Integrated Mosquito Management (IMM)

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The following is taken wholly from Chapter 9 (Mosquito Control Benefits and Risks) in the Florida Mosquito Control White Paper developed by the Florida Coordinating Council on Mosquito Control. 2009. Florida Mosquito Control: The state of the mission as defined by mosquito controllers, regulators, and environmental managers. University of Florida; Vero Beach, FL, USA

MOSQUITO CONTROL BENEFITS AND RISKS

In Florida, both mosquito control and the protection of environmentally sensitive habitats are legislatively mandated. Clearly, modern mosquito control poses some environmental risks, yet it just as obviously provides benefits. Public health protection, improved human comfort from mosquito annoyance, and economic payback are the most obvious benefits. Impacts on fish, wildlife, and non-target arthropods are some of the risks. There is also growing concern about the risks of human exposure to pesticides in general. These potential impacts to both natural communities and to humans need to be sufficiently understood to help risk/benefit analysis that can result in informed decision making.

Modern mosquito control methodology dictates the use of an integrated pest management program, utilizing adulticiding, larviciding, and source reduction as appropriate, and incorporating a public education component. Mosquito control agencies and environmental land management agencies are required to work together to resolve any controversial issues that arise by carefully weighing the risks and benefits in each situation.

INTRODUCTION

The use of various chemicals to attempt to control pests of humans, crops, and animals has been documented since ancient times. Homer described how Odysseus fumigated a house with burning sulfur to control pests (Ware 1994). The Chinese used arsenic sulfide to kill insects (Pimentel and Lehman 1993). The use and success of chemicals drastically changed with the development of synthetic pesticides a little over fifty years ago. The Swiss chemist Paul Müller discovered the insecticidal properties of the organochlorine pesticide dichlorodiphenyl- trichloroethane (DDT), and the United States Department of Agriculture (USDA) laboratory in Orlando developed it for field use by the armed services. An arsenic compound (Paris green) was used in Florida for larval control during the 1960s.

These and many other synthetic pesticides were developed by scientists for the control of insects and other pests in many situations in both public health and agriculture. In the early years their effectiveness, just like that of antibiotics, was so dramatic that their development was considered miraculous. As a result, these chemicals were widely and often indiscriminately applied. While some people questioned such a widespread use of pesticides, many more people praised it. At that time, research had not yet documented the environmental, ecological, or human hazards of these materials. What people did know throughout the world was that chemical control of mosquitoes and other pests significantly reduced human illness and death and greatly improved human comfort.

The risks involved with pesticide use were not widely questioned until the early 1960s when Rachel Carson published Silent Spring (Carson 1962). Although the science was controversial (Edwards 2002), this publication increased public awareness of issues such as:

The risks involved with pesticide use were not widely questioned until the early 1960's when Rachel Carson published Silent Spring. This and other studies and publications increased public awareness of issues such as: 1) Acute and chronic pesticide impacts to humans, wildlife, and other non-target species, 2) the persistence of certain pesticides in the environment, and 3) the transport of pesticides outside target areas, which can cause unintended environmental damage. Mosquito control contributes to these environmental problems, but compared to agricultural methods and materials, mosquito control pesticides are applied at lower dosages (Ohio Vector News, Dec. 1990) and in smaller amounts. The primary environmental difficulty with the use of mosquito control chemicals is that often pesticides are applied directly into residential areas and into sensitive natural environments.

Mosquito control contributes to some of these environmental problems, but compared to agricultural methods and materials, mosquito control pesticides are applied at lower dosages and in smaller amounts (Lyon and Steele 1998). In Florida, agriculture and lawn care are believed to represent much greater potential impacts to the aquatic environment than does mosquito control (Hushon 2006).

Mosquito control pesticides are regulated federally by the U.S. Environmental Protection Agency (EPA) which is responsible for authorizing labels for allowable chemicals. The legal authority for mosquito control in Florida is Chapter 388 Florida Statues (F.S.). Mosquito control is regulated by the Florida Department of Agriculture and Consumer Services (FDACS), which designates which chemicals are permitted for use. FDACS also oversees Florida mosquito control operations by making certain that they comply with Florida Statutes and any appropriate rules.

The University of Florida’s (UF) Bureau of Economic and Business Research (2004) estimates that from 1900 to 2000 Florida's population increased by almost 3,000%. There is little doubt that implementation of both physical and chemical mosquito control techniques aided in the development and utilization of areas that previously were not considered acceptable for human habitation. Certainly, Florida's explosive growth in coastal areas after World War II was due in large part to the use of synthetic pesticides and physical methods to control mosquitoes.

Controversy often accompanies mosquito control because the chemicals frequently are applied in developed areas, and some people are concerned with their own exposure. Treatment also occurs in natural areas, including protected public lands, and some people are concerned about effects on wildlife. It is vitally important that the risks and benefits of mosquito control practices are analyzed scientifically so that the control decisions can be made with a good understanding of their effects.

Prior to the early 1980s, mosquito control practices were questioned only when obvious, adverse effects on wildlife were observed (e.g., Patterson 2004). We now better appreciate the complex interrelationships of organisms within an ecosystem. For instance, the food of many marine organisms consists of small arthropods or organisms that are similar in size to mosquito larvae, and such organisms differ greatly in their susceptibility to pesticides (Curtis and Profeta 1993). Some organisms may be more sensitive to pesticides than mosquitoes. Impacting any portion of this food web may affect other parts or even the entire web. The current lack of knowledge concerning the biology of many non-target species and their community functions further complicates the problem of risk/benefit analysis.

