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North American Wetlands and Mosquito Control
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Title: North American Wetlands and Mosquito Control
Series Title: Int. J. Environ. Res. Public Health 2012, 9(12), 4537-4605; doi:10.3390/ijerph9124537
Physical Description: Journal Article
Creator: Rey, Jorge
Publisher: MDPI
Place of Publication: Basel, Switzerland
Publication Date: December 2012
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Abstract: Wetlands are valuable habitats that provide important social, economic, and ecological services such as flood control, water quality improvement, carbon sequestration, pollutant removal, and primary/secondary production export to terrestrial and aquatic food chains. There is disagreement about the need for mosquito control in wetlands and about the techniques utilized for mosquito abatement and their impacts upon wetlands ecosystems. Mosquito control in wetlands is a complex issue influenced by numerous factors, including many hard to quantify elements such as human perceptions, cultural predispositions, and political climate. In spite of considerable progress during the last decades, habitat protection and environmentally sound habitat management still remain inextricably tied to politics and economics. Furthermore, the connections are often complex, and occur at several levels, ranging from local businesses and politicians, to national governments and multinational institutions. Education is the key to lasting wetlands conservation. Integrated mosquito abatement strategies incorporate many approaches and practicable options, as described herein, and need to be well-defined, effective, and ecologically and economically sound for the wetland type and for the mosquito species of concern. The approach will certainly differ in response to disease outbreaks caused by mosquito-vectored pathogens versus quality of life issues caused by nuisance-biting mosquitoes. In this contribution, we provide an overview of the ecological setting and context for mosquito control in wetlands, present pertinent information on wetlands mosquitoes, review the mosquito abatement options available for current wetlands managers and mosquito control professionals, and outline some necessary considerations when devising mosquito control strategies. Although the emphasis is on North American wetlands, most of the material is applicable to wetlands everywhere.
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Publication Status: Published
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Source Institution: University of Florida Institutional Repository
Holding Location: University of Florida
Rights Management: All rights reserved by the submitter.
System ID: IR00001355:00001

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Int. J. Environ. Res. Public Health 2012 9 4537-4605; doi:10.3390/ijerph9124537 International Journal of Environmental Research and Public Health ISSN 1660-4601 www.mdpi.com/journal/ijerph Article North American Wetlands and Mosquito Control Jorge R. Rey 1,*, William E. Walton 2, Roger J. Wolfe 3, C. Roxanne Connelly 1, Sheila M. O’Connell 1, Joe Berg 4, Gabrielle E. Sakolsky-Hoopes 5 and Aimlee D. Laderman 6 1 Florida Medical Entomology Laboratory and De partment of Entomology and Nematology, University of Florida-IFAS, Vero Beach, FL 342962, USA; E-Mails: crr@ufl.edu (R.C.); sheilao@ufl.edu (S.M.O.C.) 2 Department of Entomology, University of California, Riverside, CA 92521, USA; E-Mail: walton@ucr.edu 3 Connecticut Department of Energy and Enviro nmental Protection, Franklin, CT 06254, USA; E-Mail: roger.wolfe@ct.gov 4 Biohabitats, Inc., 2081 Clipper Park Road, Baltimore, MD 21211, USA; E-Mail: jberg@biohabitats.com 5 Cape Cod Mosquito Control Projec t, Yarmouth Port, MA 02675, USA; E-Mail: gsakolsky@aol.com 6 Marine Biological Laboratory, Woods Hole MA 02543, USA; E-Mail: aladerman@gmail.com Author to whom correspondence should be addressed; E-Mail: jrey@ufl.edu; Tel.: +1-772-778-7200 ext 136. Received: 11 September 2012; in revised form : 21 November 2012 / Accepted: 22 November 2012 / Published: 10 December 2012 Abstract: Wetlands are valuable hab itats that provide importa nt social, economic, and ecological services such as flood control, water quality improvement, carbon sequestration, pollutant removal, and primary/secondary prod uction export to terrestr ial and aquatic food chains. There is disagreement about the need for mosquito control in wetlands and about the techniques utilized for mosquito abatement and their impacts upon wetlands ecosystems. Mosquito control in wetlands is a complex issue influenced by numerous factors, including many hard to quantify el ements such as human perceptions, cultural predispositions, and political climate. In sp ite of considerable progress during the last decades, habitat protection and environmenta lly sound habitat management still remain inextricably tied to politics and economics. Furthermore, the connections are often complex, and occur at several levels, ranging from local businesse s and politicians, to OPEN ACCESS

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Int. J. Environ. Res. Public Health 2012 9 4538 national governments and multinational institutions. Education is the key to lasting wetlands conservation. Integr ated mosquito abatement st rategies incorporate many approaches and practicable opt ions, as described herein, a nd need to be well-defined, effective, and ecologically and economically sound for the wetland type and for the mosquito species of concern. The approach will certainly di ffer in response to disease outbreaks caused by mosquito-vectored pathogen s versus quality of life issues caused by nuisance-biting mosquitoes. In this contributio n, we provide an overview of the ecological setting and context for mosquito control in wetlands, present pertinent information on wetlands mosquitoes, review the mosquito abatement options available for current wetlands managers and mosquito control professionals, and outline some necessary considerations when devising mosquito c ontrol strategies. Although the emphasis is on North American wetlands, most of the materi al is applicable to wetlands everywhere. Keywords: arbovirus; marsh; mangrove; mosquito control; surveillance; wetland Acronyms BMP = Best Management Practices Bti = Bacillus thuringensis var. israelensis EEE = Eastern Equine Encephalitis FIFRA = Federal Insecticide, Fungicide, and Rodenticide Act FWS = Free Water Surface USFWS = U.S. Fish and Wildlife Service IGR = Insect Growth Regulator IMM = Integrated Mo squito Management IPN = Integrated Pest Management Ls = Lysinibacillus sphaericus MMF = Monomolecular Film NOI = Notice of Intent NPDES = National Pollutant Discharge Elimination System OMWM = Open Marsh Water Management PNW = Pacific Northwest RIM = Rotational Impoundment Management RRV = Ross River Virus SLE = St. Louis Encephalitis SSF = Sub-surface Flow ULV = Ultra-low Volume VEE = Venezuelan Encephalitis WEE = Western Equine Encephalitis WN = West Nile WNV = West Nile Virus

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Int. J. Environ. Res. Public Health 2012 9 4539 1. Introduction Wetlands are valuable habitats that provide important social, economic, and ecological services such as flood control, water quality improvement, carbon sequest ration, pollutant removal, and primary/secondary production export to terrestrial and a quatic food chains. They represent important habitats for a large number of anim al and plant species, some of whic h are threatened or endangered. Wetlands protect adjacent habitats from erosive fo rces, and have important flood control and water storage functions. Wetlands also ha ve high aesthetic and recreationa l value which makes neighboring areas highly desirable for human habitation. Howe ver, wetlands are also natural producers of mosquitoes and this sometimes creat es conflicts with human neighbors. Most frequently, wetlands mosquito production is a “nuisance” issue, affecti ng the quality of life of nearby residents by instigating ge nerally undesired behaviors. Ex amples include postponement or cancellation of pleasurable activitie s such as hikes, picnics, and other forms of outdoor recreation; necessity to apply repellent while outdoors; or si mply having to endure uncomfortable and irritating mosquito bites during the course of normal or extracurricular activities. Large biting mosquito populations can sometimes also have social, cultu ral, and economic impacts by limiting community activities. Examples include cancellation of, or reduced attendance to revenue-generating activities such as concerts and sporting events; drops in t ourism; and reduction in outdoor activities that drive local economies and support local me rchants (e.g., hunting, fishing, hiking, etc. ) [1–3]. Mosquitoes can have grave health impacts on th e population at large when mosquito-transmitted pathogens such as West Nile virus, eastern equine encep halitis virus, and Plasmodium spp. (the causative agent of malaria) are being amplified and transmitted locally. Mosqu itoes can also routinely have serious health impacts on individuals with allergies to mosquito bites [4]. Severe reactions to mosquito bites can be local or systemic and can cau se tissue necrosis, urtic aria, inflammation of the mucous membranes, fever, lowering of blood pressu re, loss of consciousness an d other sympto ms [5,6]. Mosquitoes can also have significant health impact s on wildlife, livestock, and pets including wild birds, cattle, dogs, and horses [7,8]. There is disagreement about the need for mosquito control in wetlands and about the techniques utilized for mosquito abatement and their imp acts upon wetlands ecosystems. For example, some authors [9] consider permanent and semi-permanent source reduction techniques to be suitable only for wetlands already heavily impacted by human activiti es or for intensely managed wetlands, whereas others consider some of these techniques to be a form of marsh restorat ion [10,11]. Furthermore, public misconceptions abound about the role of wetla nds in local mosquito production and disease transmission, and on the ecological impacts of pa rticular mosquito cont rol activities even though published research does not support such misconceptions. There is often a lack of inform ation on wetlands ecology and manage ment in the mosquito control literature, but the opposite is also true; informa tion on mosquitoes, mosquito-borne pathogens, and mosquito control technology is al so lacking in the wetlands, c onservation, restoration, and wetlands/water management literature [12]. In fact, ev en the wetlands literature is often fragmented by wetlands types (e.g., freshwater swamps vs. coastal wetlands), with few insights forthcoming from patterns and processes common to many wetland types [13] We consider this situation to be a critical

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Int. J. Environ. Res. Public Health 2012 9 4540 shortcoming in our ability to deal with wetlands mosquito produc tion in an effective and ecologically sound manner. In this contribution, we provide an overview of the ecological setting and context for mosquito control in wetlands, present pertinent informatio n on wetlands mosquitoes, review the mosquito abatement options available for current wetlands managers and mosquito control professionals, and outline some necessary considerations when devisi ng mosquito control strategies. We also provide relevant literature for wetlands practitioners and mosquito control/public health personnel and discuss pressing research needs. We encourage research on ecologically-sound mosquito abatement techniques and on strategies and policies that further the above goal. 2. Types of Wetlands Below, we briefly describe the major types of we tlands in North America to establish the context and scope of mosquito control-wetlands issues (Table 1). It is important to note that many variations for a particular wetland “type” occur and that in r eality, no two wetlands are exactly alike. It is not possible to cover every single wetl and type [13], but we expect that most, including many highly localized types can be included as subtypes of the wetlands listed here. Figure 1 shows the general location of some of these wetlands. There are seve ral excellent references that offer more detailed discussion on the different wetland types. Included among these are: Mitsch and Gosselink [13], Batzer and Sharitz [14], Perillo et al [15], Batzer and Bald win [16]. Sub-tidal areas such as seagrass beds and high energy coastlines are not included b ecause they normally do not provide suitable larval habitats for mosquitoes. Table 1. Summary of wetland types discussed in the text. Type USFWS 1 classification Major hydrologic influence Flooding frequency Mangrove Estuarine forested/shrub ocean tide daily-seasonal Tidal salt marsh Estuarine intertidal emergent ocean tide daily-seasonal Pacific Northwest tidal wetland Estuarine intertidal emergent ocean tide daily-seasonal Tidal brackish marsh Estuarine intertidal emergent tide/surface daily-seasonal Tidal freshwater wetland Palustrine emergent surface daily-seasonal Bottomland swamp Palustrine emergent/ forested river, precipitation, ground semi-permanent Atlantic white cedar wetland forest Palustrine emergent/ forested precipitation, ground seasonal 2 Riverine riparian floodplain wetland Palustrine emergent/ forested river, precipitation, variable Wet meadow Palustrine emergent ground seasonal Wet prairie Palustrine emergent ground permanent, semi-permanent 2 Playa Palustrine emergent surface seasonal Bog Palustrine shrub precipitation/runoff variable/seasonal2 Pocosin Palustrine shrub ground semi-permanent2 Fen Palustrine shrub ground semi-permanent2

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Int. J. Environ. Res. Public Health 2012 9 4541 Table 1. Cont. Type USFWS 1 classification Major hydrologic influence Flooding frequency Carolina Bay Palustrine shrub preci pitation/ground permanent-seasonal Pothole Pond natural precipitation variable Vernal pool Pond natural precipitation seasonal Mississippi deltaic plain wetlands Mixed various variable Everglades Mixed various variable Constructed wetlands Mixed permanent 1 U.S. Fish and Wildlife Service; 2 Includes saturated surface with or without standing water. 2.1. Coastal Wetlands Coastal wetlands include a variety of ecosystems in fluenced in some way by ocean tides. Here we consider mangrove forests, tidal salt marshes, Paci fic Northwest tidal wetlands tidal brackish marshes, and tidal freshwater wetlands. Wolanski et al. [17] estimate worldwide coverage of mangroves, and freshwater wetlands to be 230,000 and 300,000 km2, respectively. North American salt marsh cover is close to 300,000 km2 [13]. These ecosystems are particularly vulnerable to human impacts because of the desirability of the habitat for human habitation a nd also to effects of sea level changes due to their geographic location. 2.1.1. Mangroves The term mangrove refers to assemb lages of tropical trees and shrubs that grow in the intertidal zone. It is a non-taxonomic term used to describe a diverse group of pl ants that share certain ecological characteristics including adaptation to wet salin e habitats. Terms such as mangrove community, mangrove forest, mangrove swamp, mangrove wetla nd, and mangal are used interchangeably to describe the entire mangrove community. They occu r worldwide along tropical and subtropical coasts, in areas with unconsolidated sedime nts and low to moderate wave ac tion [18]. In the United States (U.S.) mangroves are found principally in Florida south of 30N latitude, predominantly in the Florida Keys, southwest Florida, and southeast/east-centr al Florida (Figure 1). As with other coastal vegetation, mangal hydrology is pr imarily influenced by tides [1 8]. Freshwater inputs from precipitation and upland runoff can be important and can play important roles in modifying salinity regimes, nutrient cycling, and flushing [19]. Worldwide there are approximately 40 to 50 species of mangroves distributed among 15–16 families of plants. Three mangrove species occu r in Florida: the red mangrove ( Rhizophora mangle ), the black mangrove ( Avicennia germinans ), and the white mangrove ( Laguncularia racemosa ). A variety of herbaceous halophytes often occupy the mangrove understory. Examples include Spartina alterniflora Batis maritima Salicornia virginica and Distichlis spicata.

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Int. J. Environ. Res. Public Health 2012 9 4542 Figure 1. Map showing the distribution of some of the wetlands types disc ussed in the paper. Outlines show general location and not actu al coverage. ( A) North America; ( B) United States East Coast north of Florida (approximately 30.5N lat.).

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Int. J. Environ. Res. Public Health 2012 9 4543 Figure 1. Cont.

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Int. J. Environ. Res. Public Health 2012 9 4544 Mangrove forests serve as important perman ent habitat, and as foraging, refuge, and breeding/nursery habitat for a large number of te rrestrial and aquatic orga nisms including several threatened or endangered species. Many of these sp ecies are highly valued by sports and commercial fisheries, inshore and offshore. Marine inverteb rates such as crustaceans, mollusks, and worms, terrestrial invertebrates (insec ts and arachnids), reptiles (e.g., the American crocodile, Crocodylus acutus ), and a multitude of birds are co mmon in mangrove forests. Many important fish species such as snapper ( Lutjanus spp.) and tarpon ( Megalops atlanticus ) depend on these areas during part of their life cycle. Mammals known to frequent mangrove areas include the West Indian Manatee ( Trichechus manatus ) and the endangered Florida Key Deer ( Odocoileus virgininaus clavium ). Mangroves are well known for their high primary production and are extremely important for nutrient dynamics of adjoining estu aries. Although the role of ma ngroves as contributing to “land building” is doubtful, mangroves do serve as barrie rs to shoreline erosi on, and help to stabilize sediments thus reducing the effects of storm surg es and heavy surf. Mangroves also help improve water quality by extracting excess nutrients and by facilitating the detoxification and storage of pollutants in the sediments. Mang roves are prime areas for outdoor recreational activities such as fishing, boating, sightseeing, wildlife observation, and many others. Human impacts have resulted in major losses of mangrove habitat [19] Major impacts worldwide include clearing for residential, industrial, and commercial development; agriculture and charcoal production; salt extraction; and others. Pollution related to human deve lopment (residential; commercial, including tourism; and industrial), and n earby agriculture has also resulted in significant loss and degradation of mangrove habitats. Mangrove wetlands can produce significant numbers of mosquitoes and because of topography and tidal phenomena a large proportion of the mangrove acreage in Florida is suitable for mosquito production [20,21]. For example, Carlson and Viglia no [22] report that 12 mosquito broods were produced during a mosquito season from a si ngle quadrat (of unknown size) in an impounded mangrove wetland in Florida, with brood sizes of up to 349 immature mosquitoes per 350 mL sample. The primary mosquito species is the black salt marsh mosquito Aedes taeniorhynchus This species is an aggressive biter and a strong flier, with potenti al impacts 30 km from the mangrove forests [23] and as far as 90 km under ideal conditions [24]. The species bites during both da y and night and is an important vector of canine heartworm ( Dirofilaria immitis ) and Venezuelan encephalitis [25,26]. Aedes taeniorhynchus can transmit eastern equine and St. L ouis encephalitis [27,2 8], and West Nile virus [28] but it has never been implicated as a major vector of these diseases in Nature. Aedes sollicitans Culex nigripalpus, and Culex salinarius are infrequently coll ected in the less saline (brackish) sections of mangals (e.g., [22]). 2.1.2. Tidal Salt Marshes Tidal salt marshes are coastal wetl ands that are regularly influen ced by ocean tides. In very broad terms they can be divided into low salt marsh, whic h is influenced by daily tides, and high salt marsh, that is only flooded by spring tides and/or seasonal high tides. The hi gh marsh is the most important habitat for mosquito production as the frequent inunda tion of low marshes usually prevents significant mosquito production from these area s [29]. Although these habitats can occur directly in front of open

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Int. J. Environ. Res. Public Health 2012 9 4545 ocean when the wave energy is low (for example al ong the Gulf of Mexico co ast), they more often occur behind protective barrier islands [13]. Ma ny intertidal marshes have very high primary production [10] that is exported directly or as s econdary production [30] to adjoining estuaries and coastal areas and supports marine and estuarine food webs. Marshes provide a va riety of other services including flood control, water stor age, erosion prevention, water qua lity enhancement and recreation. In North America they are most abundant on the Atlantic Coast from Ma ine to Florida and along the Gulf Coast (Figure 1). Limited bands of salt marshes occur in Southern California and along the Pacific Northwest Coast (see below), expanding again along the coast of Alaska. In Florida, coastal salt marshes are gradually replaced by mangroves belo w 30N latitude, but narrow spits of salt marsh can be found throughout the State. H ydroperiod is greatly influenced by the local tidal regime, with extensive tidal penetration with high amplitude luna r tides such as occur in regions of the Atlantic Coast of North America, to irre gular low amplitude flooding by wind ge nerated tides in the Gulf Coast and protected estuaries such as the Indian Ri ver Lagoon in Florida. Although ocean tides are the predominant hydrological influence, the balance betw een tidal and freshwater inflows is critical in determining marsh charact eristics and function. Above 30N latitude on the Atlantic Coast, th ese marshes are usually dominated by halophytic grasses, rushes and succulents including several Spartina species particularly smooth cordgrass, ( Spartina alterniflora ) and saltmeadow cordgrass ( S. patens ), saltwort ( Batis maritima ), glasswort, ( Salicornia bigelovii, Sarcocornia perennis ), salt grass ( Distichlis spicata ), saltmeadow rush ( Juncus gerardi ) and black needle rush ( J. roemerianus ) and many others. Several sh rubby halophytes can also be found at the higher elevations of these marshes such as the upland edges and on top of natural or artificial berms and levees [31].These include groundsel, Baccharis halimifolia ; marsh elder, Iva frutescens ; and wax myrtle, Myrica cerifera Although the Pacific coast of Nort h America is noted for its nearby mountains, steep bluffs, and rocky shores, many small, semi-isolated coastal salt marshes occur along river valleys, particularly south of Point Conception approx. 3426.7'N, 12028.3' W; [32] (Figure 1). In these coastal wetlands, Spartina foliosa predominates in the low mars h and various succulents (e.g., Salicornia spp.) and other herbaceous species such as salt grass ( Distichlis spicata ) in the high marsh [ 32]. Other common S. California marsh species include sa ltwort, glasswort, marsh jaumea ( Jaumea carnosa ), California seablite ( Suaeda californica ), and many others. Pacific Northwes t coastal wetlands are described below. As with mangrove forests, tidal salt marshes are essential foraging and nurse ry habitats for a great number of marine and estuarine species, including some of high commercial and/or recreational value such as snook ( Centropomus undecimalis ), tarpon ( Elops saurus ), and mullet ( Mugil spp.). Many salt marsh areas along all North American coasts are extr emely important habitat for waterfowl, shore and migratory birds [33] including many high priority sp ecies such as the salt marsh sharp-tailed sparrow ( Ammodramus caudacutus ), clapper rail ( Rallus longirostris ), and the roseate spoonbill ( Platalea ajaja ). In addition to a multitude of marine invert ebrates, tidal wetlands are home to numerous terrestrial vertebrates including turtles, frog, snakes, alligators; and mammals such as deer ( Odocoileus virginianus ), raccoon ( Procyon lotor ), otters ( Enhydra lutris ) dolphins ( Tursiops spp.), manatees ( Trichechus manatus ) and others [34,35].

