Marc J.B. Vreysen

Glossina austeni (Diptera: Glossinidae) Eradicated on the Island of Unguja, Zanzibar, Using the Sterile Insect Technique

Abstract An area-wide integrated tsetse eradication project was initiated in Zanzibar in 1994 by the International Atomic Energy Agency and the governments of Tanzania and Zanzibar, to eradicate Glossina austeni Newstead from Unguja Island (Zanzibar) using the sterile insect technique. Suppression of the tsetse population on Unguja was initiated in 1988 by applying residual pyrethroids as a pour-on formulation to livestock and by the deployment of insecticide impregnated screens in some of the forested areas. This was followed by sequential releases of gamma-sterilized male flies by light aircraft. The flies, packaged in carton release containers, were dispersed twice a week along specific flight lines separated by a distance of 1–2 km. More than 8.5 million sterile male flies were released by air from August 1994 to December 1997. A sterile to indigenous male ratio of >50:1 was obtained in mid-1995 and it increased to >100:1 by the end of 1995. As a consequence the proportion of sampled young females (1–2 ovulations), with an egg in utero in embryonic arrest or an uterus empty as a result of expulsion of a dead embryo, increased from <25% in the 1st quarter to >70% in the last quarter of 1995. In addition, the age structure of the female population became significantly distorted in favor of old flies (≥4 ovulations) by the end of 1995. The apparent density of the indigenous fly population declined rapidly in the last quarter of 1995, followed by a population crash in the beginning of 1996. The last trapped indigenous male and female flies were found in weeks 32 and 36, 1996, respectively. Time for 6 fly generations elapsed between the last catch of an indigenous fly and the end of the sterile male releases in December 1997.

The sterile insect technique for controlling populations of Aedes albopictus (Diptera: Culicidae) on Reunion Island: mating vigour of sterilized males.

Reunion Island suffers from high densities of the chikungunya and dengue vector Aedes albopictus. The sterile insect technique (SIT) offers a promising strategy for mosquito-borne diseases prevention and control. For such a strategy to be effective, sterile males need to be competitive enough to fulfil their intended function by reducing wild mosquito populations in natura. We studied the effect of irradiation on sexual maturation and mating success of males, and compared the sexual competitiveness of sterile versus wild males in the presence of wild females in semi-field conditions. For all untreated or sterile males, sexual maturation was completed within 13 to 20 h post-emergence and some males were able to inseminate females when 15 h old. In the absence of competition, untreated and sterile males were able to inseminate the same number of virgin females during 48 h, in small laboratory cages: an average of 93% of females was inseminated no matter the treatment, the age of males, and the sex ratio. Daily mating success of single sterile males followed the same pattern as for untreated ones, although they inseminated significantly fewer females after the ninth day. The competitiveness index of sterile males in semi-field conditions was only 0.14 when they were released at 1-day old, but improved to 0.53 when the release occurred after a 5-day period in laboratory conditions. In SIT simulation experiments, a 5∶1 sterile to wild male ratio allowed a two-fold reduction of the wild population’s fertility. This suggests that sterile males could be sufficiently competitive to mate with wild females within the framework of an SIT component as part of an AW-IPM programme for suppressing a wild population of Ae. albopictus in Reunion Island. It will be of interest to minimise the pre-release period in controlled conditions to ensure a good competitiveness without increasing mass rearing costs.

Strategic Options in Using Sterile Insects for Area-Wide Integrated Pest Management

The four strategic options, “suppression”, “eradication”, “containment” and “prevention”, in which the sterile insect technique (SIT) can be deployed as part of area-wide integrated pest management (AWIPM) interventions, are defined and described in relation to the contexts in which they are applied against exotic or naturally occurring major insect pests. Advantages and disadvantages of these strategic options are analysed, and examples of successful programmes provided. Considerations of pest status, biology and distribution affecting decision-making in relation to strategy selection are reviewed and discussed in terms of feasibility assessment, and programme planning and implementation. Unrealistic expectations are often associated with applying the SIT, resulting in high political costs to change a strategy during implementation. The choice of strategy needs to be assessed carefully, and considerable baseline data obtained to prepare for the selected strategy, before embarking on an AW-IPM programme with an SIT component.