Mosquito control practices usually focus on the monitoring of mosquito populations with little or no routine monitoring of non-target species. The difficulty and cost of monitoring non-target effects in the natural environment has impeded this type of work. Ideally, long-term goals for non-target assessments are:

Moreover, mosquito control programs must place more emphasis on non-chemical techniques to control mosquitoes in order to reduce non-target impacts.

INTEGRATED PEST MANAGEMENT (IPM)

It is important that mosquito control agencies maintain a broad selection of tools, both chemical and non-chemical, to use in managing mosquito populations in Florida. It is also important that the potential impacts to both natural communities and to humans are understood sufficiently to help in risk/benefit analysis that can result in informed decision-making. For the most part, since 1949, mosquito agency activities have been directed primarily towards nuisance mosquitoes, those which are of economic importance but do not transmit diseases to humans. However, mosquito-borne diseases are on the rise worldwide and several diseases are threats to public health and animal health in Florida. These diseases include St. Louis encephalitis, eastern equine encephalitis, Highlands J encephalitis, West Nile encephalitis, and California group encephalitis (i.e., Keystone and Trivitattus).

The most effective and environmentally sound pest control programs are based on a combination of methods including source reduction, chemical control, and biological control (Rose 2001). Using a combination of these techniques is termed Integrated Pest Management (IPM). IPM has been developed to encourage a balanced usage of cultural and insecticidal methodologies and habitat manipulations in order to minimize adverse environmental impacts. To effectively use IPM, it is necessary to have a thorough understanding of the basic biology of the pest species and the many factors that influence their density. Because of rapid mosquito population reduction and economic considerations, many mosquito control programs use chemical applications as their primary control method. A program that relies solely on chemical control is not an IPM program. While most components of an IPM program have some level of environmental risk, the overall risks are likely to be less than a program that relies solely on chemical control, which might cause undesirable non-target mortality and contribute to chemical resistance in mosquitoes.

MOSQUITO CONTROL INSECTICIDES: PAST AND PRESENT

The synthetic pesticides used for mosquito control over the years have varied greatly in structure, toxicity, persistence, and environmental impact. These chemicals include the following:

Organochlorine pesticides are no longer used for mosquito control in Florida, although methoxychlor was labeled for use until its cancellation in 2003 (Edwards 2004). Some organochlorines that were formerly used included DDT, BHC, chlordane, heptachlor, aldrin, and dieldrin. Organochlorines are relatively nonsoluble in water and very persistent in soils. Also, they are lipophilic, i.e., they bioaccumulate in fat and other lipids. Largely, it was these lipophilic properties that resulted in organochlorines no longer being labeled for use in the U.S. These bans are still actively criticized by some (e.g., Tren and Bate 2000, Bailey 2002, Edwards 2004). In spite of cancellation of all uses of these chemicals in the U.S. by the EPA between 1973 and 1988 (Ware 1994), many soils and rivers are still contaminated with residues of the most persistent of these compounds (i.e., DDT, endrin, dieldrin) (White and Krynitsky 1986), and they continue to be detected in wildlife (Clark et al. 1995, Sparling et al. 2001). The total concentration of DDT residues in the U.S. appears to be declining (Nowell et al. 1999). Organochlorines continue to be used for agricultural and mosquito control in developing countries.

Organophosphates (OP). Although OPs are generally less persistent than organochlorines, some have higher acute toxicities for mammals and other organisms (Pimentel and Lehman 1993). Currently recommended OP compounds are the adulticides malathion (Fyfanon®), naled (Dibrom®), and the larvicide temephos (Abate®). These compounds have relatively low mammalian toxicity and most usually break down rapidly; however, some intermediate breakdown products are also toxic. Accidental discharge of organophosphorus insecticides into aquatic environments has caused fish kills, and some of the OP compounds are toxic to microcrustaceans such as Daphnia spp. (WHO 1986a). Fenthion (Baytex®) is no longer used for mosquito control in the U.S.

Pyrethroids. Pyrethroid insecticides are based on the chemical structure of a group of naturally occurring compounds, pyrethrums, derived from a flower native to Africa. Products extracted from these flowers have been used for thousands of years and are still used today but are extremely expensive. Artificially created pyrethroids used today in Florida for mosquito control are resmethrin, permethrin, and sumethrin. Pyrethroids are more persistent than natural pyrethrums and in a few cases are more persistent than OPs, although resmethrin degrades rapidly in the environment (WHO 1989). Pyrethroids are broad-spectrum toxicants that are very toxic to fish, aquatic organisms, and most other cold-blooded animals. Due to their high and broad range of toxicity to insects, they may affect beneficial species, thereby lessening natural controls, and, for some pests, may actually increase the need for further chemical control (Edwards 1993). However, to date, a need for increased chemical control because of pyrethroid use for mosquito control has not been demonstrated. Pyrethroids exhibit low toxicity to birds and mammals (EPA 2002).

Carbamates. Methyl carbamates are related chemically to physostigmine, a naturally-occurring alkaloid isolated from the calabar bean (WHO 1986b). No carbamates are currently used for mosquito control in Florida, although propoxur has been used. Carbamates are broad-spectrum, tend to be more persistent than organophosphates in soil, and thus have the potential for considerable environmental impact (Edwards 1993). However, data exist that suggest carbamates are liable to degradation by soil microorganisms (WHO 1986b). Propoxur is considered to be moderately toxic to mammals (WHO 1986b).

