PEST MANAGEMENT AND THE ENVIRONMENT
E. F. Legner
Professor of Biological Control
University of California
Improvements in the successful pest management of the agricultural ecosystem and public health sectors calls for an overhaul of current procedures. The availability of specialist personnel to encourage effective management measures backed by technical research is indispensable. Without surveillance management tends to descend to environmentally ineffective or harmful practices, and scheduled routines that do not respond to periodic environmental changes are counterproductive to sound management. Inadequacies of current practices in several examples illustrate the need for research institutions to augment their participation in management and a return to research funding by unbiased sources.
Pest management is a broad concept that involves considerations of genetics, climate, ecology, natural enemies and cultural or chemical applications. Therefore, it is difficult to define this category exactly. A high level of sophistication is required to manage events in the environment for the efficient production of food and fiber and the abatement of public health and nuisance pests. A principal objective to the addition of sound environmental management is the reduction of pesticide usage albeit at the irritation of large commercial interests (Garcia & Legner 1999, Pimentel et al. 1991).
Although scientific investigations in colleges and universities have led to a high level of production and pest abatement, deployment continues to face obstacles that are largely related to the absence of competent supervisory personnel. As expertise resides largely in the research community this group is encumbered by an academic system that continues to stress research and teaching and to minimize the deployment aspect. The most successful programs in environmental management regularly require five or more years to develop. Investigator survival in the system demands frequent publication, but not in the kind of journals that stress implementation. This distracts from the ultimate goal of deployment, which diminishes the amount of time an investigator has to be directly involved in an advisory capacity. Several examples of successful projects that have receded in the absence of this supervision but which could be reactivated with the proper advisory personnel present, will explain some of the problems and difficulties involved.
Navel Orangeworm Management in Almond Orchards
The almond industry in California has suffered from the invasion of the navel orangeworm, Amyelois transitella (Walker), from Mexico and South America. Two external insect larval parasites, Goniozus legneri Gordh and Goniozus emigratus (Rohwer) and one internal egg-larval parasite, Copidosomopsis plethorica Caltagirone, which are dominant on the pest in south Texas, Mexico, Uruguay and Argentina, were successfully established in irrigated and nonirrigated almond orchards in California (Caltagirone 1966, Legner & Silveira-Guido 1983). Separate k-value analyses indicated significant regulation of their navel orangeworm host during the warm summer season. There is a diapause (hibernation) in the host triggered by several seasonally varying factors, and a diapause in the parasites triggered by hormonal changes in the host. Possible latitudinal effects on diapause (hibernation) also are present. The ability of the imported parasites to diapause with their host enables their permanent establishment and ability to reduce host population densities to below economic levels (Legner 1983).
Although navel orangeworm infestations have decreased with the establishment of the three parasites (Legner & Gordh 1992), the almond reject levels are not always below the economic threshold of 4%. Such rejects are sometimes due to other causes, such as ant damage and fungus infections. In certain years, the peach tree borer, Synanthedon exitiosa (Say), has been involved as its attacks stimulates oviposition by navel orangeworm moths and subsequent damage attributed to the latter.
In some orchards, the growers have sustained a reject level of 2 ˝ percent or less through 2008. Storing rejected almond mummies in ventilated sheds through winter allows for a build up of natural enemies and their subsequent early entry into the fields to reduce orangeworm populations before the latter have an opportunity to increase. Commercial insectaries have harvested Goniozus legneri from orchards for introductions elsewhere. Copidosomopsis plethoricus and Goniozus legneri, and to a lesser extent Goniozus emigratus successfully overwinter in orchards year after year. However, only Copidosomopsis can consistently be recovered at all times of the year. The Goniozus species are not recovered in significant numbers until early summer. Therefore, pest management in almond orchards may require periodic releases of Goniozus legneri to reestablish balances that were disrupted by insecticidal drift or by the absence of overwintering rejected almond refuges through aggressive sanitation practices. Although sanitation in this case may appeal to the grower, it is a costly procedure that also disrupts natural balances at low pest densities.