Area-Wide Integrated Pest Management (AW-IPM): Principles, Practice and Prospects

Integrated pest management (IPM) has remained the dominant paradigm of pest control for the last 50 years. IPM has been endorsed by essentially all the multilateral environmental agreements that have transformed the global policy framework of natural resource management, agriculture, and trade. The integration of a number of different control tactics into IPM systems can be done in ways that greatly facilitate the achievement of the goals either of field-by-field pest management, or of area-wide (AW) pest management, which is the management of the total pest population within a delimited area. For several decades IPM and AW pest control have been seen as competing paradigms with different objectives and approaches. Yet, the two “schools” have gradually converged, and it is now generally acknowledged that the synthesis, AW-IPM, neither targets only eradication, nor relies only on single control tactics, and that many successful AW programmes combine a centrally managed top-down approach with a strong grassroots bottom-up approach, and that some are managed in a fully bottom-up manner. AW-IPM is increasingly accepted especially for mobile pests where management at a larger scale is more effective and preferable to the uncoordinated field-by-field approach. For some livestock pests, vectors of human diseases, and pests of crops with a high economic value and low pest tolerance, there are compelling economic incentives for participating in AW control. Nevertheless issues of free riders, public participation and financing of public goods, all play a significant role in AW-IPM implementation. These social and managerial issues have, in several cases, severely hampered the positive outcome of AW programmes; and this emphasises the need for attention not only to ecological, environmental, and economic aspects, but also to the social and management dimensions. Because globalization of trade and tourism are accompanied by the increased movement of invasive alien pest species, AW programmes against major agricultural pests are often being conducted in urban and suburban areas. Especially in such circumstances, factors likely to shift attitudes from apathy to outrage, need to be identified in the programme planning stage and mitigated. This paper reviews the evolution and implementation of the AW-IPM concept and documents its process of development from basic research, through methods development, feasibility studies, commercialization and regulation, to pilot studies and operational programmes.

Back to the future: the sterile insect technique against mosquito disease vectors

With the global burden of mosquito-borne diseases increasing, and some conventional vector control tools losing effectiveness, the sterile insect technique (SIT) is a potential new tool in the arsenal. Equipment and protocols have been developed and validated for efficient mass-rearing, irradiation and release of Aedines and Anophelines that could be useful for several control approaches. Assessment of male quality is becoming more sophisticated, and several groups are well advanced in pilot site selection and population surveillance. It will not be long before SIT feasibility has been evaluated in various settings. Until perfect sexing mechanisms exist, combination of Wolbachia-induced phenotypes, such as cytoplasmic incompatibility and pathogen interference, and irradiation may prove to be the safest solution for population suppression.

Population Genetics as a Tool to Select Tsetse Control Strategies: Suppression or Eradication of Glossina palpalis gambiensis in the Niayes of Senegal

Background The Government of Senegal has initiated the “Projet de lutte contre les glossines dans les Niayes” to remove the trypanosomosis problem from this area in a sustainable way. Due to past failures to sustainably eradicate Glossina palpalis gambiensis from the Niayes area, controversies remain as to the best strategy implement, i.e. “eradication” versus “suppression.” To inform this debate, we used population genetics to measure genetic differentiation between G. palpalis gambiensis from the Niayes and those from the southern tsetse belt (Missira). Methodology/Principal Findings Three different markers (microsatellite DNA, mitochondrial CO1 DNA, and geometric morphometrics of the wings) were used on 153 individuals and revealed that the G. p. gambiensis populations of the Niayes were genetically isolated from the nearest proximate known population of Missira. The genetic differentiation measured between these two areas (θ = 0.12 using microsatellites) was equivalent to a between-taxa differentiation. We also demonstrated that within the Niayes, the population from Dakar – Hann was isolated from the others and had probably experienced a bottleneck. Conclusion/Significance The information presented in this paper leads to the recommendation that an eradication strategy for the Niayes populations is advisable. This kind of study may be repeated in other habitats and for other tsetse species to (i) help decision on appropriate tsetse control strategies and (ii) find other possible discontinuities in tsetse distribution.