Insect Growth Regulators (IGR). IGRs interfere with insect development typically resulting in larval or pupal mortality. For more than thirty years, the insect growth regulator methoprene, Altosid®,, has been a widely used mosquito larvicide in Florida and elsewhere in the world. Methoprene is specific to immature insect larvae, especially dipterans, which include mosquitoes. Methoprene has extremely low mammalian toxicity. Diflubenzuron (Dimilin®), a chitin inhibitor, has much broader non-target impacts than methoprene, especially on marine and freshwater arthropods such as shrimp and crabs. Therefore, Dimilin is severely restricted to certain sites and is not widely used.

Biologicals. Bacillus thuringiensis israelensis (Bti) and B. sphaericus (Bs) are both bacterial larvicides (acting as stomach poisons) that are quite specific to mosquito larvae and a few other aquatic dipterans. Bti is used worldwide. Bs is more recently labeled and is only effective in freshwater habitats. Bs has a narrower host range than does Bti (Bauman et al. 1991). Bs can be used in water of much lower quality than can Bti and can actually improve water quality by suppressing algal growth (Silapanunatakul et al. 1983, Su and Mulla 1999). Both are non-toxic to mammals and exhibit few or no non-target effects (WHO 1999, Ware 1994, Boisvert and Boisvert 2000).

Surface films. Petroleum distillates (i.e., oils) are used as pupacides, to suffocate mosquitoes prior to adult emergence. These oils can be toxic to predatory Hemiptera and Coleoptera, as well as sheepshead minnows, but are not toxic to rotifers and some protozoa (Mulla and Darwazeh 1981; Tietze et al. 1993, 1995). Monomolecular films, alcohol ethoxylated surfactants, are used as larvicides and pupacides. They disrupt surface tension and cause larvae and pupae to drown. Monomolecular films currently are being evaluated in Florida regarding their toxicity to non-target insects in salt water marsh habitat. Monomolecular films are not as efficacious when exposed to high winds (Nayar and Ali 2003).

BENEFITS OF MOSQUITO CONTROL

Broadly speaking, the benefits of mosquito control can be divided into three classes: nuisance benefits, economic benefits, and public health benefits. Nuisance benefits include relief to people around homes or in parks and recreational areas. Nuisance benefits can even be said to extend to pets and to wildlife. Economic benefits include increased real estate values, enhanced tourism and related business interests, or increased livestock or poultry production. Public health benefits include the reduction of infectious disease agents.

Nuisance Benefits

A benefit of mosquito control that has greatly contributed to Florida's growth is the tremendous progress made in controlling pestiferous mosquito species, especially those that are found in coastal marshes. Although many of these pest mosquitoes do not present a threat of disease transmission to humans, they significantly affect human comfort. Prior to the advent of organized mosquito control in Florida, mosquito numbers were such that residents could not go outdoors after dark, and many coastal towns closed down for the summer season (Harden 1981). The influx of an estimated 700-800 people moving to Florida daily and the fact that much new development occurs near mosquito-producing habitats puts increasing pressure on mosquito control agencies to maintain effective control programs.

The nuisance factor to pets also may be considered important to many people. Video evidence exists that mosquitoes are severe pests of purple martin nestlings (Hill 1994). The introduction of novel viral pathogens into naïve populations may Chapter 9: Mosquito Control Risks and Benefits Page 151 have impacts (Farajollahi et al. 2004, Miller et al. 2005). For example, during the 2001 West Nile virus outbreak in Florida, 1,106 dead birds reported to the Florida Department of Health were found to be infected with West Nile virus. The affected birds comprised 10 orders and 25 families (Blackmore et al. 2003).

Economic Benefits

Florida's economy benefits from tourism (almost 84 million visitors in 2006) which depends on the beaches, fishing, golfing, amusement parks, and the outdoors in general. Tourism resulted in $65 billion in taxable sales in 2006 and supported almost one million jobs for Floridians (Visit Florida 2007). Most of these visitors have little tolerance for mosquitoes, and it seems reasonable that mosquito control helps many visitors enjoy their stay and, therefore, helps the Florida economy. Perhaps the most striking illustration of the economic benefits of controlling mosquitoes is the classic graph by Dr. John A. Mulrennan, Sr. showing that for the period 1950-1967, the decline in average light trap catch for the female saltmarsh mosquito (Aedes taeniorhynchus) correlated with increasing tourist expenditures (Breeland and Mulrennan 1983). The dramatic decrease in saltmarsh mosquitoes during this period, in large measure due to impoundment, ditching, and filling of salt marshes, facilitated the development of large areas of coastal Florida and a general increase in tourism (Gaiser 1980, Harden 1981, Thomas 1981).

Economic impacts of mosquito-borne diseases have not been well documented in the past, but recent research suggests that any type of vector-borne epidemic will have local and statewide, direct and indirect economic impacts that may be in the multi-millions of dollars. For example, the 1990 SLE epidemic not only caused considerable illness (223 confirmed cases with 11 deaths), but Florida saw a 15% decrease in tourism-related revenues in the last quarter of the year (Mulrennan 1991). The 2002 West Nile virus (WN) epidemic was estimated to have cost over $20 million in Louisiana alone (Zohrabian et al. 2004). Mosquito control possibly decreases these impacts by reducing the chances for outbreaks and by helping to control them when they occur (e.g., Ruiz et al. 2004).

