, the decline in fecundity for irradiated females could be exploited to release irradiated males safely to apply the SIT in combination with classical biological control. The data presented here allow us to consider, for the first time, the irradiation of bagrada adults as a suitable and feasible technique that could contribute to guaranteeing a safe approach to control this important pest species in agro-ecosystems. More research is warranted on the competitive fitness of irradiated males to better understand mating behavior as well as elucidate the possible mechanisms of sperm selection by polyandric B. hilaris females. Full article
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