Improved quality management to enhance the efficacy of the sterile insect technique for lepidopteran pests

Lepidoptera are among the most severe pests of food and fibre crops in the world and are mainly controlled using broad spectrum insecticides. This does not lead to environmentally sustainable control and farmers are demanding alternative control tools which are both effective and friendly to the environment. The sterile insect technique (SIT), within an area‐wide integrated pest management (AW‐IPM) approach, has proven to be a powerful control tactic for the creation of pest‐free areas or areas of low pest prevalence. Improving the quality of laboratory‐reared moths would increase the efficacy of released sterile moths applied in AW‐IPM programmes that integrate the (SIT). Factors that might affect the quality and field performance of released sterile moths are identified and characterized in this study. Some tools and methods to measure, predict and enhance moth quality are described such as tests for moth quality, female moth trapping systems, ‘smart’ traps, machine vision for recording behaviour, marking techniques, and release technologies. Methods of enhancing rearing systems are discussed with a view to selecting and preserving useful genetic traits that improve field performance.

Reproductive Strategies of Aedes albopictus (Diptera: Culicidae) and Implications for the Sterile Insect Technique

Male insects are expected to optimize their reproductive strategy according to the availability of sperm or other ejaculatory materials, and to the availability and reproductive status of females. Here, we investigated the reproductive strategy and sperm management of male and virgin female Aedes albopictus, a mosquito vector of chikungunya and dengue viruses. The dynamics of semen transfer to the female bursa inseminalis and spermathecae were observed. Double-mating experiments were conducted to study the effect of time lapsed or an oviposition event between two copulations on the likelihood of a female double-insemination and the use of sperm for egg fertilization; untreated fertile males and radio-sterilised males were used for this purpose. Multiple inseminations and therefore the possibility of sperm competition were limited to matings closely spaced in time. When two males consecutively mated the same female within a 40 min interval, in ca. 15% of the cases did both males sire progeny. When the intervals between the copulations were longer, all progeny over several gonotrophic cycles were offspring of the first male. The mating behavior of males was examined during a rapid sequence of copulations. Male Ae. albopictus were parceling sperm allocation over several matings; however they would also attempt to copulate with females irrespective of the available sperm supply or accessory gland secretion material. During each mating, they transferred large quantities of sperm that was not stored for egg fertilization, and they attempted to copulate with mated females with a low probability of transferring their genes to the next generation. The outcomes of this study provided in addition some essential insights with respect to the sterile insect technique (SIT) as a vector control method.

More than one rabbit out of the hat: Radiation, transgenic and symbiont-based approaches for sustainable management of mosquito and tsetse fly populations

Mosquitoes (Diptera: Culicidae) and tsetse flies (Diptera: Glossinidae) are bloodsucking vectors of human and animal pathogens. Mosquito-borne diseases (malaria, filariasis, dengue, zika, and chikungunya) cause severe mortality and morbidity annually, and tsetse fly-borne diseases (African trypanosomes causing sleeping sickness in humans and nagana in livestock) cost Sub-Saharan Africa an estimated US

Mating Compatibility Among Four Pest Members of the Bactrocera dorsalis Fruit Fly Species Complex (Diptera: Tephritidae)

4750 million annually. Current reliance on insecticides for vector control is unsustainable: due to increasing insecticide resistance and growing concerns about health and environmental impacts of chemical control there is a growing need for novel, effective and safe biologically-based methods that are more sustainable. The integration of the sterile insect technique has proven successful to manage crop pests and disease vectors, particularly tsetse flies, and is likely to prove effective against mosquito vectors, particularly once sex-separation methods are improved. Transgenic and symbiont-based approaches are in development, and more advanced in (particularly Aedes) mosquitoes than in tsetse flies; however, issues around stability, sustainability and biosecurity have to be addressed, especially when considering population replacement approaches. Regulatory issues and those relating to intellectual property and economic cost of application must also be overcome. Standardised methods to assess insect quality are required to compare and predict efficacy of the different approaches. Different combinations of these three approaches could be integrated to maximise their benefits, and all have the potential to be used in tsetse and mosquito area-wide integrated pest management programmes.