Historical applications of induced sterilisation in field populations of mosquitoes

David A Dame 2 Christopher F Curtis 1 Mark Q Benedict 0 Alan S Robinson 0 Bart GJ Knols 3 0 Entomology Unit, FAO/IAEA Agriculture and Biotechnology Laboratory, IAEA Laboratories , A-2444 Seibersdorf , Austria 1 London School of Hygiene and Tropical Medicine , UK 2 Entomological Services , 4729 NW 18th Pl, Gainesville, FL 32605-3425 , USA 3 Div. Infectious Diseases, Tropical Medicine & AIDS, Academic Medical Center , F4-217, Meibergdreef 9, 1105 AZ Amsterdam , The Netherlands and K&S Consulting , Kalkestraat 20, 6669 CP Dodewaard , The Netherlands Research on sterile mosquito technology from 1955 to the 1980s provided a substantial body of knowledge on propagation and release of sterile mosquitoes. Radiation sterilisation and chemosterilisation have been used effectively to induce dominant lethality and thereby sterilise important mosquito vectors in the laboratory. Experimental releases of chemosterilised males provided complete control of Anopheles albimanus in a small breeding population (14-15 sq km) in El Salvador. Releases of radiation sterilised males failed to control either Aedes aegypti or Anopheles quadrimaculatus in the USA. Releases of radiation-sterilised and chemosterilised male Culex quinquefasciatus in the USA and India were successful in some instances. Development of genetic sexing systems for Anopheles and improved physical separation methods for Culex have made it possible to rear and release males almost exclusively (> 99%) minimizing the release of potential vectors, the females. Factors that affected efficacy in some field programmes included reduction of competitiveness by radiation, immigration of fertilized females from outside the release zones, and inability of laboratory-bred males to perform in the wild. Despite significant progress, institutional commitments to carry the process further were generally lacking in the late 1970s and until recently. Now, with renewed interest and support for further assessment of this technology, this paper summarizes the current knowledge base, prioritizes some areas of investigation, and challenges scientists and administrators to maintain an awareness of progress, remain realistic about the interpretation of new findings, and make decisions about the sterile insect technique on the basis of informed scientific documentation. Areas recommended for priority research status include the establishment of genetic sexing mechanisms that can be transferred to other mosquito species, re-examination of radiation sterilisation, aerial release technology and mass rearing. - Background The first successful use of the sterile insect technique (SIT), in the early 1950s, involved the New World screwworm Cochliomyia hominivorax, a serious veterinary pest of the western hemisphere. This demonstration of a very challenging new method of pest control led almost immediately to attempts to develop similar approaches to control public health pests, especially mosquitoes. Forty years later, when the New World screwworm had been eliminated from all of North America, Central America and Panama, research on mosquito SIT had dwindled from a major international thrust to a limited academic arena. This paper reviews the main research endeavours that took place from the 1950s to the 1980s, and describes the resulting knowledge and experience that now provides the informational baseline for this renewed interest in mosquito SIT. Major field trials with released sterile mosquitoes Theory and application Sterile insect technique (SIT) has been operational since the late 1950s. Despite the many SIT successes with several insect species during the last four decades, there are still scientists and administrators who do not fully understand the principles or the limitations of the technology. Yet the practitioners of the technology report that as a component of area-wide integrated pest management (AW-IPM) programmes, SIT is currently saving billions of dollars annually in commerce, export markets, reduced environmental impact from pesticides and reduced losses to pests. The initial beneficiaries of this technology were the cattle industry and the wildlife that were spared the ravages of the New World screwworm, now eliminated from North and Central America south through Panama. Knipling's theories [1] focus on AW-IPM concepts, under which SIT can target both large and small areas of pest infestation for elimination, suppression or prevention. Depending upon the specific objective and the population characteristics of the target species, SIT can very rarely stand alone and is more likely to be used in combination with prior suppression and/or complementary concurrent control activities. Initiation of AW-IPM programmes, in the USA for example, usually entails governmental and user (shareholder) agreements, which may require formal referenda in which two-thirds of the shareholders must agree. Prior planning for such programmes includes indepth economic analysis based on capital investment, long-term costs and benefits, and comparison to conventional approaches. Public education is a key component of AW-IPM programmes, which usually include several complementary modes of control. Perhaps the most important aspect of SIT is the realization that it is suitable for only a select group of pests and situations - determined by pest biology, geography, economics and political climate. Some key misunderstandings have led prominent scientists to underestimate the flexibility and utility of SIT. For example, the target insect need not be monogamous. It is important, however, that sperm of sterilised males be competitive with sperm of the wild males. It is not mandatory that a high ratio of sterile males be attained at the onset, although this certainly would be a desirable situation. The necessary level of over-flooding depends on the biology of the insect, the competitiveness of the released insect and the complementary methods of control that are being considered. It is not absolutely necessary that the infestation be isolated from other sources of the pest, but when isolation is not possible, the programme must have the capability of eliminating the influence of immigrating fertilized females. It is not absolutely necessary to eliminate the target species from an experimental plot to demonstrate that the technique works. Carefully planned research can show what the specific impacts of the releases and other factors, such as immigration, have been. With this information, managers can predict with a high level of probability what can be achieved in operational programmes and avoid the usually impossible task of finding the perfect field plot for proving that the system works. Perhaps most confusing is the relationship between numerical release requirements and the biotic (reproductive) potential of the pest. Biotic potential usually varies seasonally and may be density dependent. If the effective over-flooding sterile male ratio is 9:1, and the (...truncated)