Goniozus legneri has been reared from codling moth and oriental fruit moth in peaches in addition to navel orangeworm from almonds. A reservoir of residual almonds that remain in the trees after harvest is desirable to maintain a synchrony of these parasites with navel orangeworms in order to achieve the lowest pest densities. In fact such reservoirs often exceed 1,000 residual almonds per tree through the winter months, and produce navel orangeworm densities at harvest that are below 1% on soft-shelled varieties. Superimposed upon the system is the diapausing mechanism in both the navel orangeworm and the parasites (Legner 1983). All of these forces must be considered for a sound, reliable integrated management. Almond producers have to make reasonable decisions on whether or not to remove residual almonds, a very costly procedure, or to use within season insecticidal sprays. But orchard managers rarely understand population stability through the interaction of natural enemies and their prey. Because the management of this pest with parasitic insects depends heavily on the perpetuation of parasites in orchards it can only be accomplished by an understanding of the dynamics involved. Storing rejected almonds in protective shelters during winter months increases parasite abundance. This allows the parasites to reproduce in large numbers for subsequent spread throughout an orchard in the spring when outdoor temperatures rise. Complete sanitation of an orchard by removal of all rejected almonds is counter productive to successful management as this also eliminates natural enemies.
Australian Bushfly Management in Micronesia
Pestiferous flies in the Marshall Islands provide a classic example of the adaptation of invading noxious insects to an area with a salubrious climate. With nearly perfect temperature-humidity conditions for their development, an abundance of carbohydrate and protein-rich food in the form of organic wastes and excreta provided by humans and their animals, and a general absence of effective natural enemies, several species were able to reach maximum numbers.
There are principally four types of pestiferous flies in Kwajalein Atoll of the Marshall Islands, with the African-Australian bush fly, Musca sorbens Wiedemann, being by far the most pestiferous species. The common housefly, Musca domestica L., of lesser importance, frequents houses and is attracted to food in recreation areas. The remaining two types are the Calliphoridae [Chrysomya megacephala (Fab.), and (Wiedemann)], and the Sarcophagidae [Parasarcophaga misera (Walker), and Phytosarcophaga gressitti Hall and Bohart). These latter species are abundant around refuse disposal sites and wherever rotting meat and decaying fish are available. Most of the fly species differ from the common housefly and the bush fly in being more sluggish and noisy and by their general avoidance of humans. Because residents do not distinguish the different kinds of flies, nonpestiferous types are often blamed as nuisances when in fact they may be considered to fulfill a useful role in the biodegradation of refuse and rotting meat.
An initial assessment of the problem led to the expedient implementation of breeding source reduction to reduce the housefly, Musca domestica L., and both the Calliphoridae and Sarcophagidae to inconspicuous levels. These involved slight modifications of refuse disposal sites to disfavor fly breeding. These simple measures resulted in an estimated 1/3rd reduction of total flies concentrating around beaches and residential areas. Because the housefly especially enters dwellings, its reduction was desirable for the general health of the community, and fly annoyances indoors diminished. Thorough surveys of breeding sites and natural enemy complexes revealed that Musca sorbens reduction would not be quickly forthcoming, however. A schedule of importation of natural enemies was begun and other integrated management approaches were investigated: e.g. baiting and breeding habitat reduction.