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Int. J. Environ. Res. Public Health 2012 9 4546 More than half of the historic salt marsh habitat of the United States has been lost, in great part due to human activities [36]. Major environmental impacts to coastal salt marshes are related to residential, agricultural, and industrial development and include direct habitat loss, habitat fragmentation, and contamination. Eutrophication-related problem s such as noxious algal blooms and hypoxia are becoming more prevalent, particular ly in the southern regions [34] and modification of freshwater flow and sediments by ditching, diking, and channelizat ion of rivers have seve rely impacted coastal wetlands, particularly in the Gulf region [37]. Many salt marshes can also produce vast numbers of mosquitoes. For example, James-Pirri et al. [38] report larval densities of up to 130 per 350 mL dip in New Jersey (USA) marshes already grid ditched for mosquito cont rol, and in California coastal wetlands, more than 10,000 adult California salt marsh mosquitoes, Aedes squamiger have been collected in a single night in one Fay trap [39]. Th e major salt marsh mosquito species in the Atlantic and Gulf Coasts include the tan salt marsh mosquito Aedes sollicitans the black salt marsh mosquito Aedes taeniorhynchus and the more northern brown salt marsh mosquito Aedes cantator Along the Pacific Coast, the California salt marsh mo squito and the summer salt marsh mosquito Aedes dorsalis predominate. The Florida SLE (St. Louis Encephalitis) vector Culex nigripalpus and the un-banded salt marsh mosquito Culex salinarius may occur infrequently along th e brackish upper marsh borders of the Atlantic and Gulf coasts whereas the winter marsh mosquito Culiseta inornata and Culex tarsalis (another encephalitis virus v ector) can occur in the same gene ral locations along the Atlantic, Gulf, and Pacific Coasts. 2.1.3. Pacific Northwest Tidal Wetlands Pacific Northwest (PNW) tidal wetl ands (including norther n California) occur in a geologically and topographically diverse area. The usually steep topogr aphy of this area pres ents a limited range for these wetlands [40], and re sults in a large number of small isol ated or semi-isolated estuaries and coastal wetlands (Figure 1). Due to the hydrological forc es that create them, i ndividual wetlands in the region have unique characteristics that vary by es tuary type and landscape, although there are still some basic common characteristics [41]. In addition to the direct tidal influence, the mars hes in the major watersheds in the Pacific NW are heavily influenced by the discharge plumes of asso ciated river systems For example, Puget Sound with discharges from the Nooksack, Dungeness, and Elwha Rivers, Willapa Bay from the Bone, Niawiakum, Palix Naselle, Bear, and Willapa rivers; and most of the northern region from the plume of the Columbia River. Additi onally, precipitation in the area can vary significantly with annual amounts generally increasing from south to north, but w ith considerable local va riation associated with local characteristics such as mountain rain shadows [42]. In general, low marshes are dominated by halophytic succulents such as Salicornia virginica Jaumea carnosa and Triglochin maritima as well as several grasses and sedges such as Distichlis spicata and Lyngbye’s sedge Carex lyngbyei Tufted hairgrass ( Deschampsia caespitosa ) commonly dominates in high marshes, accompanied by mixes of many other species incl uding Pacific silverweed ( Argentina egedii ) and Baltic rush ( Juncus arcticus var. balticus ). In some areas fr esh water-influenced systems may have extensive communities of softstem and/or hardstem bulrush ( Schoenoplectus tabernaemontani and S. acutus ) [41].

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Int. J. Environ. Res. Public Health 2012 9 4547 The once common Pacific NW tidal forested wetlands are now rare due to anthropogenic impacts. Major tree/shrub species in the remaining areas include Sitka spruce ( Picea sitchensis ), black twinberry ( Lonicera involucrata ), and Pacific crabapple ( Malus fusca) with alder ( Alnus rubra ), willows ( Salix spp.), Douglas spiraea ( Spiraea douglasii ), and colonial dogwood ( Cornus sericea ) often found in freshwater influenced areas. PNW tidal wetlands support diverse coastal wetland fi sh and invertebrate communities. Of special importance in this area are anadrom ous salmonids such as steelhead ( Onchorhynchus mykyss ) and various salmon species including Chinook ( O. tshawsytscha ), chum ( O. keta ), coho ( O. kisutch ), and pink ( O. gorbusha ) which use coastal wetlands during parts of their life cycle. These wetlands also provide habitat for numerous waterfowl, shorebirds rail, including the enda ngered California clapper rail ( Rallus longirostris obsoletus ) and numerous raptors such as northern harriers ( Circus cyaneus ) osprey ( Pandion haliaetus ) and bald eagles ( Haliaeetus leucocephalus). PNW tidal marshes occur along the Pacific Flyway and includ e many important Flyway sites su ch as Morro Bay, San Francisco Bay, and Padilla Bay [42]. Mammals regularly utilizing these wetlands range from mice and shrew to North American elk ( Corvus elaphus ). Coastal wetlands of the Pacific NW have been extensively modified. For example, within California, close to 90% of historical coastal wetlands have been lost [43], Puget So und has lost 70 to 80% of its estuarine marshes, and close to 70% of the Columbia Rive r Estuary tidal wetlands no longer exist [42]. Approximately 94% and 77% of fore sted wetland losses had been reported by [44]. Land conversion for development, industry, and ag riculture has eliminat ed many hectares of productive wetlands and has resulted in subsidence, contamination, and degr adation of many others. Modification to reduce flooding and lower salinities (diking, ditching, culverts and tide gates) have changed the character of much of the remaining acr eage. Common mosquitoes in this habitat include Aedes squamiger and Aedes dorsalis 2.1.4. Tidal Brackish Marshes Tidal brackish marshes form a transition between sa lt marshes and tidal freshwater marshes. They are found along all coasts and occur ups tream of the salt marsh proper or at the mouth of coastal rivers with high freshwater discharge. There is often a gr adation of marsh types with salinity, from salt marshes at the coast to freshwater tidal wetlands upland. Some classification systems divide brackish tidal marshes into oligohaline (less than 5 ppt salin ity) and mesohaline (less than 18 ppt salinity). Tidal brackish marshes are only irregularly flooded by tid al waters and receive considerable fresh water inputs from rivers and str eams, and overland runoff. Although they share many plant specie s with the tidal salt marshes, brackish marshes tend to have higher plant diversity and lower species dominan ce, although localized monos pecific vegetation stands are common. Depending upon location, characteristic plants may include saltmeadow cordgrass ( Spartina patens ), salt grass ( Distichlis spicata ), black needlerush ( Juncus roemerianus ) or saltmeadow rush ( Juncus gerardi ), chairmaker’s bullrush ( Schoenoplectus americanus ), salt marsh bulrush ( S. robustus ), dwarf spikesedge (Eleocharis parvula ), seashore paspalum ( Paspalum vaginatum ), coastal water hyssop ( Bacopa monnieri ) saltbushes ( Atriplex spp.), threesquare bulrush ( Schoenoplectus pungens ), big cordgrasss ( Spartina cynosuroides ) and cattails ( Typha spp.). In West

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Int. J. Environ. Res. Public Health 2012 9 4548 Coast brackish marshes Typha spp. Schoenoplectus acutus (= Scirpus acutus ), Atriplex prostrata (= Atriplex triangularis ) and Phragmites spp. often dominate. Tidal brackish marshes are very important hab itats for immature forms of many marine and estuarine organisms. On the mesohaline end, brackis h marshes provide excelle nt habitat to typical estuarine animals such as blue crabs ( Callinectes sapidus ), redfish ( Sciaenops ocellatus ), spotted seatrout ( Cynoscion nebulosus ), fiddler crabs ( Uca spp.), and many others. Ne ar the oligohaline end, one finds species more typical of the freshwater marshes (see below). Because of the irregular flooding, brackish marshe s can also be significant mosquito producers. Depending on the location on the marsh, mosquitoes normally found in salt marshes such as Aedes taeniorhynchus A. sollicitans and Culex salinarius and others more typical of fresh water areas including several Culex Anopheles and Psorophora species can be produced. 2.1.5. Tidal Freshwater Wetlands Tidal freshwater wetlands occur at the head of tide in co astal areas. Salinity is less than 0.5 ppt, the flora and fauna are dominated by freshwater species, and they experience re gular tidal fluctuations. Historically, the greatest expanses of tidal freshw ater wetlands in North America occurred in the Atlantic coast between Georgia and New England [45] except where tidal amplitude is small such as estuaries protected by extensive ba rrier islands such as the Outer Banks of North Carolina. Steep, rocky coastlines in northern New England and Canada do not favor the development of extensive marshes, so in this area they te nd to be small and isol ated except for some la rge marshes along the St. Lawrence River watershed. Similar geomorphologica l conditions result in few tidal freshwater marshes along the Pacific coast of North America. Ex ceptions include extensive marshes in Alaska, in the Columbia River watershed, and along major river systems in California. Tidal freshwater wetlands also occur along the Gulf coast, but the low amplitude-mostly wind driven tides in this area result in much lower coverage and slightly different commun ities than in the Atlantic coast marshes [46]. Because tides can propagate upstream much farther th an the salt water, freshwater tidal marshes can experience hydroperiods similar to t hose of associated salt marshes, but the flooding waters are fresh rather than salt. Upland runoff and precipitation also contribute to the hydrological budget of these wetlands, but their relative contributions can vary considerably from site to site. Vegetation species diversity tends to be much higher than in salt mars hes. The natural vegetation is usually dominated by several broad-leaved plants such as spatterdock (Nuphar luteum ) and pickerelweed ( Pontederia cordata ) and by wild rice ( Zizania aquatica ) and giant cutgrass ( Zizaniopsis miliacea ) in the lower portions. Cattails ( Typha spp.), smartweeds ( Polygonum ( Persicaria ) spp.), rosemallow ( Hibiscus moscheutos ), and others [45] can dominate the upper portions. Common invertebrates in freshwater tid al wetlands include caridean shrimp ( Palamonetes spp.), river shrimp ( Macrobrachium spp.), the introduced Asiatic clam ( Corbicula fluminiea ) in the southeast, and some of the more motile estu arine invertebrates such as blue crabs ( Callinectes sapidus ), mud crabs ( Rhithropanopeus harissii ), and fiddler crabs ( Uca spp.). In tidal freshwater wetlands, freshwater, estuarine, and anadromous fish species can be found. Among the freshwater group, cyprinids, centarchid, and ictalurid fish predom inate [45]; representative species from the three groups are respectively, the spottail shiner ( Notropis hudsonius ) and silvery minnow ( Hybognathus

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Int. J. Environ. Res. Public Health 2012 9 4549 regius ), bluegill ( Lepomis macrochirus ) and pumpkinseed ( Lepomis gibbosus ), and channel catfish ( Ictalurus punctatus ) and brown bullhead ( Ameiurus nebulosus ). Common species among the estuarine group are the mummichog ( Fundulus heteroclitus ), bay anchovy ( Anchoa mitchilli ) tidewater silverside ( Menidia peninsulae ) and hogchokers ( Trinectes maculatus ) Important anadromous species include blueback herring ( Alosa aestivalis ) gizzard shad ( Dorosoma cepedianum ) and sturgeon ( Acipenser spp.). Sturgeon populati ons have been decimated by overf ishing to the point where the shortnose sturgeon ( Acipenser brevirostrum ) is an endangered species, and the Atlantic sturgeon ( Acipenser oxyrinchus ) is very rare. Several marine fish sp ecies, including th e Atlantic menhaden ( Brevoortia tyrannus ) and summer flounder ( Paralichthys dentatus ) may use tidal freshwater wetlands as nursery areas. In the s outh, these nursery areas are very important for snook ( Centropomus undecimalis ) and tarpon ( Megalops atlantica ) populations. Because of their structural diversity, freshwater tidal wetlands are the home of a large number of bird species including wading birds waterfowl, shorebirds, raptors and passerines. Mammalian residents of these wetla nds include meadow voles ( Microtus pennsylvanicus ) marsh rabbits ( Sylvilagus palustris ), beaver ( Castor spp.), muskrats ( Ondatra zibethicus ) and otter ( Lutrinae spp.). Larger mammals such as deer ( Odocoileus spp.) and bears ( Ursus spp.) regularly venture into the wetlands in search for food and/or shelter. As a result of historic development and land use pa tterns, this type of wetland has been reduced in coverage and subjected to degr ading hydrologic modification. In mo re urban areas the wetlands are commonly degraded by the dominance of almost m onotypic stands of non-native and/or invasive species such as Phragmites or Typha while in more rural areas they have been converted to agricultural production (e.g., rice, hay fields, etc. ). Stormwater runoff from urban landscapes or agricultural fields further modifies the energy regime, freshwater supply, and nutrient/pollutant supply. Floodwater mosquitoes of the area will breed in these wetlands, often prolifically. 2.2. Freshwater (Non-Tidal) Wetlands Freshwater (non-tidal) wetlands incl ude a diversity of different plan t forms, from forest-dominated through floating-leaved or subm erged species primarily depe nding upon hydrology, topography, and soils. Under some situations, freshwater wetlands may include a mosaic of these wetland plant communities, while in other situations the wetla nds may be more homogeneous in form, as in a forested swamp, pocosin, or emergent marsh. The diversity of form and the widespread distri bution of this wetland type make it difficult to standardize a policy or set of practices for mosquito manageme nt. A critical component of the mosquito producing potential for this type of wetla nd is the hydrological regime Often, natural limits to mosquito populations prevail, including patterns of inundation an d duration confined to cooler periods, the presence of natural pr edators in long duration water bodie s, and others. In other cases, particularly in disturbed areas, mosquito production is significant enough to require control measures. 2.2.1. Wet Meadows Wet meadow marshes are seasonally wet with st anding water, but typically drier than other wetlands, although the soil may remain saturated even when there is no standing water on the surface.