Another economic benefit of mosquito control is increased worker productivity. In outdoor work areas, such as crop fields, marinas, orchards, sawmills, and the construction trades, productivity of work crews can fall to near zero in the presence of large numbers of mosquitoes.

A wide cross-section of domestic animals also benefit from mosquito control. Data on loss of meat or dairy production due to mosquito attack are difficult to come by, although older literature reported losses in milk production of up to 40% and losses in beef cattle weight gain (reviewed in Steelman 1976). Research conducted in Louisiana showed that a combination of mosquito control and improved diet resulted in significant increases in weight gain by beef cattle (Steelman et al. 1972, 1973). The suffocation of cattle by hordes of mosquitoes Chapter 9: Mosquito Control Risks and Benefits Page 152 prior to modern mosquito control was documented in news reports and has occurred in recent times as well (Addison and Ritchie 1993). One source estimated an economic loss of $61 million dollars in one year due to mosquitoes (Hamer 1985, cited in Frank et al. 1997)

Birds and other wildlife may serve as reservoirs for mosquito-borne diseases that can impact animals of economic importance (USDA 2005). Horses in Florida are at risk from infection by eastern equine encephalitis virus and West Nile virus and potentially from Venezuelan equine encephalitis virus (Lord and Rutledge- Connelly 2006). During the 2001 West Nile virus outbreak in Florida, 492 horses were confirmed to have had acute West Nile encephalitis (Blackmore et al. 2003).

Public Health Benefits

Another important benefit of mosquito control is the targeting of mosquitoes that transmit diseases. Mosquito control is an important and basic public health service (ASTHO 2003). Since 1978, some public health departments and mosquito control agencies throughout the state have participated in a surveillance program using sentinel chickens to closely monitor for St. Louis encephalitis (SLE) and eastern equine encephalitis (EEE) viruses. Arbovirus outbreaks, like the 1990 SLE epidemic (223 confirmed cases with 11 deaths) (Mulrennan 1991) and the 2002 West Nile virus (WN) epidemic in the United States (4,156 reported cases with 284 fatalities) (O’Leary et al. 2004) typically result in increased and targeted mosquito control to stem the outbreaks. On a personal level, a survivor of EEE infection may need lifetime medical support costing into the millions of dollars (Villari et al. 1995). Long-term sequelae of West Nile virus infection include abnormalities of motor skills, attention, and executive functions, all of which may negatively impact quality of life and productivity (Carson et al. 2006).

There are also social justice benefits to mosquito control. At least three different studies (Kutz et al. 2003, Ruiz et al. 2004, Rios et al. 2006) have suggested that the burden of mosquito-borne viral diseases falls more heavily upon lower-income residents and minority group communities.

COSTS OF MOSQUITO CONTROL

Human Health Concerns

A consideration associated with the overall use of pesticides, of which mosquito control is a part, is the potential human health risk of pesticide exposure. In the last several years, more evidence has been evaluated concerning the impact on humans from a half-century of exposure to synthetic chemicals and other environmental contaminants. Human health problems associated with the effects of severe, acute exposure to organophosphate pesticides include irreversible neurological defects, memory loss, mood changes, infertility, and disorientation (Savage et al. 1988). However, health effects are generally attributed to exposure Chapter 9: Mosquito Control Risks and Benefits Page 153 to agricultural applications to food – not to mosquito control applications. No clear evidence exists for adverse effects on human health from long-term exposure to organophosphate insecticides at levels that do not affect acetylcholinesterase levels (WHO 1986a). In fact, recent research suggests that human health risks from mosquito control pesticides are low and that risks from WN

Idiopathic Environmental Intolerance (IEI) (“idiopathic” meaning of “unknown origin”) is the name currently applied to a phenomenon formerly known as Multiple Chemical Sensitivity (ACOEM 1999). The newer name does not assume a chemical, biochemical, or immunologic cause for the patient’s symptoms and was adopted because there is no medical consensus as to its diagnostic criteria, etiology, or therapy (AAAAI 1999, Poonai et al. 2001). Symptoms are said to be caused by exposure to a wide range of human-made chemicals at doses far below those known to cause toxic effects to humans (ACOEM 1999, Bailer 2005). Symptoms may include weakness, dizziness, headaches, heat intolerance, difficult in concentrating, depressed mood, and memory loss (Pirages and Richard 1999).

IEI is said to be “the only ailment in existence in which the patient defines both the cause and the manifestations of his own condition” (Gots 1995). Many IEI patients self-report allergies to chemicals, but IgE levels have been shown to not support an allergic cause (Bailer et al. 2005). Another study found that IEI patients showed no difference from control subjects in responses to solvents or placebos (Bornschein et al. 2008). Other researchers suggest that IEI patients have an exaggerated response due to hypersensitivity to odors (van Thriel et al. 2008). Currently, IEI is not recognized as an organic disease by the American Academy of Allergy and Immunology, the American Medical Association, the California Medical Association, the American College of Physicians, nor the International Society of Regulatory Toxicology and Pharmacology (Gots 1995).