Bush Fly Origin and Habits. -- This species is known as the bazaar fly in North Africa, a housefly in India, and the bush fly in Australia (Yu 1971). It was first described from Sierra Leone in West Africa in 1830 where it is a notorious nuisance to humans and animals. The flies are attracted to wounds, sores, and skin lesions, searching for any possible food sources such as blood and other exudations. Although not a biting species, its habits of transmitting eye diseases, enteric infections, pathogenic bacteria and helminth eggs make it a most important and dangerous public health insect (Bell 1969, Greenberg 1971, Hafez and Attia 1958, McGuire and Durant 1957)
The bush fly has spread through a major portion of the Old World, Africa and parts of Asia (Van Emden 1965). In Oceania its distribution is in AustraIia (Paterson and Norris 1970); New Guinea (Paterson and Norris 1970); Samoa and Guam (Harris and Down 1946); and the Marshall Islands (Bohart and Gressitt 1951). In Hawaii Joyce first reported it in 1950. Later Hardy (1952) listed it in the Catalog of Hawaiian Diptera, and Wilton (1963) reported its predilection for dog excrement. The importance of bush fly increased in the 1960's when it was incriminated as a potential vector of Beta-haemolytic streptococci in an epidemic of acute glomerulonephritis (Bell 1969).
On the islands of Kwajalein Atoll a substantial portion of the main density of Musca sorbens emanated from dog, pig and human feces. Inspections of pig droppings in the bush of 10 widely separated islets revealed high numbers of larvae (over 100 per dropping), making this dung, as in Guam (Bohart and Gressitt 1951), a primary breeding source in the Atoll. Pigs that are corralled on soil or concrete slabs concentrate and trample their droppings making them less suitable breeding sites. In such situations flies were only able to complete their development along the periphery of corrals. Coconut husks placed under pigs in corrals results in the production of greater numbers of flies by reducing the effectiveness of trampling. Kitchen and other organic wastes were not found to breed M. sorbens, although a very low percentage of the adult population could originate there judging from reports elsewhere. Nevertheless, this medium is certainly not responsible for producing a significant percentage of the adult densities observed in the Atoll.
Management Efforts Worldwide. -- Successful partial reduction of bush fly had been achieved only in Hawaii through a combination of the elimination of breeding sites, principally dog droppings, and the activities of parasitic and predatory insects introduced earlier to combat other fly species, e.g., Musca domestica (Legner 1978). The density of-bush fly varies in different climatic zones in Hawaii, but the importance of this fly is minimal compared to Kwajalein. At times hymenopterous parasites have been found to parasitize over 95% of flies sampled in the Waikiki area (H-S. Yu, unpublished data). Other parts of Oceania were either not suitable for the maximum effectiveness of known parasitic species (e.g. Australia) or the principal breeding habitats were not attractive to the natural enemies. Therefore, in Australia a concerted effort has been made to secure scavenger and predatory insects from southern Africa that are effective in the principal unmanageable fly producing source, range cattle and sheep dung (Bornemissza 1970).
Kwajalein Atoll. -- Integrated fly management had reached a level of partial success by 1974. Initial surveys for natural enemies of M. sorbens revealed the presence of four scavenger and predatory insects, the histerid Carcinops troglodytes Erichson, the nitidulid Carpophilus pilosellus Motschulsky, the tenebrionid Alphitobius diaperinus (Panzer), and the dermapteran Labidura riparia (Pallas). Dog numbers were significantly reduced and all privies were reconstructed or improved on one island, Ebeye. Dogs were reduced or tethered on Kwajalein Island and refuse fish, etc., disposed of thoroughly on l1leginni and other islands with American residents. Importations of natural enemies were made throughout the Atoll, and the average density of M. sorbens on Ebeye was subsequently reduced from an estimated 8.5 flies attracted to the face per minute, to less than 0.5 flies per minute, which was readily appreciated by the inhabitants. The single most important cause appeared to be the partial elimination of breeding sources, with natural enemies playing a secondary role.