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Int. J. Environ. Res. Public Health 2012 9 4550 They occur in poorly drained ar eas around lake basins and farmla nd, and high in mountainous areas. Hydrology is usually groundwater-dri ven, but the water table may lie from slightly above ground to more than 1m below the surface [47]. They are most common in the western U.S., Canada, and Alaska Plant communities in wet meadows are highly seasonal depending upon water table depth. Vegetation in wet meadows includes sedges ( Carex spp.), rushes ( Juncus spp.), wildflowers such as marsh mint ( Mentha arvensis ) and smooth swamp aster ( Aster firmus ), and the marsh fern( Thelypteris palustris ) [48]. Species with broad geographi c range include various sedges ( Carex spp.), tufted hairgrass ( Deschampia caespitosa ), Baltic rush ( Juncus balticus ), and Kentucky Bluegrass ( Poa pratensis ) Trees (e.g., Salix spp.) may be abundant in circumsc ribed areas, but never widespread throughout the entire meadow. Wet meadows support a number of amphibians and re ptiles such as the northern leopard frog ( Lithobates pipiens ) and garter snakes ( Thamnophis sirtalis ), that feed upon abunda nt invertebrates. Many birds such as the northern harrier ( Circus cyaneus ) marsh wren ( Cistothorus palustris ) North American bittern ( Botarus lentiginosus ) live in or utilize this habita t for nesting or foraging. Common mammals include muskrat ( Ondatra zibethicus ), meadow vole ( Microtus pennsylvanicus ), and ermine ( Mustela ermine ) ; large mammals such as elk ( Cervus canadensis ), black bear ( Ursus americanus ), and gray wolves ( Canis lupus ) often frequent this habitat. Major environmental impacts to this ecosystem in clude interruption or modi fication of surface and groundwater flows (reservoirs, water diversions, ditc hes, roads, water pumping). Additional habitat loss/degradation can be attributed to widespread logging and urbanization, hay production and direct grazing of cattle [47]. Although ther e are no mosquito species spec ifically associated with wet meadows, most floodwater mosquitoes th at occur in the area will breed there. 2.2.2. Wet Prairies Wet prairies are grassland ecosystems that occu r in the floodplains of streams and rivers, in depressions, and along lake margins. They occur throughout the central midwestern United States, parts of Canada and Florida [49]. These ecosystems are lowlands with moist to wet soil throughout the majority of the year due to poor drainage, often with standing stagna nt water. A high water table is characteristic of wet prairie sites with soil text ures and landforms varying with geographic location. Hydroperiod is intermediate betw een wet meadows and marshes [13] with standing water occurring for shorter duration and frequency than in marshes. Wet prairies may receive water from intermittent streams as well as from ground water and precipitati on. Northern prairie grasses include blue-joint grass ( Calamagrostis canadensis ), prairie cordgrass ( Spartina pectinata ) and sedges ( Carex spp.), and in South Florida include maidencane ( Panicum hemitomon ), spikerush ( Eleocharis spp.), beakrush ( Rhynchospora spp.), and water dropwort ( Oenanthe javanica [50]). During the wet season, wet prairie animal communitie s consist of aquatic and semiaquatic species similar to those of sloughs and include beaver ( Castor canadensis ), eastern tiger salamander ( Ambystoma tigrinum ), midland brown snake ( Storeria dekayi ), eastern massasauga ( Sistrurus catenatus ), American bittern ( Botaurus lentiginosus ), mallard ( Anas platyrhynchos ), northern harrier ( Circus cyaneus ) and sedge wren ( Cistothorus platensis ) As water levels fall in the dry season, some of the aquatic animals are forced in to the deeper pond areas. Particularly in Florida, water levels rarely

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Int. J. Environ. Res. Public Health 2012 9 4551 drop a foot below the land surface except in abnormally dry years [ 51]. Wet prairies have suffered destruction and severe alterati ons since 1900. Approximately 1,300 km2 (500 mi2) have been destroyed in southern Florida alone [52]. These alterations have occurred through drainage, water impoundment, conversion to agriculture, and exotic plant invasion [53]. Restoration effo rts, such as in the Everglades (Florida), on the Kuhl Century Fa rm (Minnesota), and at the Woolsey Wet Prai rie Sanctuary (WWPS) (Arkansas) are being undertaken th roughout the U.S. As with wet mea dows, floodwater mosquitoes of the region will also breed in wet prairies. 2.2.3. Potholes The Prairie Pothole region of No rth and South Dakota, Wisconsi n, Minnesota and the Canadian provinces of Manitoba, Saskatchewan and Alberta covers approximately 780,000 km2 [10] (Figure 1) and is considered one of the richest wetland regions in the world because of the abundance of shallow lakes, marshes and smaller wetlands located in ri ch soils and warm summer climates [54]. Pothole wetlands were formed by glacial action during the Pl eistocene. The greatest abundance of potholes is found in moraines of undulating glaci al till. Once the basins were sealed with finer silts, water retention created suitable dept hs for semi-aquatic plants. Surface water inputs to potholes is very limited by the dearth of connection to surface water sources, and groundwater inputs are limited by th e low permeability of the region’s glacial tills (although some connection is usually present). The major water sources for these potholes are snow, summer rain, and snowmelt runoff [55] Hydrological pattern s of potholes are diverse, both in time and space. There are yearly fluctuations in water levels as well as high between year variation depending upon precipitation. Individual wetlands vary in th e timing and duration of surface flooding. Some may remain flooded only for a few weeks after snowmelt, while others may be s easonal (flooded until early summer) semi-permanent (flooded until late summer) and permanent (Flooded for most of the year) One common characteristic of pr airie pothole are the concentric vegetation zones thatreflect topography-associated water level fluctuations The marsh edge is dominated by sedges ( Carex spp.), grasses ( Spartina spp.) and forbs and sometimes woody species ( Salix spp. and Populus spp.). During drought, perennial species such as Typha spp., Scirpus spp., and Sparganium eurycarpum and annuals such as Polygonum spp., and Cyperus spp. propagate from the seed bank. During wet stages, annual species that require exposed substrate for germin ation disappear and submersed species submersed species such as Potamogeton spp. and Najas flexilis appear. The emergent perennials can persist during the wet stages, but after seve ral years they disappear resulti ng in pond-like conditions with only floating and submersed plants remaining [18]. It is believed that 50 to 75 percent of all wate rfowl produced in North America originates from the Prairie Pothole region. The area is also home to many priority bird species including Franklin’s gull ( Leucophaeus pipixcan ) yellow rail ( Coturnicops noveboracensis ) and piping plover ( Charadrius melodus ) Baird’s sparrow ( Ammodramus bairdii ) Sprague’s pipit ( Anthus spragueii ) Wilson’s phalarope ( Phalaropus tricolor ), marbled godwit ( Limosa fedoa ) and American avocet ( Recurvirostra americana ) These wetlands are also important in the migration routes of the Hudsonian godwit ( Limosa haemastica ) American golden-plover ( Pluvialis dominica ) white-rumped sandpiper ( Calidris fuscicollis ) and buff-breasted sandpiper ( Tryngites subruficollis )

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Int. J. Environ. Res. Public Health 2012 9 4552 Representative amphibians include the barred tiger salamander ( Ambystoma mavortium ) and the Great Plains toad ( Anaxyrus cognatus ); reptiles the painted turtle ( Chrysemis picta ) and the smooth green snake ( Opheodrys vernalis ); and mammals the American mink ( Mustela vison ), the coyote ( Canis latrans ), and the prairie vole ( Microtus ochrogaster ). Unfortunately, it is estimated that only about 10% of the original wetlands in the area remain [13]. More than half of the original wetlands were drai ned or altered for agricultu re. Other impacts include pollution due to runoff and grazin g. Major efforts to protect the remaining prairie potholes have progressed since the 1960’s by agencies such as the U.S. Fish and Wildlife Services, Ducks Unlimited and The Nature Conservancy [13]. In an effort to restore this wetland type artificial potholes have been excavated or blasted, or existing potholes have been deepened or partitioned to enhance waterfowl habitat [56]. Mos quito species associated with prairie potholes include Aedes campestris A. dorsalis A. flavescens A. vexans Anopheles earlei Culex tarsalis C. territans and Culiseta inornata [57,58]. 2.2.4. Playas Playas are ephemeral, depressional, recharge we tlands that occur primarily in the high plains (Texas, Oklahoma, New Mexico, Colorado, and Kansas ) but are particularly abundant in the Llano Estacado (Staked Plains) region (Figure 1). Ther e are approximately 65,000 playas along the Great Plains [59,60]. They range in area from less than 1 ha to more than 250 (ave rage 6.3 ha) [18]. These shallow, seasonal wetlands capture surface runoff, can function in flood attenuation, provide water for irrigation of surrounding ag ricultural fields, and play a major role in the recharge of underlying aquifers [60]. They are often biodi versity repositories and serve as ecological refugia in the arid and intensively cultivated high plains. Playas are not normally connected to stable wate r sources and can be a ppreciably salty due to accumulation of salts from the underlying sediments a nd subsequent evaporation. They receive most of their water from precipitation and surface runoff and lose water through aquifer recharge and evaporation [61]. They are usually dry during late winter, early spring, and late summer and may experience multiple wet-dry cycles during a single year. Because of the highly fluctuating conditions, th e flora is dominated by annuals and short-lived perennials and is hi ghly dependent u pon the seed bank, and upon germinat ion and growth conditions [18]. Of the approximately 450 plant species reported from High Plain playas, only two, the spotted evening primrose (Oenothera canescens ) and the big bract verbena ( Verbenea bracteata ), occur consistently in most areas [61]. At a particular site, one can expect approximately 13 different plant species to occur at a given time, and about 19 different species during the growing season [62]. With the exception of several species that occur only at the edges, ( O. canescens turkey tangle fogfruit ( Phyla nodiflora ), and alkali mallow ( Malvella leprosa ), plant zonation is not evident in Playas. Playa wetlands can be extremely rich in wildlife as they are water sources in an otherwise dry landscape. They support numerous speci es of invertebrates that are es pecially importan t to migrating waterfowl and shorebirds during their long treks be tween wintering and breeding grounds. Playas also support significant complements of reptiles, and am phibians such as the plains spadefoot toad ( Spea bomifrons ); waterfowl such as mallards ( Anas platyrhynchos ) and pintails ( Anas acuta ); and many

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Int. J. Environ. Res. Public Health 2012 9 4553 other bird species incl uding bald eagles ( Haliaeetus leucocephalus ) and whooping cranes ( Grus Americana ). More than 50 mammal species utilize the playas [18]; Eastern cottontails ( Sylvilagus flroidanus ) and various rodents are most common. Larger mamm als include feral hogs ( Sus scrofa ) and mule deer ( Odocoileus hemionus ) Major threats to playa wetlands include sedimentation and contamination from surrounding agri cultural runoff, urbanization, ov ergrazing, deliberate filling, and water diversion for agriculture. There is evidence of pesticide contamination of playas [63,64] including by some pesticides used for mosquito control [65], some at concentrations within the LC-50 range of various aquatic invertebrate species [66]. However, cropland agriculture, and associated pesticide use, predominates in the drainage areas surrounding playas and no direct linkages between pe sticide levels and specific pest control applications have been established [64]. Some pl aya wetlands are protected due to their wildlife value and many neighbori ng farmers are adopting mo re ecologically sound farming techniques such as installing natural vege tation buffers, in recognition of the importance of playa wetlands. Although many species of mosquitoes can devel op in playa wetlands, the most common ones are Culex tarsalis C. quinquefasciatus Aedes nigromaculis Psorophora signipennis and A. vexans [67] Large numbers of Aedes and Psorophora can be produced following the heavy rains of June or July, followed by increasing numbers of Culex as the emergent annu al vegetation increase s in the playa [68]. 2.2.5. Vernal Pools Vernal pools, also known as w oodland pools, are seasonally flooded depressions that are dry for part of the year (usually summer and fall). Individual pools are genera lly isolated, but several may be connected to each other through shallow swales. In the United States they occur primarily in the Pacific Coast and in the North and Northeast. They rarely have groundwater inputs; they fill with rainfall, snowmelt, or runoff. A vernal pool may go through several cycl es of filling and drying in one year, or may not flood at a ll during dry years. Although the underlying soil types vary, in most cases there is a hardpa n layer which causes the retention of water in the pools. Vegetation in vernal pools is high ly variable and most pools are vegetated with widely distributed species. Individual pools may lack vegetation or may be vegetated w ith trees, shrubs, marsh and wet meadow species, aquatic plants or combinations of these [69]. Vernal pools provide valuable habitat to a number of rare species such as the San Diego mesa mint ( Pogogyne abramsii ), the longhorn fairy shrimp ( Branchinecta longiantenna ), and Swainson’s hawk ( Buteo swainsoni ). Vernal pools also afford critical habita t in the life cycle of certain amphibians and invertebrates, and are used by many bird species as feeding sites. Because of the regular drying, they usually do not support breeding fish populations Many species such as fairy shrimp ( Eubranchipus spp.), wood frogs ( Rana sylvatica ), and mole salamanders ( Ambystoma spp.) are considered vernal pool indicator species because th ey are obligate or semi-obligat e users of this habitat. As with other wetlands, considerable vernal pool habitat has been lost through urbanization, draining, conversion to permanent fish ponds, filling fo r mosquito control, conversion to agriculture, and many other activities [ 70]. Because of their sma ll size and dispersion, the amount of habitat lost and still existing is not really known.

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Int. J. Environ. Res. Public Health 2012 9 4554 Although predatory fish are usually absent, other larval mosquito predators such as odonates occur in the pools. Nevertheless, mosquitoes such as Aedes canadensis A. excrucians and A. strictus can often develop along changing borders, among vegetati on, and in leaf litter and other detritus. 2.2.6. Bottomland Swamps Bottomland swamps are temporarily or seasonally fl ooded habitats that occu r in the s outh-east and south-central United States. They ar e usually found along rivers and stre ams, but can occur in a variety of situations including valley bo ttoms, low-lying depressions, and ar eas of moisture-holding soils. In addition to providing important habitat for a la rge number of animal spec ies, bottomland swamps play a variety of roles in the watershed including water storage and flood control and water quality improvement by removing excess nutrients, filtering sediments, and processing organic wastes. Bottomland swamps are also extremely productive, in part due to inputs of fl ood-transported nutrients and organic matter [71]. In North America, they are most abundant along the Atlantic coastal plain from Delaware to Florida, along the Gulf coastal pl ain to Texas, and along th e Mississippi to Southern Illinois [72] (Figure 1). They are normally flooded during most of the y ear, but water levels ca n exhibit significant fluctuations throughout the year an d between years. Majo r water inputs include river overflow and runoff, but contributions from precipitation and ground water sources can be significant. Bottomland swamps are deciduous forest wetlands usually dominated by va rious species of gum ( Nyssa spp.), bald cypress ( Taxodium distichum ), and oak ( Quercus spp.). Other tree species often occurring in these swamps include black willow ( Salix nigra ), red maple ( Acer rubrum ), river birch ( Betula nigra ), and sycamore ( Platanus occidentalis ). Shrubs may include buttonbush ( Cephalanthus occidentalis ), wax myrtle ( Myrica cerifera ), eastern swamp privet ( Forestiera acuminate ), and Virginia sweetspire ( Itea virginica ). Characteristic and secondary species, however, vary considerably depending upon slope, stream volume, soil t ype, flooding regime, and successional status. Bottomland swamps support diverse aquatic inverteb rate and fish communities many of which take advantage of floodwaters to disper se into the floodplain and exploit abundant food resources there [73]. They provide habitat to a number of species of special conservation concern such as the Seminole Texan crescent butterfly (Phyciodes texana ) the Southern dusky salamander ( Desmognathus auriculatus ) the common rainbow snake ( Farancia erytrogramma ) the yellow-crowned night heron ( Nyctanassa violacea ) and the Louisiana black bear ( Ursus americanus luteolus ). Beavers ( Castor canadensis ) are important inhabitants of the swamps and are highly apparent due to their visible dams and associated flooded areas. It is estimated that bottomland hardwood swamps once covered over 12 million ha across the south eastern and south central parts of North America, but only about 40% st ill remains [74]. A major factor in the coverage loss has been conversion to ag riculture and forestry act ivities but losses to construction, flood control activiti es, reservoir construction, surf ace mining, and urban development have also been significant. Loss of this habitat ha s been partially blamed for the extinction or near extinction of several species includ ing the ivory-billed woodpecker ( Campephilus principalis ), the Carolina parakeet ( Conuropsis carolinensis ), and Bachman’s warbler (V ermivora bachmanii )

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Int. J. Environ. Res. Public Health 2012 9 4555 Mosquito species occurring in these habitats tend to utilize birds, small mammals, reptiles, and amphibians for blood feeding, but severe human pests such as several Aedes and Psorophora species can be abundant [75]. Common mosquito sp ecies found in bottoml and swamps include Aedes infirmatus A. atlanticus Psorophora spp., Anopheles crucians Anopheles quadrimaculatus Culex nigripalpus C. erraticus Culiseta melanura Coquilletidia perturbans and Uranotaenia spp. Many of these species are known vectors of several arboviruses including those that can cause eastern equine encephalitis, western equine encephalitis and West Nile virus [27,75]. 2.2.7. Atlantic White Cedar Wetland Forests Cedar-dominated wetlands are most commonly called cedar swamps or cedar bogs, with a variety of other designations restricted to specific regi ons (e.g., “spungs” in the New Jersey Pine Barrens, “juniper lights” in the Virginia-North Carolina Great Dismal, “juniper bogs” throughout the south). The native range of Atlantic white cedar ( Chamaecyparis thyoides ) is limited to freshwater wetlands along the Atlantic and Gulf coasts of the United States ranging from Ma ine to Mississippi [76] (Figure 1). Hydrologic conditions are quite va riable, but flooding usually occurs in late winter and early spring [18]. Cedar swamps situated in basins receive most of their wa ter from precipitation, but others may receive significant ground water inputs. Their shallow, dark, gene rally acid waters are low in nutrients and are buffered by complex organic acids (e .g., humates, fulvic acids) [76] Surficial deposits beneath cedar forests provide groundw ater storage and discharge and recharge areas. Peats adsorb and absorb nutrients and pollutants, purifying and prot ecting ground and surface water with which they are in contact [77]. Distinctive biotic assemblages grow under conditi ons too extreme for the majority of temperatedwelling organisms. The shallow, dark, generally aci d waters are low in nutrients and are buffered by complex organic acids (e.g., humates, fulvic acids). Surficial deposits beneath cedar forests provide groundwater storage and discharge and recharge areas. Peats adsorb and absorb nutrients and pollutants, purifying and protecti ng ground and surface water w ith which they are in contact. In many regions cedar wetlands are refugia for species that are rare, endangered, or threatened locally or nationally. The swamps form southern pockets for northern species at the ge ographic limits of their ranges, and similar northern pockets for southern species, while many locally common aquatic plants and animals are absent fro m cedar swamps [78,79]. Atlantic white cedar ( Chamaecyparis thyoides ) normally dominate the landscape, but other canopy species such as red maple ( Acer rubrum) black gum ( Nyssa sylvatica ), sweet bay ( Magnolia virginiana ), and various pines ( Pinus spp.) often co-occur. Open can opy stands usually have a well developed shrub layer that includes bitter gallberry (Ilex glabra ), fetterbush ( Leucothoe racemosa ), swamp honeysuckle ( Rhododendron viscosum ), poison ivy ( Toxicodendron radicans ), poison sumac ( T. vernk ), and highbush blueberry ( Vaccinium corymbosu ) and cranberries ( Vaccinium spp.). In many regions cedar wetlands are refugia for speci es that are rare, endangered, or threatened locally or nationally. The swamps fo rm southern pockets for northern species at the geographic limits of their ranges, and similar northern pockets for s outhern species, while many locally common aquatic plants and animals are absent from cedar sw amps [78,79] They support numerous amphibians and reptiles such as the slimy salamander ( Plethodon glutinosus ), the eastern painted turtle ( Chrysemis