This notwithstanding, medical research continues to investigate the causes of the phenomenon. Preliminary data indicate that IEI and panic disorder are related and may have a common neurogenetic origin (Poonai et al. 2000, Binkley et al. 2001). Other data indicated that IEI patients may have variant genes that code for altered drug-metabolizing enzymes (McKeown-Eyssen et al. 2004, Schnakenberg et al. 2007). Still other researchers report that IEI appears to be a variant of somatoform disorders, in which psychiatric disorders cause unexplained physical symptoms (e.g., Bailer et al. 2005).

Regardless of the cause of their symptoms, IEI patients can suffer severe disruption of work and daily life (Magill and Suruda 1998). IEI is given credence in regulatory actions, tort liability, and workers compensation claims (Gots 1995). In Florida, private pest control operators are legally required to notify registered persons prior to chemical applications (Chapter 482 F.S.). In addition, FDACS maintains a list of persons who claim to be pesticide-sensitive, requiring a Chapter 9: Mosquito Control Risks and Benefits Page 154 physician’s certification of a health concern, and typically mosquito control offices avoid spraying their residences or notify them prior to spray operations.

The concept of chemical trespass (i.e., applying chemicals to an individual or their property against their wishes) extends back to old Florida statutes. However, statutory law (Chapter 388 F.S.) now permits the application of mosquito control chemicals in the public domain. The potential for conflict is obvious, and this conflict has been the basis for some claims in the past (e.g., by beekeepers).

Adulticide drift, in particular, invites claims of chemical trespass. Mosquito adulticides are not labeled for application to wetlands and most environmentally sensitive publicly owned upland is also off-limits. Because any wind will create drift, mosquito control operators face the difficult task of both hitting their targets and avoiding the adjacent non-target areas. Adulticides have been shown to drift three miles and in some extreme instances up to five miles (Dukes et al. 2004). One study in the Florida Keys found that aerial thermal fog drifted 750 meters (½ mile) into protected no-spray zones which harbored endangered vertebrate and plant species, though no harm was demonstrated (Hennessey and Habeck 1991, Hennessey et al. 1992). Such data may appear to suggest the need for larger buffer areas and/or careful attention to meteorological conditions to fully protect no-spray zones. With the general replacement in Florida of aerial thermal fogging by aerial ULV treatments, some of these concerns may be allayed.

Tietze et al. (1992) and Tietze and Shaffer (1997) documented microscopic damage to automotive paint finishes due to the application of malathion and naled.

Problems resulting from chronic exposure to chemicals are a general public health issue, because everyone is exposed daily to chemical and pesticide residues in food, water, and air. In regard to chronic exposure to chemicals, animal endocrine and immune system dysfunction studies have provided evidence that synthetic pesticides and industrial chemicals in very low quantities, after repeated exposures, may affect these functions (Pimentel and Lehman 1993). Such chronic exposure has been associated both with decreases in human sperm counts and sperm abnormalities. Swan et al. (2003) and Swan (2006) examined effects of pesticides on quality of human semen in the United States. These studies revealed that among men living in agricultural areas exposure to atrazine, alachlor, and diaznon appeared to decrease sperm concentration and motility, whereas exposure to malathion and DEET did not. A documented problem in Lake Apopka believed to be caused by chronic exposure to chemicals, included small genitalia size and sperm abnormalities in male alligators (Colburn et al. 1996). While mosquito control chemicals are not implicated in these instances, they are a part of the total insecticide use picture. It should be noted that organophosphates, such as malathion, have been used routinely for over 40 years in some Florida communities without any documented chronic effects. This lack of documentation should not be misunderstood to be proof of absence of risk, however (Thier 2001). This lack of data may be a detriment to public relations. For example, Petty et al. (1959) observed the development of two extreme points of view regarding the use of organophosphate pesticides in Louisiana. On the one hand were people who were too casual in mixing and applying pesticides. On the other were people so frightened by any use of pesticides that they created “localized hysteria”.

There do not appear to be significant ill effects to humans attributable to longterm, low-level exposure to organophosphate pesticides (WHO 1989, Steenland 1996, Leon-S. et al. 1996, others reviewed by Eskenazi et al. 1999). Insecticides used for mosquito control in Florida have been evaluated for this use by the EPA. They pose minimal risk to human health and the environment when used according to label directions. The EPA estimates that the exposure and risks to adults and children posed by ULV aerial and ground applications of malathion and naled range from 100 to 10,000 times below the quantity of pesticide that might present a health concern (IDPH undated). Lal et al. (2004) examined blood cholinesterase levels of applicators and residents of villages involved in a kalaazar control program in India. These researchers found that blood cholinesterase levels of applicators and villagers decline immediately after treatment of homes with 5% malathion suspension but still were within the normal range of blood cholinesterase levels. One week after application the applicators’ blood cholinesterase levels were still depressed but remained within normal limits. After one year of exposure the villagers’ blood cholinesterase levels had returned to pretreatment levels (Lal et al. 2004). Few data concerning inhalation toxicity of malathion to humans are available, but Culver et al. (1956) and Golz (1959) found no significant health effects beyond nasal irritation.