For the further reduction of bush fly numbers the integration of a nondestructive insecticidal reduction measure was desirable. Sugar bait mixtures that have been used for houseflies in years previous to 1972 were wholly ineffective for killing adult M. sorbens due to their almost complete lack of attractiveness. However, a variety of decomposing foodstuffs including rotting eggs and rotting fish sauces were very highly attractive. Experiments using a 6-day old mixture of one-part fresh whole eggs to one part water (Legner et al. 1974) attracted over 50,000 bush flies that were then killed by a 0.5 ppm Dichlorvos (R) additive. The poisoned mixture was poured in quantities of 100 mI. each in flat plastic trays with damp sand at 20 sites in the shade and spaced every 10 meters along a public beach on Kwajalein. Baits placed above the height of 1m or against walls in open pavilions were only weakly attractive. After 48 hours, flies were reduced to inconspicuous levels all over Kwajalein Island. This condition endured for at least three days after which newly emerging and immigrating flies managed to slowly increase to annoying levels as the baits ceased to be attractive. But the former density of flies was never reached even one week after the baiting; and these populations were subsequently reduced to even lower levels by applying additional fresh poisoned baits.
Baiting was extended to other islands in the Atoll with the result of sustained reductions of bush flies to below general annoyance levels (less than 0.01 attracted per minute on Kwajalein, Roi-Namur, Illeginni and Meck Islands.) A new attractant that augmented the rotting egg mixture consisted of beach sand soaked for one week in the decomposing body fluids of buried sharks. This new attractant was far superior to rotting eggs both in rate and time of attraction, the latter sometimes exceeding 5 days. The baiting method could be used effectively if applied initially twice a week, and only biweekly applications were necessary in the following months.
After January 2000 in the absence of specialist supervision the baiting procedure in the Atoll has not continued with the sophistication initially determined necessary. In the absence of supervision the flies were not adequately reduced. Periodic personnel changes precluded the passing on of accurate information critical to managing the fly densities. Of vital importance is habitat reduction, the proper preparation of baits and the latter’s placement in shaded wind calm areas of the islands. Because such sites are generally out of sight of the public, baiting has rather shifted to populated areas where only very conspicuous but nonpestiferous species of flies are attracted to the baits in large numbers. Sometimes even ammonia baits were substituted that attract harmless blow fly species but not the targeted bush fly.
Aquatic Weed Management by Fish in Irrigation Systems
Imported fish species have been used for clearing aquatic vegetation from waterways, which has also reduced mosquito & chironomid midge abundance. In the irrigation systems, storm drainage channels and recreational lakes of southern California, the California Department of Fish and Game authorized the introduction of three species of African cichlids, Tilapia zillii (Gervais), Oreochromis (Sarotherodon) mossambica (Peters), and Oreochromis (Sarotherodon) hornorum (Trewazas). These became established over some 2,000 ha. of waterways (Legner & Sjogren 1984). Their establishment reduced the biomass of emergent aquatic vegetation that was slowing down the distribution of irrigation water but that also provided a habitat for such encephalitis vectors as the mosquito Culex tarsalis Coquillet. Previous aquatic weed reduction practices had required an expensive physical removal of vegetation and/or the frequent application of herbicides.
One species, Tilapia zillii can reduce mosquito populations by a combination of direct predation and the consumption of aquatic plants by these omnivorous fishes (Legner & Fisher 1980; Legner & Murray 1981, Legner & Pelsue 1983). As Legner & Sjogren (1984) indicated, this is a unique example of persistent biological suppression and probably only applicable for relatively stable irrigation systems where a permanent water supply is assured, and where water temperatures are warm enough in winter to sustain the fish (Legner et al. 1980). A three-fold advantage in the use of these fish is (1) clearing of vegetation to keep waterways open, (2) mosquito abatement and (3) a fish large enough to be used for human consumption. However, optimum management of these cichlids for aquatic weed reduction often is not understood by irrigation district personnel (Hauser et al. 1976, 1977; Legner 1978), with the result that competitive displacement by inferior cichlids minimize or eliminate T. zillii, the most efficient weed eating species (Legner 2000).