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Int. J. Environ. Res. Public Health 2012 9 4556 picta ), the Southern copperhead ( Agkistrodon contortris ), and the timber rattlesnake ( Crotalus horridus ). These wetlands provide excellent habitat for deer, rabbits, and birds. Parulid warblers such as yellowthroats ( Geothlypis trichas ) and prairie warblers ( Setophaga discolor ) are common inhabitant of these areas and many other bird species including the barred owl ( Strix varia ), The sharp-shinned hawk ( Accipiter striatus), and the purple finch ( Haemorhous ( Carpodacus ) purpureus ) frequent this habitat. White cedar foliage is a preferred winter browse for white-tailed deer ( Odocoileus virginianus ), and cottontail rabbit ( Sylwilagus floridanus ) and meadow mouse ( Microtus pennsylvanicus ) feed on cedar seedling, and in some areas bear feed on berries from the shrubby understory [76]. There are 13 species in 4 genera of mosquitoes that utilize AWC wetlands as larval habitat [80]: Aedes abserratus A. aurifer A. canadensis A. excrusians A. triseriatus A. cinerius A. vexans Culex pipiens C. restuans C. territans Culiseta melanura Cs. morsitans and Uranotaenia sapphirina Among these species A. canadensis and A. excrucians are aggressive mammal biting mosquitoes that can create nuisance problems [81]. Culex pipiens and C. restuans are known West N ile virus (WN) vectors. This habitat also supports development of Culiseta melanura the enzootic vector of eastern equine encephalitis (EEE) virus. Culiseta melanura larvae are found and ofte n over-winter in crypts under the arching roots of mature cedars. Although A. vexans Cs. morsitans A. canadensis and A. triseriatus are believed to be capable of harboring EEE virus, only Cs. melanura is known to transmit EEE to humans. Passerine birds are impor tant enzootic hosts for the EEE virus [82]. 2.2.8. Bogs and Pocosins (Including Carolina Bays) A bog (synonymously referred to as mire, moor a nd muskeg) is a peat-accumulating wetland with no significant inflows or outflows. They are characterized by spongy p eat deposits, acidic waters, and a floor dominated by a thick carpet of mosses, mainly sphagnum species [18]. Bogs rece ive all or most of their water from precipitation (termed ombrotr ophic or “cloud-fed”) rath er than from runoff, groundwater or streams. As a result, bogs are low in the nutrients needed for plant growth, a condition that is enhanced by acid forming peat mosses. Depending on their location in the landscape, which determines their development, bogs can be describe d as “valley”, “raised”, “blanket” and “quaking” bogs. Bogs generally form in one of two ways: as sphagnum moss grows over a lake or pond and slowly fills it (terrestrialization), or as sphagnum moss blankets dry land and prevents water from leaving the surface (paludification). Over time, many feet of acidic peat deposits build up in bogs of either origin. Water flowing out of bogs has a charac teristic brown color from dissolved peat tannins. Bogs are widely distributed in co ld, temperate climes, generally asso ciated with low temperatures and short growing seasons where ampl e precipitation and high humidity cause excessive moisture to accumulate, mostly in the boreal regions of the north ern hemisphere. In the U.S. bogs are mostly found in the glaciated northeas t (New England, the Adirondack region of New York and Pocono region of Pennsylvania) and Great La kes regions (Figure 1). Bogs serve an important ecological function in preventing downstream flooding by absorbing precipitation and have been recogni zed for their role in regulating the global climate by storing large amounts of carbon in peat deposits. The unique and demanding physical and chemical characteristics of bogs result in the presence of plant and an imal communities that demonstrate many special

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Int. J. Environ. Res. Public Health 2012 9 4557 adaptations to low nutrient levels waterlogged conditions, and acidic waters, such as insectivorous sundew ( Drosera spp.) and pitcher plants ( Sarracenia spp.). Bogs also suppor t species like high bush blueberry ( Vaccinium corymbosum ), cranberries ( Vaccinium spp.), Labrador tea ( Ledum groenlandicum ), cotton grass ( Eriophorum spp.), and a number of protected plant and animal species. As the peat builds and the bog surf ace is further removed from the wa ter interface or along the upland edges trees such as black spruce ( Picea mariana ) and tamarack ( Larix laricina ) may grow. There is a number of pestiferous mosquito specie s associated with boreal wetlands and because of the short summer season, these mosquito species can emerge in very large numbers. These habitats may be commonly referred to as “bogs”, however, they tend to be more minerotrophic and productive than true bogs and may in fact be more likely to be classified as forest or shrub swamps. Perhaps because these peatlands are largely remote, unde velopable and sometimes vast, mosquito control efforts are, for the most part, nonexistent. Bogs because of their acidic and nutrient-poor nature generally do not support mosquito la rvae. However, one mosquito species, Wyeomia smithii has adapted to develop in water collected in insectivor ous pitcher plants. This species is not of public health significance. Similar to bogs in their development, pocosins are densely vegetated evergreen shrub wetlands. These evergreen shrub and tree dominated landscapes are found on the Atlantic Coastal Plain from the Delmarva Peninsula to northern Florida, and are pa rticularly dominant in North Carolina. The word pocosin comes from the Algonquin Native American word for “swamp on a hill”. Usually, there is no standing water present, but a shallow water table leaves the so il saturated for much of the year. Pocosins range in size from less than an acre to several thousand acres and in most instances are located between and isolated from old or existi ng stream systems. Because pocosins are found in broad, flat, upland areas fa r from large streams, they are ombr otrophic like northern bogs. Also like bogs, pocosins are found on waterlogged, nutrient poor, ac id soils. The soil is often a mixture of peat and sand containing large amounts of charcoal from periodic burnings. Pocosins are subjected to fire about every 10 to 30 years because they periodically become very dry in the spring or summer. The fires are ecologically important be cause they increase the diversity of shrub types in pocosins. The most common plants in pocosins are evergreen trees (loblolly pine ( Pinus taeda ) red bay ( Persea borbonia ), and sweet bay ( Laurus nobilis )), and evergreen shrubs (wax myrtle ( Myrica cerifera ), gallberry ( Illex glabra ), titi ( Cyrilla racemiflora), fetterbush ( Leucothoe racemosa ), and zenobia ( Zenobia pulverulenta ). Bogs and pocosins often harbor abundant invertebra te, particularly insect, communities. Bogs rarely harbor fish because of the acidic conditions, although small minnows (e.g., Umbra limi ) can sometimes be found. Surprisingly, bogs and fens are home to abundant amphibian populations including the rare four-toed salamander ( Hemidactylium scutatum ) and the green frog ( Rana clamitans ). Few reptiles are common in bogs, but some, like the bog turtle ( Glyptemys muhlenbergii ), can often been found there. Over 100 bird species are known to breed in North American peatlands (bogs, pocosins and fens) and many more use the ha bitat during other parts of their life cycle [83]. Included are the white throated sparrow ( Zonotrichia albicollis ) and the palm warbler ( Dencroida palmarum ). Mammals are rarely abundant in peatlands, but small rodent populations often exist, and large mammals such as moose ( Alces alces ) and black bear ( Ursus americanus ) often frequent these areas, particulalry the edges (see also fens, below). Some pocosins are very large and difficult to

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Int. J. Environ. Res. Public Health 2012 9 4558 develop, and so they remain largely undisturbed thereby providing sizeable tracks of undisturbed habitat for species like black bears ( Ursus americanus ) and the endangered red-cockaded woodpecker ( Picoides borealis ). About 1,400 square miles of undisturbe d pocosins remain today. By comparison, more than 3,000 square miles were drained be tween 1962 and 1979. Historically, pocosins were mostly threatened by agriculture. Today, timber harvesting, peat mining, and phosphate mining join agriculture as the biggest threats to the remaining undisturbed pocosins. 2.2.9. Fens Fens are also peat-forming wetlands that are distri buted mostly in the cool boreal regions of the northern hemisphere. They are generally associated with low temperatures a nd short growing seasons, where ample precipitation and high humidity cause excessive moisture to accumulate. Fens are distinguished by their strong conne ction to ground water that recei ves nutrients from sources other than precipitation: usually from upslope sources through drainage from surrounding mineral soils and from groundwater movement. Depending on the underlyi ng parent material fens may be acidic to strongly alkaline, the former bei ng labeled a “poor” fen (more simila r to a bog) and the latter often called “rich”, “marl” or “calcareous” fens. Fens differ from bogs because they have a ground-water discharge, are less acidic, and have higher nutrien t levels. In North America fens are found in the glaciated mid-western and northeast ern United States, the Great La kes region, the Rocky Mountains, portions of the Appalachian Mountai ns and much of Canada [13,84]. Because of higher nutrients in the root zone than bogs, they are able to support a much more diverse plant and animal communities. Fens are often covered by grasses, sedges, rushes, and wildflowers. Depending upon acidity, the vegetation may be dominated by Sphagnum mosses in acidic areas, with sedges, shrubs, and dicot herbs of ten prevalent in neutral and alka line areas. Examples of the later include tussock cottongrass ( Eriophorum vaginatum ), Carex spp, and heather ( Calluna vulgaris ) and Some fens are characterized by pa rallel ridges of vegetation sepa rated by less productive hollows. The ridges of these patterned fens form perpendicular to the down slope direction of water movement. Over time, peat may build up and separate the fen from its groundwater supply. When this happens, the fen receives fewer nutrients and may become a bog.B ecause of habitat losses elsewhere, fens are becoming increasingly important habitat for moose ( Alces alces ), deer ( Odocoileus virginianus ), black bear ( Ursus americanus ), beaver ( Castor canadensis ), lynx ( Lynx spp.), fishers ( Martes pennanti ), snowshoe hare ( Lepus americanus ), otter ( Lontra canadensis ), and mink ( Neovison vison ). Because of the less acidic conditions and conne ctions to streams, fens support more fish species than bogs. Species such as pike ( Esox Lucius ), walleye ( Sander vitreus ), bluegill ( Lepomis macrochirus ), smallmouth bass ( Micropterus dolomieu ) brook trout ( Salvelinus fontinalis ) brown trout ( Salmo trutta ), and killifish may inhabit fens or connected streams. Fens also provide critical habitat to many species of birds including the gr eater sandhill crane ( Grus canadensis ), great gray owl ( Strix nebulosa ) short eared owl ( Asio flammeus ), sora rail ( Porzana Carolina ), and sharp-tailed sparrow ( Ammodramus nelsoni ). Fens provide important benefits in a waters hed, including preventing or reducing the risk of floods, improving water quality, and providing hab itat for unique plant and animal communities. However fens, like most peatlands, experienced a decline in acreage at a rate of about eight percent from 1950 to 1970, mostly from mining and drai ning for cropland, fuel, and fertilizer. Although

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Int. J. Environ. Res. Public Health 2012 9 4559 mining and draining these ecosystems provide needed resources, a fen natura lly requires up to 10,000 years to complete formation [85]. Since fens are hydrologically driven by a high, re latively stable ground-water table they seldom flood in a manner that would support mosquito produc tion. There are references in the literature regarding “fens” and heavy mosquito infestatio ns however the terms fen, bog and marsh are used interchangeably in the lay literature. The acidic conditions of poor fens could support species like pitcher plants ( Sarracenia purpurea ) which, although carnivorous, do provide larval habitat for Wyeomyia smithii This species however, is autogenous (can de velop eggs without a blood meal, see below) and not of medical or economic importance [86]. 2.2.10. Riverine, Riparian, Floodplain Wetlands Riparian wetlands form adjacent to rivers and st reams and some may occur near the coast. Soils tend to be alluvial, and are periodically or regularly flooded by upstream runoff, and underground flows. Riparian wetlands are importa nt as filters of upland runoff before it enters rivers and streams. Riparian wetlands comprise a wide variety of forms, from frequen tly wetted short duration forested floodplain through long duration emerge nt wetlands occurring in quiescen t areas in large water bodies, and an incredible variety of conditions between th ese extremes. Many of these wetlands may be small and highly interspersed in the la ndscape, but many are extensive an d cover thousands of contiguous acres. Riverine wetlands are normally supported by rive r hydrology, and with the exception of man-made regulators of flow (e.g., dams, in-lin e and off-line storage reservoirs, etc. ), are not problematic in the development of high mosquito populations levels. So ils tend to be alluvial, and are periodically or regularly flooded by upstream runoff, and undergr ound flows. Riparian wetlands are important as filters of upland runoff before it enters rivers a nd streams (see also Bottomland Swamps). Riparian wetland areas are generally forested, narrow, and have only small areas of inundation, if present at all. These areas typically do not produc e significant mosquito population de nsities. However, as a result of the diversity of these wetland types, their distributi on through the built environment, and the presence of tree falls, water holding debris (e.g., tires), and other elements, these systems can produce pestilential mosquito populations. Rockpools within these areas flood intermittently and can produce mosquitoes such as Aedes atropalpus and A. japonicus As a result of their diversity of form and hydrologic regime, widespread distri bution, and small scale, it is very difficult to manage mosquito populations effectively. Similar to both the riverine and riparian wetla nds, the term “floodplain wetlands” represent a diverse range of wetland conditions from bottomland hardwood forest s with months of inundation to well drained herb and forb dominated systems that are infrequently inunda ted for relatively short durations. Floodplain systems can be major producers or several species of mo squitoes—in natural and modified settings. For example, river floodplains in Vermont often produce significant numbers of mosquitoes in the spring following snowmelt which can have major impacts on tourism as well as on livestock and public health. Simila r situations arise along the Susque hanna and Delaware Rivers. Other good examples are the Sudbury and Concord River floodpl ains near the city of Boston, which are very productive Aedes vexans (a potential bridge vector for eastern equine encephalitis). These floodplain

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Int. J. Environ. Res. Public Health 2012 9 4560 wetlands may be associated with uber rural landscapes where mo squito populations present no problem to ultra-urban systems where even relativ ely low mosquito population levels are seen as problematic. These factors often complicate pl anned approaches to mosquito management. 2.3. Wetland Complexes Several regions in North America support very large wetlands complexes. Two of the most important ones are the Florida Ever glades and the Mississippi Deltaic Plain wetlands. Because of their extent, complexity, and ecological and economic impor tance, we include below short descriptions of these areas. Other important wetlands complexes in North America include the Great Lakes wetlands complex, the San Francisco Bay marshes, the H udson Bay Lowlands, and the Canadian Central wetlands (Figure 1). 2.3.1. The Florida Everglades The term Everglades does not identify a distinct habitat type, but defines a South Florida watershed, part of which is technically a wide and slow flowing river, that contains a mosa ic of habitats some of which are wetlands. The major wetlands in the regi on include the Everglades proper, the Big Cypress swamp, and the coastal mangal of Fl orida Bay. In addition to wetlands, the region supports a variety of habitats including marine/estuarine, pinelands, and hardwood hammocks. The Everglades is dominated by sawgrass ( Cladium jamaicensis ) with interspersed hammocks that support a variety of tropical and su btropical plant species including pa lms and hardwoods. This “River of Grass” once conducted the water flowing from the Kissimmee chain of lakes, down the Kissimmee River into Lake Okeechobee to its ultimate destina tion in Florida Bay. Originally spanning almost 28,500 km2, the Everglades now covers half that area due to habitat alteration for agriculture, development, and flood control (Figure 1). West of the sawgrass Everglades is the Big Cypress Swamp, which is dominated by cypress ( Taxodium ) species with interspersed pinelands and wet prairies. To the South, the mangrove forest of Fl orida Bay contain the three major mangrove species described above, red ( Rhizophora mangle ) black ( Avicennia germinans ) and white ( Laguncularia racemosa ) and common associates such as buttonwoods ( Conocarpus erectus ). The Comprehensive Everglades Re storation Plan (http:///www.evergl adesplan.org) is an ambitious State-Federal initiative that aims to restore and pr otect the water resources of South Florida, including the Everglades. In spite of the f act that both local and national pol itics have caused complications in the implementation of various aspects of the plans, progress is steadily being made. The very steep price tag of the project (over US $13 billion), however, also means that implementation will surge and wane depending upon the economic situation and mood of the country. There are 43 mosquito species reported in the Everglades National Pa rk, with the salt marsh mosquito A. taeniorhynchus being one of the most troublesome for humans. Ot her species commonly found include C. nigripalpus and Wyeomyia spp. [87].

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Int. J. Environ. Res. Public Health 2012 9 4561 2.3.2. The Mississippi Deltaic Plain Wetlands (“Louisiana Wetlands”) The Mississippi Deltaic Plain region is the largest wetlands system in the United States, with an extension of nearly 7,250 km2. Wetlands in this deltaic plain co mplex are often re ferred to as the “Louisiana Wetlands” [88] (Figure 1). The Mississippi Delta plain is composed of six major drainage basins, each of which represents shifts (in time) of the major distributary of the river [89]. The Atchafalay a basin is the youngest and receives approximately one third of the flow from the Mississippi and Red Rivers. The large input of fresh water and the shallow depths result in a predominance of freshw ater marshes. The next youngest is the current Mississippi River Delta which receives approximately two-thirds of the river’s flow. The associated wetlands are also mostly fresh, but there are brackish marshe s along the edges. The Barataria, Terrebonne, Vermillion-Cote Blanche, an d the Ponchartrain-Lake Borgne basins, are increasingly older and s upport extensive salt, brackish, and freshw ater marshes, as well as forested wetlands along the upland edges. Vegetation in these marshes is fairly typical of the specific marsh types elsewhere. In the salt marshes, smooth cordgrass ( Spartina. alterniflora ) and saltmeadow cordgrass ( Spartina patens ) predominate, and black rush ( Juncus roemerianus ), saltgrass ( Distichlis spicata ), and turtleweed ( Batis maritima ) occur in varying degr ees of abundance. The same species occur in the brackish marshes, with S. patens more dominant than in the saline marshes and Schoenoplectus americanus (chaormaker’s bullrush) becomi ng common in some areas. Panicum hemitomon (maidencane), Sagittaria falcata (duck potato, bulltongue) several spikerush ( Eleocharis ) species, and Alternathera philoxeroides (alligatorweed) dominate the freshwater marshe s, and often there is a transitional zone between these and the brackish marshes where Phragmites australis (common reed), S. falcata (duck potato) and Bacopa monnieri (water hyssop) are most abundant [58] In what is left of the forested wetlands, cottonwood ( Populus deltoides ), silver maple ( Acer saccharinum ), and box elder ( Acer negundo ) are the predominant canopy species. Because of extensive developmen t along the Mississippi River, these wetlands are very vulnerable to human impacts. In addition to pollution and extensive habitat loss to residential, commercial, industrial, and agricu ltural development, artificial channeling and other modificatio ns for flood control and irrigation have decreased the amount of sediment reachi ng the wetlands. The reduced sedimentation, and both natural and accelerated subsid ence caused by extracti on of oil and gas, and withdrawal of groundwater, have re sulted in wetlands losses of 65–100 km2 per year [90]. The U.S. Geological survey estimate s a loss of over 500 km2 of coastal wetlands due to Hurricanes Rita and Katrina [91]. However, the hurricanes may have also had beneficial effects by stabilizing parts of the coastline via the deposition of tons of silt and sediments [92]. Mosquito communities in these wetlands also resemble those of southern fresh-salt water marshes, with Aedes taeniorhynchus and A. sollicitans predominating in the salt marshes and in the brackish areas along with several Culex species such as C. salinarius and C. nigripalpus In the freshwater areas, several Aedes species including A. infirmatus various Psorophora species, Anopheles crucians Culiseta melanura Coquillettidia perturbans, C. nigripalpus, and several others can become abundant.