Beyond the risks to humans and wildlife from pesticide exposure, application procedures may cause problems by promoting pesticide resistance, resulting in the need for increasing doses or new chemicals. In some locations, the widespread use of pesticides by agriculture, homeowners, and mosquito control may have contributed to resistance (Boike et al. 1989). In some geographically distinct areas (i.e., island situations), spraying has helped lead to mosquito resistance to certain chemicals (Reimer et al. 2005). Mosquito populations subject to chemical control operations may be especially vulnerable to development of resistance due to widespread applications of a single pesticide coupled with the short generation time with abundant progeny of the mosquito life cycle (Hemingway and Ranson 2000).

Since it is currently impossible to predict the long-term consequences of human exposure to synthetic compounds, including mosquito control agents, a prudent strategy is for society to reduce all unnecessary chemical applications. For mosquito control, strides have been made in this direction by regulations that allow adulticide applications only after adequate surveillance verifies a nuisance level. Mosquito control and all other industries applying chemicals should use alternative procedures that reduce the need for chemical applications whenever possible. Such actions may result in decreased environmental risks.

Environmental Costs of Adulticiding

In recent years, some politicians, private interest groups, and the general public have become increasingly vocal in their concerns about potential human and environmental hazards associated with the use of chemicals to control mosquitoes, especially aerially applied adulticides (Gratz and Jany 1994). This concern has generated greater accountability by mosquito control operations when applying insecticides, and some tighter environmental restrictions have been implemented at the Federal and State levels. Hopefully in the future, more effective alternative strategies such as biological control agents and non-chemical larvicides will be available for mosquito control. Realistically, however, chemical companies see the mosquito control market as being relatively small and usually not providing adequate economic incentive to allocate the tremendous costs (easily tens of millions of dollars) necessary to develop and receive a label for a new and safer product (Rose 2001).

Non-target Insect Mortality

At times, an adversarial relationship has existed between Florida mosquito control and beekeepers. Bees are very sensitive to organophosphates, and extensive kills from mosquito control have been documented. Acute problems usually include immediate bee kills, but sublethal amounts of organophosphates can also cause a general decline in hive vigor and/or a loss of feeding ability (Atkins 1975). Despite documented cases involving mosquito control, aerial agricultural spraying probably accounts for more bee kills. Bee exposure to ground adulticiding is minimal because treatment is almost always conducted after the evening or before the morning crepuscular periods. However, under certain conditions, aerial adulticiding sometimes occurs while bees are foraging and therefore can be an increased threat.

The incidence of conflicts between beekeepers and mosquito control peaked in the 1980s and has declined in recent years. In some parts of Florida, mosquito control programs are now required to notify beekeepers in advance of spray operations to give the beekeepers the option of covering or moving hives. The impact to honeybees within target areas can be minimized if insecticide deposition on the ground is reduced to below the effect threshold (Zhong et al. 2003, 2004). Improvements in mosquito control equipment also have led to reductions of honeybee mortality (Zhong et al. 2004). In the 1980s, the state distributed to beekeepers a state map depicting where most aerial operations occurred (Sanford 1998). Currently, mosquito control and beekeepers maintain communication about timing of insecticidal treatments. Other pollinators less well known than the honeybee may be impacted by adulticiding. Perhaps 65% of flowering plants depend upon insect pollination, with many plant species relying upon a specific insect species.

In Florida, and particularly in the Florida Keys, there has been controversy regarding the impact of mosquito control on Lepidoptera, especially the Schaus’ swallowtail (Papilio aristodemus ponceanus) and the Miami blue butterfly (Cyclargus thomasi bethunebakeri). Emmel (1991) reported that insect diversity was much lower in areas subjected to mosquito control operations (i.e., Key Largo) compared to areas not exposed to mosquito control (i.e., Elliott Key). Eliazar and Emmel (1991) and Salvato (2001) calculated LD50 values for some mosquito control adulticides against butterfly species. Laboratory analyses are not always reflective of events in the field (Clark 1991, Charbonneau et al. 1994, Blus and Henny 1997). Experiments currently are being conducted in the Florida Keys to determine the impacts of mosquito control operations on the Miami blue butterfly under field conditions. Walker (2001) also suggested that mosquito control was responsible for extirpating a wood cricket (Gryllus cayensis) from the Florida Keys, although he stated he had no proof this was the case.

The impact of adulticides on the nocturnal insect fauna, both flying and nonflying, has not been well documented. One study in California evaluated the effects of aerial application of pyrethrin, malathion, and permethrin on night flying non-target insects. A significant reduction in numbers of non-target insects was observed on the night of the insecticide treatments, but insect numbers had rebounded 24 hours later (Jensen et al. 1999). Non-target impacts could be far beyond what we know. These possible non-target impacts are worthy of further study.

Impacts on Insectivores

Just as the impacts of mosquito adulticiding on non-target insects are not well quantified (Stevenson 1980), the ecological impact from the reduction of mosquitoes is also largely unknown. Nevertheless, it is commonly claimed that mosquitoes play an important role as a food source for larger organisms. Claims include that larvae are an important food for other aquatic organisms, that adults of many mosquito species have an important role in the pollination of plants, and that adults serve as important food sources for birds, bats, and other arthropods, including dragonflies and spiders.