The three imported fish species varied in their influence in different parts of the irrigation system. Each fish species possessed certain attributes for combating the respective target pests (Legner & Medved 1973a, b). Tilapia zillii was best able to perform both as a habitat reducer and an insect predator. It also had a slightly greater tolerance to low water temperatures, which guaranteed the survival of large populations through the winter months; while at the same time it did not pose a threat to salmon and other game fisheries in the colder waters of central California. It was the superior game species and most desirable as human food. Nevertheless, the agencies supporting the research (mosquito abatement and county irrigation districts) acquired and distributed all three species simultaneously throughout hundreds of kilometers of the irrigation system, storm drainage channels and recreational lakes. The outcome was the permanent and semi permanent establishment of the two less desirable species, S. mossambica and S. hornorum over a broader portion of the distribution range. This was achieved by the competitively advantaged Sarotherodon species that mouth-brood their fry, while T. zillii did not have this attribute strongly developed. It serves as an example of competitive exclusion such as conjectured by Ehler (1982). In the clear waters of some lakes in coastal and southwestern California, the intense predatory behavior of S. mossambica males on the fry of T. zillii could be easily observed, even though adults of the latter species gave a strong effort to fend off these attacks.
This outcome was not too serious for chironomid reduction in storm drainage channels because the Sarotherodon species are quite capable of permanently suppressing chironomid densities to below annoyance levels (Legner et al. 1980). However, for the management of aquatic weeds, namely Potamogeton pectinatus L., Myriophyllum spicatum var. exalbescens (Fernald) Jepson, Hydrilla verticillata Royle and Typha species, they showed little capability (Legner & Medved 1973b). Thus, competition excluded T. zillii from expressing its maximum potential in the irrigation channels of the lower Sonoran Desert and in recreational lakes of southwestern California. Furthermore, as the Sarotherodon species were of a more tropical nature, their populations were reduced in the colder waters of the irrigation canals and recreational lakes. Although T. zillii populations could have been restocked, attention was later focused on a potentially more environmentally destructive species, the White Amur, Ctenopharyngodon idella (Valenciennes), and other carps. The competitively advantaged Sarotherodon species are permanently established over a broad geographic area, which encumbers the reestablishment of T. zillii in storm drainage channels of southwestern California.
Managment of Filth Fly Abundance in Dairies and Poultry Houses
The most important of muscoid fly species are broadly defined as those most closely associated with human activities. Breeding habitats very from the organic wastes of urban and rural settlements to those provided by various agricultural practices, particularly ones related to the management and care of domestic animals. Their degree of relationship to humans varies considerably with the ecology and behavior of the fly species involved. Some are more often found inside dwellings.
Research to reduce fly abundance has centered on the highly destructive parasitic and predatory species, such as the encyrtid Tachinaephagus zealandicus Ashmead, five species of the pteromalid genus Muscidifurax, and Spalangia species that destroy dipterous larvae and pupae in various breeding sources. The natural enemies are capable of successful fly suppression if the correct species and strains are applied in the right locality (Axtell & Rutz 1986, Legner et al. 1981 , Mandeville et al. 1988, Pawson & Petersen 1988). Other approaches have included the use of pathogens and predatory mites, and inundative releases of parasites and predators (Ripa 1986, 1990). Although partially successful, none of these strategies have become the sole method for fly abatement, and the choice of a ineffective parasite strain may have detrimental results (Legner 1978). Instead, the focus is on integrated management including habitat reduction, adult baiting and aerosol treatments with short residual insecticides. Also, it is generally agreed that existing predatory complexes exert great influences on fly densities (Geden & Axtell 1988) and that many natural enemies of these flies have a potential to significantly reduce their abundance if managed properly (Legner 2000, Mullens 1986, Mullens et al. 1986). Because climatic and locality differences dictate which abatement strategies are effective, simple instructions to the public are impossible and the involvement of skilled personnel is required. Of primary importance for successful management is the provision of relatively stable breeding habitats and their natural enemy complexes. Periodic cleaning operations should stress the partial removal of breeding sites and the deposition of such waste into large stacks that favors the generation of destructive heat while minimizing the area and attractiveness for fly oviposition. Nevertheless, this management procedure is difficult for abatement personnel to grasp in the absence of competent supervision.
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