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Int. J. Environ. Res. Public Health 2012 9 4562 2.4. Constructed Wetlands Constructed wetlands are man-made aquatic systems that are designed to carry out wastewater treatment. Municipal wastewater is most commonl y treated by these systems; however, constructed wetland systems have been used to treat a vari ety of wastewaters including urban stormwater, agricultural wastewater, mine drainage, aquacultu re wastewater, and indus trial wastewater [93]. Constructed wetlands are categorized broadly into two types: free water surface (FWS) wetlands and subsurface flow (SSF) wetlands [94]. Most FWS wetlands contain rooted emergent vegetation inundated with standing water and are similar in appearance to natural marshes. FWS systems that utilize only submerged or floating vegetation are comparatively less common [93]; however, large FWS wetlands usually support a diverse flora with ve getation of more than one growth type [95]. SSF wetlands typically consist of a bed of porous material which is underlain by an impermeable layer such as a synthetic membrane or natural mate rial such as clay. While these systems often also include plants rooted in the treatment matrix, the water table is maintained below the surface of the bed. The pattern of water flow through SSF systems can be horizontal perpendicular to the inflow and outflow water control structures, vertical moving either up or down through the permeable treatment matrix, or a mixture of vertical and horizontal flow regimes [94,96] Mosquito production from SSF systems is usually not a concern unless clogging of the permeable medium occu rs or the inflow rate exceeds the water-holding capacity of the wetland system and water subse quently pools above the surface of the bed. A third type of constructed wetland s, which is not usually included in the engineering literature that focuses on freshwater treatment syst ems for improving water quality, is ti dal-flow wetlands. Tidal-flow wetlands represent a hybrid appr oach between a natura l wetland and completely man-made wetland. Tidal-flow wetlands are impoundments built to su rround brackish wetlands such as coastal salt marshes and mangrove swamps that are flooded for ex tended periods with a primary goal to reduce the production pestiferous floodwater mosquitoes [97]. S econdary-treated wastewater is used occasionally as a supplement to brackish water to inundate a subs et of these wetlands. Rete ntion of the wastewater provides a dual benefit of water quality improve ment prior to draining seasonally. Rotational impoundment management (RIM) is used to allow tidal flow during a portion of the year and to dry the impoundment during other times annually [98]. Depending on the design, water a nd vegetation management, and water quality, mosquito production can differ appreciabl y among FWS and tidal-flow wetla nds. Constructed wetlands receiving low quality wastewater can produce larg e numbers of mosquitoes. Because treatment wetlands, especially large wetlands, include a variet y of habitats and vegetation types, the mosquito fauna can be quite diverse [95]. Culex species tend be do minant in constructed wetlands treating nutrient-rich wastewater Cx. nigripalpus [95], Cx. erythrothorax and Cx. tarsalis [99]. However, floodwater mosquitoes such as Psorophora spp. and Aedes spp. can be common in systems supporting habitat features that u ndergo frequent inundation and drying. Mosquitoes ( Mansonia spp. and Coquilletidia spp.) with larvae that use their siphons to puncture macr ophytes to obtain oxygen can also be prevalent at wetlands, especially when floating macrophytes or e xposed root systems of emergent macrophytes are present. Anopheles spp. can be common in systems with comparatively low organic loading rates and esp ecially when mats of filame ntous algae proliferate [100].

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Int. J. Environ. Res. Public Health 2012 9 4563 Control of mosquito production from construc ted treatment wetlands is accomplished by a combination of source reduction techniques, such as vegetation management, and utilizing design features such as deep water zone s that reduce mosquito production (bot h discussed in more detail in sections 5.3.2 and 6.6, below), and applica tion of mosquito control agents [101–103]. 3. Mosquitoes 3.1. Mosquito Biology Mosquitoes are true flies of the Order Diptera, with two wings and a pair of halters to aid in flight. These holometabolous insects devel op through four morphol ogically distinct stag es: egg, larva, pupa, and adult (Figure 2). Mosqu itoes can be classified in two broad ca tegories by the type of egg they lay. Floodwater mosquitoes lay eggs on moist surfaces, not standing water, and ther e is a drying out period that is required before the egg can hatch. Perman ent water mosquitoes lay eggs on the water surface and will lose their viability if they dry out. Both floodwater and permanent water mosquitoes occur in wetlands. Figure 2. Mosquito ( Aedes spp.) life cycle. 1. eggs, 2. larvae, 3. pupa, 4. adult. Adult emerging from the pupa is shown between 3 and 4. The larval and pupal stages are strictly aquatic. The larval stage develops th rough four instars, each one progressively larger, feeding until the final days of the fourth instar. The pupal stage is different from many other insects in that th ey are active and swim when distur bed. The pupal stage is typically the shortest, often lasting just a few days.

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Int. J. Environ. Res. Public Health 2012 9 4564 Soon after emergence, mosquitoes begin flight ac tivity. The males and females fly to seek sources of sugars for energy, consuming fl ower and plant nectars, honeydew, juices from decomposing fruits, and other sources [104]. After mati ng, the female mosquitoes feed on blood which is utilized to nourish the developing eggs. Some mo squito species can lay the initial egg batch without a bloodmeal, a biological function known as autogeny [105]. The first egg batch from a non-bloodfed female typically includes a small number of eggs relati ve to the potential. Once a bloodmeal has been consumed, egg batches can include as many as several hundred eggs. 3.2. Why Do Mosquitoes Bite? The morphological structure of the female mosquito mouthparts allows them to pierce the skin of a blood host, probe for a blood vessel, and then imbibe blood. Prior to and simultane ous with the action of taking in blood, saliva is released from the salivary glands. If the salivary glands are infected with pathogens, the saliva can deliver those pathogens to the host. Female mosquitoes feed on blood for the protein cont ent. The protein is util ized to make yolk and to develop the eggs [106]. Some mosquito species are strict in their choice of a blood host. For example, Culiseta melanura a species found in fres hwater swamps, feeds primarily on avian hosts. Other species are generalists and will feed on vari ous readily-available hosts. An example of an opportunistic species is the container mosquito Aedes albopictus which has been re ported to feed on rabbits, deer, dog, humans, cats, squirrels, rode nts, and avian hosts among others [107]. Generally, about three days is re quired for the fully engorged female to digest a blood meal. After this period, and after she lays the developing batch of eggs, she is ready to seek blood hosts once again. She will continue to consume blood meals and la y eggs for her entire life (7–60 days, normally about a month). 3.3. Mosquitoes and Disease When female mosquitoes feed on blood, it is possible that they will feed on hosts that are infected with viruses and other pathogens. If the mosquito is a competent vector of a pa rticular pathogen, after the infected blood meal is digested and an incuba tion period is completed, she can infect new hosts. She continues to bloodfeed for the remainder of her li fe and as the female mosquito ages, she becomes more dangerous, with the ability to infect new hosts simply by probi ng for a blood vessel and releasing saliva. Pathogens of historical and im mediate concern in North Ameri can wetlands include West Nile virus, St. Louis encephalitis virus, eastern equine encephalitis virus, western equine encephalitis, and the malaria Plasmodium parasite. Wetland vectors of importance in maintaining the cycle of these diseases include Coquillettidia perturbans Culiseta melanura Anopheles quadrimaculatus A. hermsi A. freeborni Aedes vexans A. infirmatus A. sollicitans Culex quinquefasciatus C. erraticus C. nigripalpus and C. salinarius. Some of these species feed prim arily on birds and play a role in maintaining the virus in an enzootic cycle. Others are generalists that may be playing some role in the enzootic cycle, but serve a primary role in infect ing mammals and other hosts outside of the wetland areas.

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Int. J. Environ. Res. Public Health 2012 9 4565 Some species are common to specific larval habita ts, however, they are often found outside of what is considered their preferred water source. The ta ble below (Table 2) provi des a list of the North American mosquito species most commonly associat ed with the wetlands types described in this document. Table 2. List of the North American mosquito sp ecies most commonly associated with the wetlands types described in th is document. EEE = eastern e quine encephalitis, SLE = St. Louis encephalitis, VEE = Venezuelan encephalitis, WEE = western equine encephalitis, WN = West Nile virus. Mosquito Species Habitat Nuisance and/or Disease Associations Associated Wetland Type Range Aedes abserratus Freshwater cedar forests Nuisance Atlantic White Cedar wetland forest North Atlantic Coast Aedes atlanticus Floodwater Bottomland swamp Southeastern US; Atlantic and Gulf Coasts Aedes atropalpus Floodwater Riverine Northeastern US, Atlantic Coast Aedes aurifer Freshwater cedar forests Atlantic White Cedar wetland forest North Atlantic Coast Aedes campestris Floodwater Potholes Northwestern US Aedes canadensis Floodwater: temporary shaded woodland pools and shaded pools adjacent to wooded areas EEE, WN, dog heartworm Vernal pools, Atlantic White Cedar wetland forests Atlantic and Gulf Coasts, East of Rocky Mountains Aedes cantator Floodwater Nuisance Tidal salt marshes Northern US Aedes cinereus Floodwater: freshwater cedar forests WN, Nuisance Atlantic White Cedar wetland forests, bogs and swamps Atlantic Coast, Northern and Southeastern US Aedes dorsalis Floodwater: marshes and pools, overflow from wells WEE, WN Tidal salt marshes, coastal wetlands, potholes Western US, Pacific Northwest, Northeastern US Aedes excrucians Floodwater: freshwater cedar forests Nuisance Vernal pools, Atlantic white cedar wetland forests Atlantic and Gulf Coast, Northeastern and Northwestern US Aedes infirmatus Floodwater EEE Bottomland swamp, Mississippi deltaic plain Gulf and South Atlantic Coasts, Southeastern US Aedes flavescens Floodwater Nuisance Potholes Northeastern and Northwestern US

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Int. J. Environ. Res. Public Health 2012 9 4566 Table 2. Cont. Mosquito Species Habitat Nuisance and/or Disease Associations Associated Wetland Type Range Aedes japonicus Floodwater: containers, rock holes, shaded areas with water of high organic content WN Riverine Eastern US Aedes nigromaculis Floodwater Nuisance Playas Western US Aedes sollicitans Floodwater EEE, nuisance Mangrove, tidal salt marshes, tidal brackish East and Gulf Coasts, Mississippi Deltaic Plain Aedes squamiger Floodwater Nuisance Tidal salt marshes, coastal wetlands California, Pacific Northwest Aedes sticticus Floodwater Nuisance, dog heartworm Vernal pools Eastern and Northwestern US Aedes taeniorhynchus Floodwater: salt marsh Nuisance, dog heartworm Mangrove, tidal salt marsh, tidal brackish, Florida Everglades, Mississippi deltaic plain Atlantic, East and Gulf Coasts Aedes triseriatus Floodwater: treeholes, freshwater forests Nuisance, EEE, WN, dog heartworm Atlantic White Cedar wetland forest, Treeholes of deciduous trees Eastern North America Aedes trivitattus Floodwater Nuisance, dog heartworm Meadows, swamps, woodlands Eastern and Central US Aedes vexans Floodwater: freshwater cedar forests Nuisance, EEE Atlantic White Cedar wetland forests, Potholes, playas Continental US Anopheles atropos Permanent water Nuisance Saltwater pools and marshes Atlantic and Gulf Coasts Anopheles crucians Permanent water Malaria Bottomland swamp, Mississippi deltaic plain Southeastern US; Gulf and Atlantic Coasts Anopheles earlei Semi-permanent and permanent water Nuisance Potholes, Bogs, marshes, woodland pools Northern US Anopheles quadrimaculatus and sibling species Permanent Water: freshwater cypress swamps, river backwaters Malaria Bottomland swamp, Mississippi deltaic plain Eastern US; Atlantic and Gulf Coasts Coquillettidia perturbans Permanent Water: Cattail ponds EEE, nuisance Tidal Freshwater (cattails), bottomland swamp, constructed wetlands, Mississippi, deltaic plain Atlantic and Gulf Coasts, Eastern US; Northwestern US

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Int. J. Environ. Res. Public Health 2012 9 4567 Table 2. Cont. Mosquito Species Habitat Nuisance and/or Disease Associations Associated Wetland Type Range Culex erraticus Permanent Water: Freshwater cypress swamps EEE, SLE, WN Bottomland swamps Eastern US; Atlantic and Gulf Coasts Culex erythrothorax Permanent water WEE, WN Cons tructed wetlands West Coast Culex nigripalpus Permanent Water: ubiquitous in fresh water sources; sometimes found in brackish water EEE, SLE, WN Mangrove, bottomland swamp, Mississippi deltaic plain, constructed wetlands, Florida Everglades Atlantic and Gulf Coasts Culex pipiens Permanent water, freshwater forests WN Atlantic White Cedar wetland forests, Constructed wetlands, playas North Atlantic Coast, Northern US Culex quinquefasciatus Permanent water SLE, WEE,WN, dog heartworm Constructed wetlands, playas Southern US Culex restuans Freshwater cedar forests WN Atlantic White Cedar wetland forests North Atlantic coast Culex salinarius Permanent water Nuisance, WN Mangrove, tidal salt marshes, tidal brackish, Mississippi deltaic plain, constructed wetlands Atlantic, Gulf and Pacific Coasts Culex tarsalis Permanent water SLE, WEE, WN Potholes, playas, constructed wetlands Western and Southern US Culex territans Permanent water, freshwater forests None for humans, feeds on cold-blooded vertebrates such as frogs Atlantic White Cedar wetland forests, Potholes North Atlantic Coast, Continental US Culiseta inornata Permanent water and temporarily flooded areas WEE, WN Tidal Salt Marshes (brackish upper marsh), Potholes Atlantic and Gulf Coasts, Continental US Culiseta melanura Permanent Water: freshwater cypress swamps EEE Bottomland swamp; Atlantic White cedar wetland forests, Mississippi deltaic plain Atlantic and Gulf Coasts; Eastern US Culiseta morsitans Freshwater cedar forests EEE Atlantic White Cedar wetland forests North Atlantic Coast Deinocerites cancer Crab holes in tidal marshes Nuisance Tidal salt marshes Eastern Coast of Florida Deinocerites mathesoni Crab holes Nuisance Tidal salt marshes South Texas Coast

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Int. J. Environ. Res. Public Health 2012 9 4568 Table 2. Cont. Mosquito Species Habitat Nuisance and/or Disease Associations Associated Wetland Type Range Deinocerites pseudes Crab holes Nuisance Tidal salt marshes South Texas Coast Mansonia dyari Permanent water Nuisance Constructed wetlands Florida Mansonia titillans Permanent water VEE, nuisance Constr ucted wetlands Florida to Texas Psorophora ciliata Floodwater Nuisance Rain-filled pools Eastern US Psorophora ferox Floodwater Nuisance Woodlands, potholes Eastern US Psorophora signipennis Floodwater Nuisance Playas Central US Uranotaenia lowii Semi-permanent and permanent water; shallow margins of lakes None for humans— Feeds on amphibians Bottomland swamp Southeastern US Uranotaenia sapphirina Freshwater Cedar forests, Permanent pools and ponds None for humans Atlantic White Cedar wetland forests, Bottomland swamp North Atlantic Coast, Eastern US Wyeomyia smithii Pitcher plants None for humans Bogs, fens Northeastern US Wyeomyia mitchellae Bromeliads Nuisance Florida Everglades Southern Florida Wyeomyia vanduzeei Bromeliads Nuisance Florida Everglades Southern Florida 4. Mosquito Control 4.1. Strategy Mosquito control in wetlands can become necessary for a variety of reasons. Foremost among these is prevention of diseases caused by mosquito-transm itted pathogens such as West Nile virus, eastern equine encephalitis virus, and many others. More frequently, however, cont rol is required because mosquito production from these areas can significantly impact quality of life and local economies [1] although there still exists a need to recognize that “ quality of life” r easons for mosquito abatement are perfectly valid. Often local politics play a major role in mosquito control decisions. Mosquito control, as a technology-based endeavor, should be science-based. However, in modern societies science is seldom applied in a vacuum and social, political, ec onomic, legal, and other considerations also contribute to decisions regardi ng the use of technologies, particularly in the public sector. These factors can influence mosquito c ontrol in different ways. For example, economic considerations may result in mosqui to control being applied unnecessari ly as when an important tourist or revenue-producing event is about to occur rega rdless of mosquito popul ations, or against a

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Int. J. Environ. Res. Public Health 2012 9 4569 non-pathogen transmitting species when disease transmi ssion has been reported in an area. Conversely, necessary mosquito control may sometimes be preven ted by pressure from indi vidual citizens or from local, regional, or nationa l groups or organizations. 4.2. Surveillance Responsible mosquito management should start with an effective su rveillance program. We recognize two fundamentally different types of surv eillance in mosquito management: (1) mosquito abundance surveillance, and (2) mosquito-transmitte d disease surveillance. The former is usually carried out by professional mosqu ito control programs or local pe st/animal control departments, whereas the latter is more often carried out by local, st ate, or federal health agencies. Here we will deal only with the first type. See Moore et al. [108] and Rutledge [109] for general information and examples of disease surveillance guidelines. Ideall y, both types of surveillance programs should be integrated to formulate risk assessments that help make informed decisions for mosquito control before a public health emergency occurs. The basic objective of a mosquito surveillance progr am is to establish baseline and contemporary data bases of mosquito population sizes and specie s composition, identify breeding/resting habitats, establish temporal and sp atial patterns of abundance, and determin e nuisance levels. Surveillance data are then used to evaluate the mosquito situation, to guide daily mosquito control operations including determining when and where treatment is necessar y, and to evaluate the effectiveness of control measures. Inclusion of spatial data (mosquito-produc ing locations), physical data (e.g., temperature, rainfall, tide information, vegetation cover, etc. ), and other variables known to affect mosquito ecology and behavior is often essential for an effective program [110]. Many mosquito surveillance programs also include an environmental monitoring component, particularly where habitat modifications, and/or water management for mosquito control are be ing employed (e.g., Boyce and Brown [111], Connelly and Carlson [97]). Surveillance protocols should be tailored to local needs, and will differ depending upon local mosquito problems, habitats, climate, and resources A clear definition of which local mosquitoes represent a potential problem (nuisance, economic, health, etc. ) and monitoring the production and abundance of these species in space and time shoul d form the foundation of mosquito surveillance programs. Successful programs incorporate immatu re and adult mosquito sampling to estimate mosquito abundance. Larval/pupal surveys are used to sample immature mosquitoes, whereas landing rate counts and a variety of trap ping techniques are used to samp le adult mosquitoes. Specific techniques for each will differ depending upon mosquito species, habitat, weather, etc. [112], but in general it is recommended that a combination of techniques be us ed to assure thorough sampling. Often, citizen reports/complaints can form an important part of the surveillance protocol and can help identify and temporally fill gaps in the program. Ideally, surveillance, environmenta l, physical, and spatial data shou ld be integrated with control data in a geographical information system that allows near-real-time analysis of the various data sets and their interactions in a spatial context to help guide day to day mosquito abatement operations and evaluate their effects. In some cases GIS/GPS assi sted surveillance and contro l operations can result in increased efficiency and precision, better mosquito control, and can provide automatic documentation