The evidence is lacking for commonly cited species such as Purple Martins (Kale 1968) and bats (Easterla and Whitaker 1972, Vestjens and Hall 1977, Sparks and Valdez 2003). Adults of most mosquito species are not active during the hours that most dragonflies are seeking prey (Pritchard 1964a, Walton 2003). Nevertheless, adult dragonflies will prey on adult mosquitoes when the two are present in the same habitat (Wright 1944a, 1944b; Pritchard 1964a). Analysis of gut contents has revealed that consumption of mosquitoes by dragonflies is greater Chapter 9: Mosquito Control Risks and Benefits Page 158 in the early morning hours; up to 19% of gut contents consisted of mosquitoes (Pritchard 1964a). The importance of mosquito larvae as food for fish, aquatic salamanders, and predatory aquatic insects seems better demonstrated (e.g., Pritchard 1964b, Mathayan et al. 1980, Whiteman et al. 1996, Lundkvist et al. 2003). Boone and Bridges (2003) have pointed out that control measures that reduce population sizes of plankton and aquatic invertebrates can have adverse effects on amphibians due to reduction of available foods.

Fish

Impacts of mosquito adulticides on fish have received considerable attention. Fish may be killed in small streams or ponds where slow flow rates allow pesticide concentrations to increase in excess of toxic levels or where heavy rainfall within a large watershed area allowed high pulse loads to enter small aquatic habitats (EPA 2006). Risk to fish is lower in swiftly flowing streams because pesticides are transported downstream and rapidly diluted (McEwen et al. 1996-2000). Field studies have shown that operational mosquito control applications of pesticides can be of shorter duration and of lesser concentration that those used in worst-case scenarios for environmental risk assessments (Clark 1991). For example, in one field study, application of naled according to label directions did not impact fish (Bearden 1967). Temephos applied at label rates resulted in no adverse impact on bluegill (Sanders et al. 1981). Malathion ground ULV and thermal fog applications presented no acute toxicity to fish (Tagatz et al. 1974). Clark et al. (1989) and Coates et al. (1989) have reviewed the literature pertaining to toxicity of pesticides to aquatic organisms.

Aquatic Crustacea

Aquatic crustaceans – cladocerans, copepods, lobsters, and shrimp – can be impacted by mosquito control adulticides, probably due to their close phylogeny to insects (Clark 1991). Older studies documented effects of fenthion on ostracods and cladocera (Khudairi and Ruber 1974, Ruber 1963). Zulkosky et al. (2005) reported that resmethrin was more toxic to American lobsters (Homarus americanus) than was malathion during 96 hour tests. Operational application of naled according to label directions resulted in no significant mortality of shrimp or crabs (Bearden 1967). Aquatic habitats are avoided operationally to minimize such impacts.

Environmental Costs of Larviciding

Controlling a brood of larval mosquitoes while they are still concentrated in a pool of water is easier, more efficient, and less costly environmentally than controlling dispersed adults. Nevertheless, there still are costs, and they should be recognized and minimized to the extent practicable. Using biorational materials (e.g., Bti, methoprene) minimizes non-target effects because of the specificity of these materials. Nevertheless, research has shown there are short-term effects on nonChapter target insect species when methoprene is used for mosquito larviciding (Hershey et al. 1998). That same study revealed that there was a delayed effect of 2-3 years between initiation of treatment with Bti and evidence of effects on the wetlands food web. Methoprene can affect copepods, crabs, and shrimp, although effects generally are seen at concentrations higher than those of operational rates (Miura and Takahashi 1973, McAlonan et al. 1976, Christiansen et al. 1977, Bircher and Ruber 1988). A review of 75 studies of non-target effects of Bti, concerning nearly 125 families, 300 genera, and 400 species is available (Boisvert and Boisvert 2000). Most research on the use of monomolecular films to control larvae or pupae has shown that there is little or no effect on non-target organisms (reviewed by Stark 2005). However, Takahashi et al. (1984) observed mortality of aquatic Hemiptera (Corixidae, Notonectidae), Coleoptera (Hydrophilidae), and clam shrimp (Limnadiidae) in field trials of Arosurf®. Regarding the loss of mosquitoes as important prey, in the case of methoprene, since mortality generally occurs during the pupal stage, larvae remain as a prey source. Nevertheless, the reduction of the huge biomass of saltmarsh mosquitoes (potentially many millions of larvae per acre) must be significant to some aquatic predators. Nielsen and Nielsen (1953), for example, described the voracious consumption of Ae. taeniorhynchus larvae by minnows and water beetle larvae. The loss may be mitigated by some species, however (Harrington and Harrington 1961, 1982) have shown that a few species of fish are capable of dietary shifts following impoundment when mosquito broods were lost as a food source.

Adulticiding versus Larviciding

Both larvicide and adulticide chemicals may impact non-target species, although it is widely accepted that larvicides have less environmental impact than adulticides. Larvicides can be quite target specific (e.g., Bti, methoprene) and are used in specific habitats and under certain conditions. Adulticides, on the other hand, are more broadly distributed by truck or aircraft, thus impacting both the target area and potentially other nearby areas through drift and run-off. Such movement is a problem when the insecticide enters wetlands or public lands where they are not allowed. All mosquito control programs should continue to concentrate their efforts on developing effective larval surveillance and control programs in order to effectively minimize the need for adulticiding.

All industries need to continually review and improve their operations. Mosquito control is no exception. When larval or adult control has not worked effectively, a thorough assessment should be conducted so the program can be improved. Larval control will usually allow some mosquitoes to emerge, mostly due to the inspection program's failure to identify a mosquito brood or to implement thorough treatment coverage. Likewise, adulticiding is by no means 100% effective. An education program to inform the public that at least some mosquitoes are to be expected in Florida is warranted.