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Int. J. Environ. Res. Public Health 2012 9 4570 for permitting and other reporting/regulatory purposes thus conserving resources and reducing the environmental impact of mosquito control [113]. 4.3. Risk Assessment Sound mosquito control strategies should originate from risk assess ment procedures that clearly identify the (mosquito) problem, the possible mitigati ng (mosquito control) actions, and the anticipated adverse effects of each. The modern art and science of risk assessment or iginated in the 1970s from the urgent need to regulate pollution and has evolved co nsiderably since then (see Calla han and Sexton [83] for a concise review). Two major types of risk assessment schemes th at are directly relevant to mosquito control in wetlands are: ecological risk assessment —the process for evaluating how likely it is that the environment may be impacted as a result of exposur e to one or more environmental stressors such as chemicals, land change, disease, invasive species, and climate change; and health risk assessment —the process used to estimate the nature and probability of adverse health effe cts in humans, domestic animals and livestock who ma y be exposed to chemicals (in this case mosquitocides) now or in the future. In the present context, health risk assessment also in cludes risk of infection wi th a mosquito-transmitted pathogen (see below). Mosquito control entities are also tasked with assessing the nuisance/quality of life effects of local mosquito production. Even though “risk” is not necessari ly a quantifiable entity, most cu rrent risk assessment frameworks assume that risk can be measured and expressed quantitative ly [114]. This is partly a result of legal considerations, particularly the 1980 Supreme Court’s “Benzen e Decision” (Industrial Union Department, AFL-CIO vs. American Petroleum Institute) which emphasized the notion that quantitative demonstration of risk was a pre-requisite for regulator y intervention [115]. Particularly germane to this discussion is the fact that, often, th e principal goal of mosquito control operations is to reduce mosquitoes to below nuisance levels, but we r eally do not have a clear definition of what those levels are [116]. Disease prevention is generally a much less frequent need in North America. Formal risk assessment methodology is constantly changing in response to new technologies, evolving and emerging environmental challenges, a nd ever-changing societal pressures. Currently, issues such as challenges presen ted by climate change, new chemi cals affecting endocrine system functions, new strategic soci etal priorities, and concern about cumulative risk assessment are forcing a re-examination of methods and techniques for formal risk assessment [114]. Many current risk analysis methodologies do not deal well with second, third, and higher order effect s that may reinforce or offset the more obvious effects of a proces s or action under analysis [117]. Given the above, a formal qualitative risk assessment for mosquito control may not necessarily be desirable in many cases. Ideally, however, the followi ng risk assessment and risk management issues must be evaluated before any significant wetlands mosquito control action is undertaken: Risk Assessment: (1) The mosquito production profile of the target wetland (based upon an effective surveillance program). (2) How local and re gional wetlands fit into the overall mosquito problem. (3) What is the affected population (human and animal)? (4) What ar e the consequences of not managing mosquito production from the wetland in question? Risk Management: (1) When a mosquito problem becomes severe enough to warrant intervention that impact wetlands and/or human

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Int. J. Environ. Res. Public Health 2012 9 4571 or animal health. (2) What potential control strate gies are appropriate for the area? (3) What the anticipated impacts of the different c ontrol strategies are. (4) Can a step -wise or integrated approach be devised that employs only the minimum response necessary for a given situation? (5) How the performance of the control activities will be mon itored and reported. (6) Design and implementation of an outreach campaign that engages locals and teach es residents (including public officials) about wetlands, mosquitoes, local control activities, and personal protection. These and other issues, depending upon circumst ances, should form the basis for a mosquito management plan for any given area that should be formulated a priori and that should consider routine as well as emergency management scenarios. This plan should be thought of as a work in progress, to be revised and modi fied as experience dictates or changing circumstances require. The plans should include guidelines and information on the surveillance and cont rol of mosquito-borne pathogens, flexible risk assessment and decision s upport system models, a desc ription of surveillance and control activities associated with virus transmi ssion risk level, and elucidation of the roles and responsibilities of local and stat e agencies involved with mosquito borne virus surveillance and response [118]. Response plans for what are c onsidered nuisance mosquitoes should also be developed. Ideally, such plans would allow vector c ontrol agencies and wetland managers to plan and modulate control activities to best represent the local conditions a nd surveillance methods as well as meet the objectives of wetland management. The effi cacy of response plans to lessen mosquito related problems needs to be assessed. More specifically, mosquito management plans incorpor ating adult mosqu ito control must be flexible to accommodate changing risk levels associated with decision-maki ng criteria and to a ddress unforeseen changes in factors not cons idered routinely as part of the decision-making crite ria. The decision-making matrix of adult mosquito control programs often incorporates seven factors [111,119,120]: (1) initiation criteria, (2) treatme nt area delineation, (3) land use pr actices including the presence of sensitive species, (4) meteorological conditions, (5) c ontinuance criteria, (6) termination criteria, and (7) additional factors that influence implementation of the plan. Additional factors could include unforeseen biological or environm ental conditions in the wetlands, introduction of a novel invasive disease vector or pathogen, changes in legislati on and/or regulations, availability of economic resources or equipment for mosquito control, ava ilability of suitable adulticides, changes in the susceptibility of immature mosquito populations to larvicid es (evolution of resistance), or a natural disaster. The thresholds for control actions are determined primarily by three factors: (1) initiation criteria trigger the initiation of adult mosquito c ontrol application measures ; (2) continuance criteria trigger additional applications in an area that has previously attained an initiation criterion. These criteria are considered until a termination criterion is achieved for a treatment area. (3) Termination criteria include adult mosquito control application measur es in a treatment area until initiation criteria are again met by the surveillance program. Thresholds for control actions will differ as a function of the surveillance methods being employed, the mosquito species, the lands cape and location, presence of pathogens in th e mosquito vectors, disease activity in the pathogen reservoirs and su sceptible animals, as well as the aforementioned factors of the decision-making matr ix. Thresholds for action incorporat ed into public health codes and regulations that must address mosquito producti on across all potential habita t types are stringent by necessity. For example, the presence of one mosquito larva in larval surveillance may be sufficient to

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Int. J. Environ. Res. Public Health 2012 9 4572 trigger legal abatement proceedings. From a practical standpoint, the cost of abatement to achieve the elimination of all mosquitoes might be too high and the risk to public health or the nuisance activity from mosquito biting might be too low to merit inte rvention at this level. The immature mosquito abundance that triggers abatement efforts coul d range from an average of 0.2 for salt marsh mosquitoes, 0.25 mosquito larva/dipper sample for vectors of human malari a in floodplain wetlands and ricefields to 1.0 la rva/dipper sample for vector s of arboviruses in wetla nds of waterfowl hunting clubs. Treatment thresholds could be <0.2 larva/dippe r sample for historically problematic mosquito developmental sites or where mosq uito production per unit surface area is low but huge expanses of inundated habitat are present. These thresholds w ill be lower when pathogens are prevalent in the mosquitoes and/or disease activity is detected in sentinel animals and in wildlife, human and companion animal populations. Because the area of water in mosquito developmental sites often changes over time, the abundance of mosquito immature s in samples will increas e as the water surface area decreases and concentrates the mosquito im mature stages; a single threshold of immature mosquito abundance to trigger abatement activitie s is probably ill-advised under such conditions. Likewise, the abundance of adult mosquitoes that triggers the initiation and continuance of abatement activities differs among habitats and ongoi ng pathogen activity. For example, in agricultural wetlands in the Central Valley of California, 100 female Culex tarsalis or 150 female mosquitoes of any genus ( Aedes Anopheles Coquillettidia Culex Culiseta Ochlerotatus or Orthopodomyia ) or 200 female mosquitoes in total co llected during a single night or for three consecutive days by a carbon dioxide-baited trap will trigger abatement ac tivities [80]. If New Jersey light traps (without carbon dioxide bait [81]) are used for adult mosquito surveillance, then only 10 female C. tarsalis or 25 female mosquitoes of any genus ( Aedes Anopheles Coquillettidia Culex Culiseta Ochlerotatus or Orthopodomyia ) or 50 female mosquitoes in total for thr ee consecutive days (and nights) will trigger abatement activities. Moreover, if 1-minute sweep net samples or landi ng-count collections are used as the surveillance method, then 10 female Aedes or Ochlerotatus and/or 25 total female mosquitoes will trigger abatement ac tivities [80]. If arbovirus activity is detected, then the treatment thresholds decrease by 75%. While 100 or more female C. tarsalis collected per trap-night in traps deployed at rice fields tri ggers abatement activities, a dozen indivi duals collected in a trap in an urban area could be indicative of the need for abatement activities in a wetland in a nearby park or in a riparian zone. Establishing thresholds for mosquito control inte rventions is further comp licated because, unlike agricultural systems where actual measurable indicato rs such as pest density or crop damage are directly relevant, individual perceptions and indi vidual nuisance tolerance, both highly subjective and variable entities, must often be factored into mosquito contro l decisions. Furthermore, unlike agricultural crops, where economic losse s due to pests are directly quan tifiable in terms of crop losses and their corresponding dollar value, costs of mosquito infestations must be calculated in terms of quantities such as tourism and business losses, qualit y of life degradation, costs of human and animal diseases, and other equally indirect and often subjective variables. Mosquito management when local arbovirus transmi ssion is likely or has been demonstrated is a particularly tricky situati on. First, the concept that only one or a few mos quito species are capable of transmitting a particular pathogen is not easily accepted by the public so during disease-transmission events mosquito agencies are often tasked with cont rol of mosquito species that would normally not be

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Int. J. Environ. Res. Public Health 2012 9 4573 targeted. Second, even though in many cases the indi vidual probability of bei ng infected, even during documented transmission events/outbreaks, is low [121–123], intensive vector control may still be required because even a single disease case is ofte n deemed locally unacceptable, a resulting death unfathomable, and the social and economic ramificati ons of local disease transmission for the local community considerable [124–127]. 4.4. Community Relations An integral part of mosquito management is co mmunity outreach and education [128]. This activity includes three major components: (1) Public education about mosquito biology, ecology, and disease transmission; (2) Public outreach on local mosquito control operations; and (3) Continuous education of mosquito control workers on mosquitoes, mosqu ito control practices, and professional conduct. The first two help eliminate misconceptions about mosquito es and mistrust of local agencies charged with mosquito management whereas the third makes mos quito control workers sour ces of information for the public and effective community ambassadors for th eir agencies. A better informed public will also be able to identify and eliminat e sources of mosquitoes around the home, and take steps to reduce human contact with mosquitoes [129]. 4.5. Personal Protection In most pest control operations, a 90% reduction in the target pests is usually considered a success but in mosquito control, citizens can still be freque ntly bitten by mosquitoes after a 90% reduction in the mosquito population. Citizens must understand th at personal protection such as the use of repellents and protective clothi ng, avoidance of mosquito produci ng habitats, reduction of outdoor activities during peak mosquito activity periods, and other precautions may still be necessary, particularly during diseas e transmission episodes. 5. Transient Methods of We tlands Mosquito Control 5.1. Chemical Control Use of chemicals for controlling wetlands mosquito es should be undertaken only as part of an integrated pest management pla n, and exclusive reliance upon pestic ides is strongly discouraged. Chemical control of mosquitoes is by nature temporary and rarely 100% effective so it generally needs to be repeated in time to maintain adequate control. Insecticides can be applied to control mosquitoes during their immature stages (l arvae and pupae—larvicid es/pupacides) or duri ng the adult stage (adulticides). It is generally agr eed that larviciding is more eff ective than adulticiding because the aquatic immature forms are constrained within a water body where they are usually easily accessible, relatively immobile, and unable to escap e. Flying adults on the other ha nd tend to be widely dispersed, often inaccessible, and highly mobile, and usually requi re adulticides to be a pplied over a larger area than larvicides. Furthermore, adults often tend to exist in closer proximity to humans than their larval counterparts [130]. Application of mosquitocides in wetla nds should always be based upon conditions previously defined in a mosquito management pl an, and documented via an effective surveillance program. Relative to other classes of pesticides such as those used in agricultu re or horticulture, public

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Int. J. Environ. Res. Public Health 2012 9 4574 health pesticides (including mosquitocides) are very limited in number. Pesticides for mosquito control occur in several chemical families, including organophosphates (e.g., Malathion), and pyrerthroids (e.g., permethrin). Other mosquitocides not easily clas sified by chemical family include insect growth regulators (IGR—e.g., methoprene), ne onicotenoids and chloronicotinyls, microbial pesticides (e.g., Bti) and surface oils and films. Larvicides can be applied using a wide variety of techniques incl uding manually or with equipment mounted in trucks, boats, and all-terrain vehicles. The principal larvicides currently used in the U.S. for mosquito control include methoprene several microbial agents, temeph os, and various su rface oils and monomolecular films. Methoprene is an IGR that mimics juvenile hormones of mosqu itoes and other insects and prevents mosquito pupae from emerging into adults. It is effective in both fresh and salt water habitats. Microbial larvicides include Bacillus thuringensis var. israelensis (Bti), a naturally-occurring soil bacterium that is toxic to mosquitoes. The t oxins are activated by gut enzymes of dipterans, particularly mosquitoes, black flies and midges so it is highly selective. Bti is effective in most habitat types. Another naturally-occu rring bacterial larvicide is Lysinibacillus (formerly Bacillus ) sphaericus (Ls) which is slower acting than Bti, but can r ecycle in nature and is thus more persistent. Temephos is an organophosphate that is currently labeled for use in wetlands and has been used for mosquito control since the mid-1960s. Various types of surface oils have b een used for mosquito control since the 1800s. They work primarily by suffocating the immature mosquitoes. Monomolecular films (MMF) are surfactants that reduce the surface tension of the wa ter body and cause mosquitoes to drown. MMFs can also be effective against emergi ng adults and those that use the water surface for resting and drying their wings after emergence. Mosquito adulticides are generally applied as lo w-volume sprays or ultralow volume (ULV) mists. Product droplets sprayed by ULV equipment are very small and thus stay alof t for long periods, thus exposing actively flying adult mosq uitoes to the pesticid e longer than standard spray droplets. ULV equipment can also be mounted in a variety of terres trial, aquatic and airborne vehicles. Thermal fogs, were commonly used in the past for both ground and aerial control of adult mo squitoes, but currently the method is only infrequently used to treat very small, usually i ndoor or peridomestic, areas via handheld equipment (e.g., [131]). Common products used for adult mosquito control include malathion and naled (organophosphates) and permethrin, resmethr in and sumithrin (synthe tic pyrethroids). These chemicals are usually applied in very small concentrations thus minimizi ng non-target effects [132,133]. In addition to documenting the need for adult mos quito control and selecting the appropriate chemicals and equipment, application timing is critical for adult mosquito control because adulticides must be applied when mosquitoes are active and exposed. Generally, this is during dawn, dusk an d early nighttime (19:00– 24:00) hours. Different sp ecies of mosquitoes ar e active at di fferent times (e.g., [134–136]) and environmental conditions also critically affect mos quito activity patterns [137–140]. Furthermore, it is essential to apply the chemicals und er favorable weat her conditions ( i.e. no rain, no thermals, wind speed <10 mph) to maximize efficacy and minimize drift of the product outside the target area. As previously stated larvicides tend to be more focused in their applicati on and are generally more specific than adulticides. Adulticides are applied ove r larger areas and have greater potential to impact other flying insects and nontarget organisms. However, adulticide s are applied at lo w concentrations of active ingredient and often at times when othe r organisms are not active thus minimizing exposure to non-target species. All larvicides and adulticides must be registered with the U.S. Environmental

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Int. J. Environ. Res. Public Health 2012 9 4575 Protection Agency and state pesticide agencies before they can be applied. A series of rigorous studies must be conducted on the efficacy of the product, environmental fate, and impacts to other organisms before a product is considered for registration. Ther e are also an extensive number of published studies by independent researchers on the laboratory and field efficacy of these products as well as impacts to non-target organisms. By and large, the vast majority of these studies conclude that, when applied at label rates and under favorable operational conditions, bo th larvicides and adulticides have negligible impacts on non-target organisms. The National Pollutant Discharge Elimination Sy stem (NPDES) is a recent Federal permitting program that regulates point source discharges from pesticide applications to waters in the United States and requires all a pplicators to obtain a Pesticides Ge neral Permit (PGP) before applying pesticides. The system will greatly affect the applicat ion of chemicals for mosquito control to wetlands within the United States. There has been considerab le debate over this issu e as the regulations and requirements for application of mosquito pesticides to or over aquatic habita ts are already covered by the Federal Insecticide, Fungicide and Rodenticide Act (FIFRA). The PGP requires all operators to minimize pestic ide discharges (by using the lowest effective amount of pesticide, preventing l eaks and spills, and calib rating equipment) and monitor for and report any adverse incidents. Operators who exceed the annual treatment area threshold must also submit a Notice of Intent (NOI) for coverage, implement inte grated pest management practices to minimize the discharge of pesticides to waters of the U.S., develop a Pesticide Discharge Management Plan, submit annual reports, and maintain reco rds of pest control practices. Inquiries to mosquito control officials in Florid a reveal that major impacts as of February 2012 include mostly time spent in compliance, which translates into manpower and additional expenses. Estimates of increased workload for implementation ra nge from 5% to 20%. It is apparent from some of the comments that the NPDES will represent a greater burden to small mosquito control entities such as small municipalities or private organizatio ns than to large ones. Also in some instances mosquito control entities are faced with complia nce/coordination with several NPDES plans, for example, different county agencies may have thei r own plan which must be coordinated with the county’s plan, and perhaps with those of other county agencies. Several agencies reported that they had to invest in inexpensive GIS t echnology to automate the NPDES r ecord-keeping requirements. None of the agencies contacted have experienced non-targe t impacts so the burden to mosquito control of that aspect of the new reporting requirements is not known. However, in some locations the cost of water tests and of monitoring for non-target effects has been substantial (per s. comm., David Brown— Manager, Sacramento-Yolo Mosquito and Vector Control District). 5.2. Biological Control There are several biological agents that have been show n to cause mortality in mosquitoes including algae [141,142], oomycetes [143,144], bacteria ( Bti Ls and recombinant bacteria) [145,146], microsporidian and gregarine parasites [147,148] pathogenic viruses [ 145], nematodes [149], predatory insects [150,151] including other mosqu itoes [152,153], copepods [154,155], fish [156,157] and others. For general revi ews of biological control of mosquitoes consult Ch apman [158], Floore [159], and Rey [160].

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Int. J. Environ. Res. Public Health 2012 9 4576 One environmentally-attractive char acteristic of biocontrol agents, particularly of pathogens and parasites, is their specificity. These organisms genera lly attack one or a few closely related species thus minimizing the potential for non-targe t effects. This specificity, howev er, also severely limits their potential market, which together with the usually high start-up co sts for new products, often makes their commercialization difficult. Issues that need to be addressed when embarking on a biological control program against mosquitoes include the response of the bioc ontrol agents to pollution, their mechanisms for surviving drought periods, their me thod of recolonization of the target habitat following population crashes, their tolerance of pes ticides including herbicides and their anticipated interactions with local fauna. Further difficulties with the use of biological agents include varyi ng control efficiencies depending upon environmental conditions; the known dangers of introducing exotic species into nature or overusing native ones [161]; mass production, storage, and transport limitations; and lack of efficient delivery methods [158,159,162]. Other issues that must be considered when evaluating biological control of mosquitoes incl ude determination that the anticipated reduction in mosquito populations will be adequate in terms of reducing nuisance/quality of life impacts and/or the risk of disease transmission [163–165] and if dens ity dependent compensatory or overcompensatory responses to reduced larval density could resu lt in no changes or even increases in the mosquito population as a consequence of attempted biological control [166]. For these reasons, biological agents (except for Bti and Ls formulations) will not be the exclusive method of mosquito control in the n ear future except in very small ar eas. Biological agents, however, should continue to form an integral part of IPM protocols for mosquito control (see below). Without doubt, the mosquitofish Gambusia affinis and G. holbrooki are two of the most common biological control agents used for mosquito control but may pose problems if introduced as exotic fish (see later). These hardy species are extremely adaptable and efficient mo squito control agents if they have access to the larval habitats, and have been introduced for mosquito control throughout the world during the past 100 years [157,158]. Un fortunately, introduction of thes e species where they are not native can have devastating consequences to loca l ecological systems [167–170] so there continues to be an active search for local larvivorous fish speci es adapted to the appropriate habitats for use in mosquito control programs [157,171–173]. Mass produc tion, storage, transport, and deployment of predaceous fish are areas where significant technological advances are still needed. Cyclopoid copepods are another group of organi sms recognized as mosquito predators [174,175]. They have proven extremely effective in eliminating Aedes mosquito production from container habitats such as water storage vessels and di scarded containers [155,176,177]. Copepods are easy to mass produce and transport and can li ve for long periods in aquatic ha bitats [155]. They can survive on other prey when mosquito larvae are not availa ble but the presence of alternate food does not significantly compromise their effici ency for mosquito control [178]. The efficacy of copepods in open water habitats such as wetlands is less well documen ted. They have been found effective in temporary pools and Louisiana marshes [154], rice fields [179], and in road side ditches and some polluted habitats where larvivorous fish are lacking [180]. Use of fi sh is often more effici ent in large open water habitats but copepods may still have a place to comple ment fish predation or in inaccessible areas or where fish are not present or hard to maintain [ 130]. As with other planktonic animals, the bodies of

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Int. J. Environ. Res. Public Health 2012 9 4577 copepods can harbor diseas e-causing bacteria such as Vibrio cholera [181] and Enterococcus spp. [182] and some authors recommend filtering water containing copepods before drinking [183]. 5.3. Habitat Management 5.3.1. Water Management High water flow rates and volumet ric turnover rates can negatively influence mosquito production, but the flow rates needed to directly impact mosqu ito populations are too high to be of use as a sole technique for mosquito control (s ee below). Indirectly, however, water flow and turnover rates can impact mosquito populations by reducing or increasing stagnant pools of organicrich waters that are attractive to certain mosquito species, particularly several Culex species [95,184] and by influencing water quality variables that are important for the survival of mosquito la rval predators such as larvivorous fish and aquatic invertebrates. Various water manipulation technique s can also be used for vegetation management to eliminate some mosquito producing locations a nd to enhance predator access to others (see below). We note that wetlands hydrology is intimately connected with a multitude of ecological processes including vegetation com position; primary production; salinity and oxygen regimes; nutrient cycling; microbial dynamics; se diment transport; plankton, benthos, and nekton composition and population dynamics and many others [13, 185–187]. Thus, artificial modification of wetlands hydrology should be undertaken with great care as it can severely impact wetland structure and function. 5.3.2. Vegetation Control Vegetation management, as it relates to mosquito c ontrol, is undertaken to create open water areas that are unfavorable for mosquito development or resting habitat [99] and to increase predation pressure on mosquito larvae [188] This technique is most relevant to constructed wetlands, and is particularly important to consider during the design phase of the wetl ands creation process. Vegetation provides food resources for mosquitoes in the form of plant detritus and also fosters the production of other mosquito food such as bacteria, algae, and pr otozoa [189,190]. Thick vegetation stands also may reduce water flow thus reducing physical disturban ces such as high currents, eddies, and waves that can negatively impact developing mosquito la rvae [190]. Reduction of vegetation coverage can significantly reduce mosquito popula tions [191–193], but the plant specie s, the method of vegetation thinning, and the spatial configura tion of the remaining vegetation can have significant impacts upon the magnitude (or lack thereof) of the resultin g mosquito population reduction [190]. For example, limiting vegetation coverage by using deep open water zones is probably more effective for mosquito control than periodic vegetati on thinning [190,192,194]. Emergent ve getation usually recolonizes cleared areas quickly and there tends to be a fl ush of mosquito production after re-inundation of the marsh which offsets any reduction brought about by the ephemeral limitation of vegetative cover. Likewise, Lawler et al. [193] recommend using a combination of he rbicides and disking rather than plain mowing (or grazing) due to rapid grow back of the vegetation. A lthough vegetation cover reduction can often be beneficial for wildlife and compatib le with natural resource management goals [95,195], many important wetland functions such as water quality and wildlife habitat enhancement, are

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Int. J. Environ. Res. Public Health 2012 9 4578 dependent upon wetland plant coverage, diversity, and productivity [9] a nd could suffer with reductions in vegetation cover. Once again flexibility, compromise, and effective mosquito surveillance are essential for environmentally s ound mosquito control via vegetation management. 5.3.3. Emergent Vegetation Control A wide variety of techniques can be utilized for vegetation management in wetlands. These include selective removal (by plant species or marsh location), controlled burn ing [196], herbicide application, mowing and disking, grazing and other mechanic al removal techniques [56,197], water level manipulations [198], and combinations of the above. 5.3.4. Aquatic (Submerged and Floating) Vegetation Control Several mosquito species, particularly Mansonia and Coquillettidia species use aquatic plants for oviposition and for respiration during immature development. Conventional mosquito control techniques such as surface films, larviciding, and biological control are usually not effective because of the great degree of shelter afforded by the usually thick mats of vegetati on [199]. In such cases, vegetation removal or reductions in its coverage are the only alternatives to reduce mosquito populations. Mechanical harvesting of the vegetation using equipmen t such as aqua tic harvesters, cranes, aquatic weed trimmers, and hand tools is routinely utilized, but coverage is limited to areas accessible to the equipment, and applica tion to large areas can be expensive. Herbicides can be used for aquatic plant manageme nt and can be applied aer ially, from land-based, vehicle-mounted equipment, from boats, or “ma nually” using back-pack sprayers. The chemical herbicides are usually specific for one or a few aqua tic plants. For example, Diquat is used against water lettuce ( Pistia stratiotes ), and 2,4 amine is used to control water hyacinths ( Eichhornia crassipes Eichornia spp.). Some biological control agents for aquatic plants such as the mottled water hyacinth weevil ( Neochetina eichhorniae ) and the water lettuce weevil ( Neohydronomus affinis ) have been utilized successfully in the past. The Salvini a weevil ( Cyrtobagous singularis ) has been effective in Australia [200], and several lepidopterans have been effective against milfoil ( Myriophyllum spicatum ; [201]), but large scale applica tions have been few and new ag ents and much more research are needed before the technique beco mes reliable and co st-effective [202]. 6. Long-Lasting Wetlands Modifi cations for Mosquito Control Source reduction denotes techniqu es used to reduce mosquito popul ations by eliminating their oviposition and/or immature rearing sites, or by making habitats less conducive to mosquito production. Some of the techniques al ready discussed, such as aquatic vegetation control, are examples of source reduction techniques. In this section, howe ver, we will deal with more enduring techniques. Long-lasting approaches to source reduction are often more economical than temporary control and if effective, eliminate or drastically reduce the need to use pesticides [203]. Some of these techniques, however, also have negative environmental impacts a nd tradeoffs will always need to be considered before their implementation in an y given area. The most commonly used wetlands source reduction techniques include filling, d itching and runneling, impounding, open marsh water management, and

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Int. J. Environ. Res. Public Health 2012 9 4579 the already mentioned topographic modifications to manage submerged and emergent vegetation, mostly in constructed wetlands. 6.1. Filling In the past, filling wetlands to prevent mosquito breeding was an acceptable technique, particularly in wetlands close to populated areas or near ne w developments [11,204]. Since the “no net loss of wetlands” pledge by President Bush Sr., in 1986 it has become increasingly difficult to obtain permits for outright filling of wetlands for any reason and wh en they are issued they are accompanied by a mitigation requirement. The mitigation process, however is highly flawed because of lack of oversight of the mitigation, in particular la ck of criteria to evaluate mitiga tion success [205,206]. Because of the outright habitat and wetlands function losses, filling of wetlands fo r mosquito control is not considered an option in the present day. 6.2. Ditching Ditching wetlands as a mosquito cont rol technique has been in use at least since the turn of the 20th century [187]. Large wetlands expanses were ditched during the 1930s as part of work relief programs. This often included many low marsh areas that did not produce mosquitoes [207,208]. The standard procedure at the time called for shallow parallel ha nd-dug ditches (grid ditc hing) at approximately 200 linear m per ha [208]. Estimates of the extent of coastal wetlands ditching include over 90% from Maine to Virginia [209] and 94% along the New England coast [210]. In theory, ditching can reduce mosquito produc tion by lowering water tables, reducing the number and size of water-holding depressions, and enhanc ing access by predatory fish to developing mosquito larvae. A properly designed ditch system can reduce the mosquito popu lation using fish as biocontrol agents therefore reducing the need for pesticide inte rvention. Regular maintenance of the system will prevent the development of mosquito habitat, and th e marsh can continue to be attractive to wildlife [211]. However, frequently, considerable mosquito producti on still occurred in grid ditched wetlands because ditches usually did not specifically ta rget the mosquito producing areas [1 16]; considerable breeding still occurred in the areas between th e ditches [11]; and many of the d itches quickly silted-in, sometimes creating isolated depressions wh ere prodigious numbers of mosqu itoes could be produced [207]. Ditching can profoundly cha nge the nature of the impacted wetland [209]. By lowering the water table, ditching can transform a wetland into an upland habitat a nd can promote invasion by exotic plants [212]. Ditching can also significantly imp act numerous wetland func tions [187] and biota including vegetation [209], nekt on, plankton, and bentho s [187,213,214], terrestria l invertebrates [215], birds [216], and many others. Artifici al ditching can also result in loss of open water habitat on the marsh surface [217]. Spoil associated with conventi onal ditching can be a significant impact on marsh ecology by interfering with natural marsh hydrology and providing additional substrate for upland plant species and weedy exotics [212]. In many areas existing ditch systems must be maintained for a variety of reasons includ ing water management, flood control, and mosquito control. For example, in Cape Cod, many (freshwater) ditches must be main tained by local mosquito control agencies where houses, roads, etc. have closed off creeks. These ditches are the only way water is carried from fresh to salt water. In some areas, mosquito control also assi sts with the maintenance of herring runs (pers. obs.

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Int. J. Environ. Res. Public Health 2012 9 4580 GESH). Further, there are a large number of mainte nance projects (with rakes or rotary ditcher) that are undertaken to maintain ditches on salt marshe s. These projects limit the salt marsh mosquito populations leaving only small areas of larval habitat that can be treated with backpack sprayers using Bti. The local tidal tidal range is probably a huge factor in the success of the ditch maintenance program. Tidal ranges can be over 11 ft on a spri ng moon tide in coastal Massachusetts. Large tidal ranges drive the movement of water into and out of the marshes with significant momentum helping to keep outlets open and water levels low at th e lowest tide cycles (pers. obs. GESH). Ditching can also be used as a restoration technique for impacted wetlands. For example, in Florida, many coastal wetlands that were impounded for mos quito control have been re-connected to the estuary by using limited and directed ditches to control mosquito production [3,176,181]. These ditches are normally cut using rotary equipment that distributes the sp oil as a very thin layer on the marsh surface. Although the remedy is not ideal, reconnection the adjoining estuary allows interchange of organisms and nutrients between both system s and often significantly improves environmental conditions in the former impoundment ([6], see below). 6.3. Runneling Runneling is a technique developed in the 1980s a nd used predominately in Australia to control mosquitoes in intertidal salt marshe s with no existing modifi cations for mosquito cont rol. Runnels are very shallow (>0.3m) spoonshaped channels that are c onstructed to follow natural water flow patterns [218]. The runnels are used to connect mosquito breedi ng depressions to a tidal source, thus increasing aquatic predator access to the de veloping larvae, and flushing out immature mosquitoes from the marsh before they can complete their development (see OMWM below). Runneling has fewer environmental impacts than conve ntional ditching and can be very effective in controlling mosquitoes [219,220]. It is particularly effective in acid sulfate soils, where deeper substrate disturbance could create significant acidity problems (e.g., [2 21]). Because of the increased flushing, physical conditions in areas near runnels often resemble those of slightly lower areas [219]. Morton et al. [222] suggest that runneling actually enha nces marsh-associated fish populations by increasing habitat access, and improving nutrient exchange between marsh and estuary. Chapman et al. [223] found little effect of runneling upon marsh crab populatio ns except for a shift in species composition. Runneling can also sometimes lower wate r tables and salinities, particularly near the runnels [224]. Long term (>20 yrs.) effects tend to parallel those described above, and appear to be small, yet often statistic ally significant [225]. The maintenance costs of the runnels vary depending upon runnel system design and location [219], but are generally low [225]. 6.4. Open Marsh Water Management (OMWM) OMWM is a technique developed in New Jersey in the 1960s for control of high salt marsh mosquitoes. It uses a variety of methods to e liminate actual mosquito br eeding locati ons and to enhance tidal circulation, and/or improve predator access to others. Ponds or shallow pools (0.1–0.5 m) are constructed in areas with a high density of breeding depressions, and ch annels emanating from these (pond radials – similar to runn els) are used to connect other de pressions in the vicinity of the

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Int. J. Environ. Res. Public Health 2012 9 4581 ponds. Open (tidal), sill (semi-tidal), and closed pond and ditch networks ditches are used to eliminate mosquito breeding depressions and increase ci rculation throughout the system (Figure 3). Figure 3. An OMWM project in Connecticut. Rotary ditches, ponds, and pond radials are visible. Spoil generated by the ditches and ponds is used to fill in other mosquito breeding depressions [10]. Originally, ditches and ponds were constructed by hand or via dragline [226] and the spoil had to be carefully spread and graded to avoid creating more mosquito breeding depre ssions or undesirable high areas in the marsh. At the end of a long hot day of ditching, the extra efforts associated with spreading out the spoil would be left until last and often fo rgotten. These retained spoil mounds paralleling the ditches reduced ditching effectiveness and supporte d the establishment of i nvasive plant species not initially present in the marsh. Later projects utilized rotary ditching equipment [227], which spread the spoil in a very thin layer over the marsh surface t hus greatly reducing the need for grading and the creation of high points on the marsh surface, and faci litating natural re-v egetation of impacted areas [228]. Equipment malfunctions may sometimes also creat e low mounds paralleling the ditches, but when properly used, the technique can pr ovide excellent mosquito control with a concomitant reduction or elimination of pesticides while minimizing negative impacts to marsh resources [229]. OMWM is frequently used by coastal mosquito control organizations al ong the Atlantic United States. The techniques used vary by locale due to hydrological/t opographical differences at control sites [230]. For example, in some areas such as New Jersey and Delaware, standard OMWM modifications as described above are usually employe d, but in some New Engla nd marshes, ditches are often plugged to create more long-lasting standing wate r areas [38]. Standards have been developed at

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Int. J. Environ. Res. Public Health 2012 9 4582 the state level in New Jersey [231] and Delaware [107]. These standards have been modified by various mosquito control organizations along the coast and applied according to their specific requirements. OMWM is very effective in reducing mosquito pr oduction from the affected area. Early studies documented significant reduction in mosquito abunda nce in OMWM modified marshes, and recent quantitative studies indicate sign ificant reduction in mosquito produc tion after application of OMWM techniques [38,232,233]. If properly applied, the tech nique can be compatible with other natural resource management/enhancement goals [233], and has been proposed by some as an element of more complex integrated marsh management techniques for mosquito control and natural resource enhancement [215]. There are also documented negative impacts of OMWM. For example, the technique may cause changes in soil surface moisture and wate r table [116,234,235] with accelerated rates of remineralization of organic detritus, effectivel y lowering the marsh surface [236] and negatively impacting some obligate marsh bird species due prim arily to reduced forage effectiveness [237]. Other effects observed in wetlands subjected to OMWM in clude vegetation changes [238], loss of vegetation through subsidence and pond formation, increases in pH through oxidation of acid sulfate soils, degradation of water quality, changes in salinity [224,236], and shifts in the nekton communities from fish dominance to crustacean dominance [236]. 6.5. Impounding Wetlands impoundments have been used in the past for a variety of purposes including waterfowl management, water management and storage, flood c ontrol, agriculture, waste treatment, aquaculture, recreation, and many others [ 231]. The major North American salt marsh mosquitoes Aedes spp. will not oviposit upon standing wate r, so diking and flooding will effectively prevent mosquito breeding in the area. Only a thin film of wa ter is necessary to prevent mosqu ito oviposition. A mosquito control impoundment is basically a marsh that has been dike d (at least along the coasta l edge) to allow the area to be flooded. A variety of water cont rol structures such as pumps, cu lverts, and spillways can be used for water control. Management va ries depending upon the location and other uses such as waterfowl management; some are flooded only during the mos quito breeding season and others may be flooded year-round or intermittently throughout the year [6]. An impoundment for mosquito control was constr ucted in Florida in th e late 1930s [239,240] but was not very effective because of excessive water losse s and no practical means of replacing them [241]. During the 1950s, impoundments (often constructed for other purposes such as salt-hay production) were managed effectively for mosquito control in the Mid-Atlantic St ates [242,243] and this encouraged the use of this technique in Florida, particularly along the Indian River Lagoon, in the east central part of the State. Ditches are not very eff ective in the coastal wetlands along this part of the State because lunar tides are very sm all or non-existent so there is very little natural energy to circulate water through ditch or OMWM systems. Also, the ma jority of the marsh acreage in this region is composed of high marsh, thus requ iring modification of extensive ar eas for proper mosquito control. Finally, wetlands vegetation in th e central and southern part of this region consist primarily of mangroves, whose complex above-ground structure (Fi gure 4) makes it difficult to construct ditches