SOURCE REDUCTION

Achieving permanent mosquito control by eliminating mosquito larval habitats is called source reduction. It ranges from efforts as simple as collecting discarded tires to long-term habitat altering measures. Several source reduction techniques for saltmarsh mosquito control are presently used. For more information about source reduction, see Chapter 4.

Ditching is a strategy whereby mosquito producing depressions of tidal water or rainfall are engineered to drain and larvivorous fish are allowed access. Ditching is most effective where daily tides flush the potential mosquito oviposition sites on the marsh. Ditching can increase tidal flushing of soils, increase oxygen availability to plants, reduce soil salinity, and contribute to increased primary productivity of salt marsh plants. It also can increase fish diversity within the marsh and can provide additional habitat for birds (Anonymous 1990, Resh and Balling 2003). The environmental costs of ditching include creation of permanent scars on the marsh and adverse effects on natural hydrology and biological productivity. Ditching historically has created berms which allow encroachment of woody, often exotic, vegetation. While ditching can be effective for mosquito control, it also can create larval habitat for biting midges (Culicoides spp.), insects which are difficult to control and frequently are perceived as being much more annoying than mosquitoes.

Impounding became popular along the Indian River Lagoon in the 1950s and 1960s when earthen dikes were built around approximately 42,000 acres of high salt marsh to allow for their seasonal flooding. This technique became the most effective and economically feasible approach to saltmarsh mosquito control on Florida's central east coast. Although early impounding efforts greatly decreased the need for adulticiding and virtually eliminated the need to larvicide, the environmental consequences included high mortality of the native marsh vegetation and the isolation of thousands of acres of salt marsh. These habitats are critical for the development of many important marine species (e.g., fish, crustaceans, mollusks), and their loss negatively affected the multibillion dollar commercial and recreational fishery. Despite these impacts, high saltmarsh impoundments have provided good feeding opportunities for ducks and wading birds (Provost 1959, 1969), although some use of these impoundments may be due to loss of habitat elsewhere (e.g., loss in the Kissimmee River and St. Johns River flood plains due to human development and drainage).

Unintentional effects of source reduction practices have included: changes in plant composition and abundance that affect their value as forage or shelter, changes in animal diversity and abundance which alter the food web, changes in competitive relationships between predators and prey, and increased susceptibility to disease and parasitism. An extreme example of unintentional pesticide impacts is that the use of some agricultural chemicals has altered entire ecosystems, resulting in freshwater eutrophication.

Since the early 1980s scientific research has identified improved water management techniques that reintegrate impounded marshes with the estuary. This reconnection restores many natural marsh functions while still controlling mosquito populations with a minimum of pesticide use. There are two salt marsh management techniques which best accomplish these desirable goals, and they have been aggressively implemented by mosquito control agencies: Rotational Impoundment Management (RIM) and Open Marsh Water Management (OMWM), typically utilizing rotary ditching (Carlson 2006).

MOSQUITO CONTROL ON BIOLOGICALLY PRODUCTIVE STATE-OWNED LANDS

Florida public land management agencies generally believe that any external influence that potentially threatens the flora, fauna, or natural systems under their management must be considered with caution. For example, although pest control once was a priority in Florida’s parks (e.g., Provost 1952), park managers now pursue an ecosystem management approach that considers the well-being of entire biological communities (e.g., Stevenson 1991). Chapter 388.4111 F.S. mandates that public lands may be designated by their managers to be “environmentally sensitive and biologically highly productive”. Once declared, and where such lands have public health or nuisance levels of mosquitoes, their mosquito control activities are conducted according to a special “public lands arthropod control plan”. The plan is written by mutual agreement between the agency and the mosquito control program to authorize activities that are the minimum necessary and economically feasible to abate the health or nuisance problem and impose the least hazard to fish, wildlife, and other natural resources. Since adulticiding is not highly selective and non-target species can be adversely affected, state land managers generally believe adulticiding is contrary to the legislative mandate to protect environmentally sensitive and biologically productive state lands. Other control methods, ideally biological controls (e.g., Gambusia spp. for larval control) or larviciding with Bti or methoprene, which are mostly target-specific, are usually acceptable to the agencies. Allowing these practices on most properties is viewed by the state as a reasonable compromise for adhering to the legislative mandates regarding public land protection and mosquito control.

MUTUAL ACCOMMODATION

The effects of pesticides on target and non-target organisms, wildlife, soil, and water can both benefit and negatively impact Florida's quality of life. Both mosquito control and the protection of environmentally sensitive habitats in Florida are legislatively mandated, needed, and important to the state. Indeed, they need not be mutually exclusive goals (e.g., O’Bryan et al. 1990, Batzer and Resh 1992). Because the selection of chemicals available for both larviciding and adulticiding is becoming increasingly limited without many new products in development, and because of the possibility of non-target insecticide effects, it is incumbent that mosquito control pesticides be applied wisely in integrated pest management programs. It is also important that new, more environmentally acceptable methods are developed, tested, and used as they become available, and that research continues to document non-target and human health effects of the pesticides used. The American Public Health Association has noted, “debates over the use of pesticides for public health vector control have sometimes divided the public health and environmental communities … at a time when maximizing public health and environmental protection requires close coordination and mutual trust between those communities” (APHA 2001). Continued dialogue between mosquito control and environmental resource agencies is necessary to make certain that mosquito control minimizes all its adverse

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