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Int. J. Environ. Res. Public Health 2012 9 4583 and ponds in the required locations. Impounding in this area commenced in 1954, and by 1970 over16,000 ha of coastal wetlands had been impounded for mosquito control [207,239]. Figure 4. Florida (USA) mangroves illustrating their complex above-ground structure. Originally, impoundments were flooded much highe r than needed for mo squito control to compensate for seepage and evaporation. The hi gh flooding caused significant mortality of marsh vegetation including mangroves and herbaceous halophytes. Wate r quality in these early impoundments was also severely degraded [2 44,245] and plankton and ne kton communities were severely impacted with drastic d ecreases in diversity an d shifts in community composition [213,246–251]. Research on impacts of impounding in Florida a nd elsewhere led to reconnection of impounded wetlands, at least, during part of the year to th e estuary through culverts, and the use of dedicated pumps to eliminate the need to overflood the ar eas. Many management modifications have been implemented to mitigate some of the adverse effects of impoundments [6,208]. Nevertheless, impounding requires a high degree of habitat modifi cation and is not recommended unless needed for other management purposes such as waterfowl management. 6.6. Basin/Topography/Habitat Design Constructed wetlands are effective means of wate r treatment and provide a number of ancillary benefits including provisi on of wildlife habitat, fl ood control, education a nd recreation opportunities, and aesthetic improvement of the landscape. These wetlands can also produce mosquitoes that will impact nearby human populations a nd resident wildlife. There are design elements that can be incorporated into a cons tructed wetland that will limit mosqu ito production and fa cilitate abatement

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Int. J. Environ. Res. Public Health 2012 9 4584 efforts, but mosquito production is not often taken into consideration during the design phase of these wetlands [12]. Dividing a constructed wetla nd into cells (compartmentalization) to facilitate treatment by mosquito control equipment can significantly reduce mosquito ab atement costs. Areas of deep water (>1m) limit the growth of aquatic vegetati on, and reduce mosquito production by promoting waves and currents that limit oviposition and can drown immature mos quitoes and also enhance predation on mosquito larvae by fish and other aquatic predators. Alth ough limited deep water z ones are often recommended for constructed wetlands [101], de ep water areas in general are le ss effective for water quality treatment than shallow vegetated areas. Steep embankments also reduce mosquito pro duction by reducing emergent vegetation, allowing better predator access to mosquito larvae, limiting the amount of habitat for floodwater mosquitoes created by water level fluctuations and promoting wave action and currents that decrease habitat suitability for immature mosquitoes however, st eep banks sometimes inte rfere with foraging by shorebirds. Bottom slopes must permit drainage wit hout exposing the bottom to mosquito oviposition. Maintaining deep water zones and limiting emergent vege tation to raised plant beds can be effective in limiting mosquito production [192]. Growth of floa ting vegetation is sometim es a problem that can limit the effectiveness of these deep wa ter areas for mosquito abatement [101]. As pointed out above, in many cases permanent e limination of emergent vegetation via topographic modification is more effective for mosquito cont rol than repeated vegeta tion removal, and often reduces the disturbance-related in vasion of exotics [9]. This technique however involves drastic modifications of wetlands and shoul d be reserved for highly impacted areas, or for newly constructed treatment wetlands. In the case of the latter, if mosquito producti on concerns are addressed early during the design phase of a treatment wetland, the n eed for future interventi ons for mosquito control can be significantly reduced [102]. Th is is also true for wetlands restor ation projects, but in this case the options for mitigating mosquito production by structural design means are severely limited. 7. Integrated Mosquito Management (IMM) In most applications, the most e fficient and ecologically sound pest control strategies consist of a combination of techniques that integrate public education, surveillance, chemicals (including repellents), biological control ag ents, cultural manipulations, habita t management, and others into a flexible scheme that produces th e desired results with the minimum possible intervention [252,253]. Note that “minimum intervention” is not necessarily synonymous with less expe nsive as less intrusive techniques may often be more e xpensive to implement than more intense ones. Mosquito abatement agencies in the United States have been using integr ated mosquito management practices for more than a century. Combinations of surveillance, sanita tion measures, habitat management, chemicals, exclusion screens, educa tion, and legislation were routinely us ed in many states in the early 20th century [254]. The major advantage of IMM is the reduction or elimination of pesticides with more benign alternatives. Other advantages include more effec tive mosquito control by use of complementary or supplementary techniques, ability to implement a tiered control approach depending upon need as determined by surveillance results, slower developmen t of resistance to mosquitocides, reduced risk of

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Int. J. Environ. Res. Public Health 2012 9 4585 chemical contamination of nei ghboring areas (including populated places), and many others. The major disadvantage of IMM is that it is a more complex process requ iring more intimate knowledge of the habitat than simple chemical control. Othe r disadvantages include requirement of greater surveillance and record-keeping efforts, more intr icate implementation, and sometimes higher overall costs. 8. Discussion Mosquito control is an important part of the la rger issue of wetlands pr otection and conservation. Agricultural, industrial, commercial, and residential development remain the major threats to wetlands, either as direct causes of outright habitat loss, or as primary cause s of habitat degradation. Continued and increased legal protection of we tlands from the above forces remains the top priority, as without it, management related issues such as mosquito control will eventually become irrelevant and the much needed legislative mandates for responsible ma nagement of the country’s remaining wetlands unnecessary. Although efforts at mitigating current wetlands losses appear to be effective, with more wetlands acreage created or restored than lost during the period 1996–2005 [ 255], the actual f unction of many of the rehabilitated/created wetlands is unknown, and the tangible gains in wetlands coverage are minute compared to historical wetlands losses. An exampl e of an ambitious wetland s restoration program in North America is the reclamation of wetlands fr om agriculture to reduce nitrogen pollution and enhance carbon sequestration along the Mississippi-Ohio-Missouri basin [256–258]. Many restoration projects are directly asso ciated with mosquito control; exampl es include hydrological reconnection of impounded wetlands along the Indian River Lagoon in Florida [6,208] a nd various salt marsh restoration projects in Conn ecticut and New York [253]. In spite of considerable progre ss during the last decades, habita t protection and environmentally sound habitat management still remain inextricably tied to politics and economics. Furthermore, the connections are often complex, a nd occur at several levels, rangi ng from local businesses and politicians, to multinational institutions and the Fede ral Government. Education is one of the keys to lasting wetlands conservation [259]. In the final an alysis, politicians will do what will get them the most votes, and politicians, not wetlands scientists or public health professionals will decide the fate of this country’s wetlands. Unless we can produce a voting population interest ed in wetlands, the effective and lasting protection and restoration of these habitats will never be achieved. The current state of affairs, where the importance of envi ronmental issues waxes and wanes depending upon a fickle electorate leads to a s ee-saw effect that is both in efficient and counterproductive. The education of the American voters and future vot ers must be comprehensive so that regardless of the political climate and the Nation’s inclination, wetlands protection and restoration remains part of the National agenda. This means that the educa tion process must influence a wide variety of individuals, of varying backgr ounds, socioeconomic status, age, education, and na tional origins. To achieve lasting results, the wetlands protection agenda must be based on science and fact. Untrue statements or misrepresentation of facts for pol itical leverage or public relations effect are not helpful in the long term. This includes many comm only used assertions such as “healthy unimpacted

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Int. J. Environ. Res. Public Health 2012 9 4586 wetlands do not produce mosquitoes” or “wetlands are disease reservoirs that without r outine mosquito control would produce regular disease epid emics among human and animal populations”. In reality, some healthy unimpacted wetlands can pr oduce prodigious numbers of mosquitoes. One only has to read the accounts of the early Florida explorers that ha d to bury themselves in the sand at night to survive the onslaught of mosquito es produced in Florida’s wetland s to appreciate this (e.g., [260,261]. And no, wetlands will not necessarily produce diseas e outbreaks if left un attended; many wetlands do not produce appreciable numbers of mosquitoes or disease vectors and in fact, it takes a rare combination of events involving, v ectors, amplification hosts, pa thogens, weather, and many other variables to produce an arboviral di sease outbreak, and an even rare r combination to produce a real epidemic (although conditions may be more frequently met in other areas such as in malarious regions). Unfortunately, such claims have become comm onplace even among professionals because of the current politically-driven climate and because of the adversarial positions often existing between wetlands conservationists, develope rs, politicians, and mosquito cont rol/public health workers. Such claims are counterproductive because they generate mistrust between mosquito control and wetlands professionals and politicians, public officials, a nd the general public. They also hinder cooperative work (and funding thereof) between wetlands ecologi sts and mosquito biolog ists that could produce more sound management of the Nation’s wetlands. Two of the more difficult problems presently facing us are quantific ation of the nuisance mosquito problem, and private ownership of wetlands. The form er is particularly vexing because different individuals have different tolera nces for mosquito bites, and mo squito species vary in their aggressiveness when seeking blood meal, in their preferences for human bl ood, and in their flight ranges. Private ownership is a problem because it often interferes with establishment of best management practices in wetlands [6]. The purchase of privately owned wetlands by local, state, or Federal agencies is an obvious solution, but often funding is not available, property owners are not willing to sell, or they have unrealistic concepts of th e true value of their land. Because of the diversity of situati ons, there can be no hard and fast set of rules for mosquito control in wetlands. Several situations are clear, for example, failure to deal with vector mosquito production when significant arboviral disease transmission a nd amplification have been demonstrated near a populated area would be irre sponsible, regardless of the overall pr obability of epidemic development. Likewise, undertaking permanent physical modifications for mosquito control of unimpacted or lightly impacted wetlands simply as a “precaution” is totally indefensible. Most situations, however, are not as clear cut. Once po litical and popular suppo rt for responsible management of wetlands exists, many individual on-si te determinations will still need to be made regarding wetlands management and mosquito cont rol. This will necessi tate working cooperation between mosquito control professionals, wetlands managers, and policy makers. Some variables such as the t ype of wetland, land ownership, ecolo gical status, location and size, surrounding habitats, proximity of human populations mosquito production history, and others can be expected to be important in the management equati on for most wetlands. Othe r variables however will be highly site and situation specific and will have to be factored in by professionals with local knowledge. A broad selection of mana gement tools for the wetland profe ssional is essential; this will allow development of flexible and site-appropriate management strate gies for the Nation’s wetlands.

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Int. J. Environ. Res. Public Health 2012 9 4587 In most cases, a surveillance-based tiered approach to mosquito control w ill be the best option for wetlands located near human populations. Whether w ithin a framework of ex isting source reduction, personal protection, education, and community outreach programs, or where none exist, an escalating list of interventions may include no additional control when mosquito production is low, augmentation of biological control agents if mosquito nuisan ce levels are reached, limited use of biorational pesticides when nuisance levels become excessive, and comprehensiv e mosquitocide application when local disease transmission and amplification has been demonstrated. Dogmatic investment in specific techniques for mosquito control is not conducive to a good final product and no viable strategy shou ld be discounted a-priori on strictly philosophical grounds. For example, in some cases a well-designed OMWM project may be the best solution for a particular wetland, however in other cases, OMWM ma y not be appropriate, modifications to existing OMWM systems may be desirable, or other means of mosquito control may be more suitable. Closures of certain wetlands to th e public during heavy mosquito production times should be a vi able alternative to heavy pesticide use or irrevers ible wetlands modifications when mo squito production from the site will not significantly impact densely populated ar eas. Economic impacts of such closures, (e.g., impacts to local livestock, tourist revenues, etc. ) will need to be considered and will certainly be central to local political decisions. One of the most pressing needs facing mosquito control workers and wetlands managers is the development of research-based guidelines for determin ing appropriate responses for different levels of nuisance mosquito production. This is a difficult task as a multitude of variables must be considered and some are difficult to measure/characterize. In cluded among these are the mosquito species, the type of wetland, the surrounding habitat and land use, the demographic characteristics and desires of the relevant human population, land ownership, weat her conditions, local vector control capabilities, and many others. Development of defensible and tran sparent guidelines is further complicated by the fact that treatment criteria need to be based in part on the toleranc es of the affected human population, and this can change with the make-up of the population and with local social and cultural characteristics that will influence a number of relevant variables su ch as the extent of exposure to mosquitoes of the population. A start would be de velopment and field testing of protocols for quantifying impacts of nuisance mosqu ito population upon nearby human populations. Development of operationally feasib le and statistically valid met hodology to quantitatively evaluate mosquito production is also highly de sirable and applies directly to the above issue. Ideally, such a system would accurately reflect production from the study area (including spatia l variation) and allow quantitative comparison of contemporaneous data with established standards for intervention (see above and section 4.3). Collins and Resh [262] disc uss a well-grounded approach for nontidal wetlands based on sequential sampling technique s that had been previously used to sample mosquitoes in southeastern U.S. rice fields, and Walton [263] deve loped a sampling program us ing this approach to assess the effectiveness of BMPs for mosquito abat ement in state-owned wetlands. Recent attempts to develop and apply statistically robust sampling methodology to wetlands mosquito populations include work by Rochlin and James-Pirri and collabor ators [38,215,233]. Although the methodology used in such research studies is probably too cumberso me and expensive for routine mosquito control operations, they may provide a theoretical framew ork for developing more operationally friendly protocols.

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Int. J. Environ. Res. Public Health 2012 9 4588 A related urgent need is the de velopment of reliable models of arboviral disease transmission that can provide decision makers with quantitative estimates of local disease risk given environmental conditions and measurable vector, host, and pa thogen dynamics. Developing criteria and methodology for evaluating the accuracy and relevance of such ri sk models is an equally pressing need. Currently, most predictions of arbovirus tr ansmission risk are based solely upon viral activity detection [264]. Some weather-based models exist th at can call attention to conditions conducive to increased vector abundance, and weather based models have been us ed locally with some success, for example, to predict outbreaks of Ross River Virus (RRV) in Aust ralia [265]. However, for most diseases current models based solely on w eather and related variable s have very limited poten tial for generating truly predictive output [264]. Independe nt models will likely be needed to accommodate the different ecological dynamics of different mosquito-borne pathogens [266]. Accurate information on the species and numbers of mosquitoes produced from different types of wetlands, deeper understanding of the factors that influence mosquito production in different habitats, and the spatial and temporal trends in mosquito production during wetland succession are also needed. Vezzani et al [267] noted a dearth of information on im mature mosquito habi tats in the general scientific literature that is a ccessible to wetlands managers and policy makers. Some of this information may be available at local mosquito cont rol agencies, but fine scale detail on the ecology of immature stages is still needed. Dale and Knight [ 224] point out that there ar e still large gaps in our knowledge of long-term effects of mosquito ma nagement activities upon non-target organisms and wetland functions. These authors also point out that our knowledge of the role of mosquitoes in the overall ecology of wetlands leav es a lot to be desired. The number of products registered for vector cont rol is small and dwindling. Many products are not being re-registered by the manufacturers because of cost of required tests relative to the amount of revenue generated by sales. Further research in need ed to find new mosquito control products that are specific, effective and cost effici ent, with negligible impacts to non-target organisms. Technological advances in the production, storage, transport, and deployment of biol ogical control agents suitable for use in wetlands, as well as field studies on the e fficacy, applicability, and environmental impacts of existing and novel biological control agents are also urgently needed. Another crucial area in need of continued research is the anticipa ted impact of climate change upon wetlands ecosystems (and their management), upon mosquitoes, upon mosquito transmitted pathogens, and upon their interactions. Anti cipated effects of climate ch ange upon human health can be considerable and diverse [268], but our inability to estimate the nature, rate and extent of the anticipated change obstructs our ability to forecast the effects upon arthropod-borne virus systems and nuisance mosquito populations arising from wetla nds. Direct impacts upon wetlands and mosquito ecology will obviously affect our overall wetlands management stra tegies, and our approach to mosquito management, but indirect effects upon vect or-pathogen-host-environm ent systems, including socioeconomic and political re percussions, effects upon diseas e transmission, and many others complicate the issu e by orders of magnitude. Re search on controlling mechanisms of vector-pathogen-host interactions, and genotype based exploration of res ponse patterns to environm ental forcing are required to increase predictability of disease risk unde r different scenarios [269]. Broad environmental monitoring is generally advanced as a critical need for dealing with climate change [268], and this of

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Int. J. Environ. Res. Public Health 2012 9 4589 course includes wetlands. Establ ishing baseline relationships betw een weather and disease is also considered essential in evaluating th e possible effects of climate change upon all types of diseases [270]. 9. Concluding Remarks Presently, mosquito control is undertaken to protect public health and mainta in expected quality of life. Mosquito control in wetlands is a complex i ssue influenced by numerous factors, including many hard to quantify elements such as human perceptions cultural predispositions, and political climate. We have over 100 years of experience and of t echnological development that afford responsible agencies the capabilities to use integrated, survei llance-based approaches for controlling mosquitoes. These options, however, are contex t-dependent and the decision-maki ng for abatement activities needs to be transparent and defensible. Integrated mosquito abatement strategies incor porate many approaches and practicable options, as described herein, and need to be well-defined, e ffective, and ecologically and economically sound for the wetland type and for the mosquito species of concern. The approach will certainly differ in response to disease outbreaks caused by mosquito-v ectored pathogens versus quality of life issues caused by nuisance-biting mosquitoes. We encourage continued research on mosquito ab atement techniques and on strategies and policies that enhance our ability to addr ess wetlands mosquito production in an effective and ecologically sound manner. Acknowledgements The authors wish to thank, Ma rk Felton, Leslie Gecy, Cather ine Mayhew, Jeff Mengler, Bill Meredith, Nancy Read, and Chad Roberts for many profitable discussions and comments on the subject of mosquito control and wetlands; and D oug Carlson, Mark Latham, Jim David, Jim McNelly, and David Brown for their insights into the NDPES program. We also thank two anonymous reviewers for many helpful suggestions on an ear lier draft of this paper. Publica tion of this article was funded in part by the University of Flor ida Open Access Publishing Fund. Conflict of interest The authors declare no conflict of interest. References 1. Mulrennan, J.A. Mosquito control—Its impact on the growth and deve lopment of Florida. J. Fl. Med. Assoc. 1986 73 310–311. 2. Higgs, S. The 2005–20 06 Chikungunya Epidemic in the Indian Ocean. Vector-borne Zoon. Dis. 2006 6 115–116. 3. Maartens, F.; Sharp, B.; Curtis B.; Mthembu, J.; Hatting, I. The impact of malaria control on perceptions of tourists and tourism operators co ncerning malaria preval ence in KwaZulu-Natal, 1999/2000 versus 2002/2003. Int. Soc. Travel Med. 2007 14 96–104. 4. Simmons, F.E.R.; Peng Z. Skeeter syndrome. J. Allergy Clin. Immunol 1999, 104 705–707.

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