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1 Journal of Medical Entomology Andrew Monaghan 1 DEVELOPMENT, LIFE HISTORY Research Applications Laboratory 2 National Center for Atmospheric Research 3 PO Box 3000 4 Monaghan et al.: Energy balance Boulder, CO 80307 5 model for water-holding containers Phone: (303) 497 8424 6 Fax: (303) 497 8386 7 E-mail: [email protected] 8 9 WHATCH'EM: An Energy Balance Model for Determining Water Height and 10 Temperature in Container Habitats for Aedes aegypti and Aedes albopictus 11 12 ANDREW J. MONAGHAN, 1,2 DANIEL F. STEINHOFF, 1 MICHAEL J. BARLAGE, 1 13 THOMAS M. HOPSON, 1 ISAAC TARAKIDZWA 3 , KARIELYS ORTIZ-ROSARIO, 4 14 SAUL LOZANO-FUENTES, 5 MARY H. HAYDEN, 1 AND LARS EISEN 5 15 16 1 National Center for Atmospheric Research, P.O. Box 3000, Boulder, Colorado 80307 17 2 Corresponding author, e-mail: [email protected] 18 3 African Risk Capacity, 11 Naivasha Rd, SunningHill, 2157, Johannesburg, South Africa. 19 4 Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 20 of Turabo, P.O. Box 3030, Gurabo, Puerto Rico, 00778 21 5 Department of Microbiology, Immunology and Pathology, Colorado State University, 22 3195 Rampart Road, Fort Collins, Colorado 80523 23 24
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Page 1: 1 Journal of Medical Entomology Andrew Monaghan 5 Monaghan · 20 4Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 21 of Turabo, P.O. Box 3030,

1

Journal of Medical Entomology Andrew Monaghan 1

DEVELOPMENT, LIFE HISTORY Research Applications Laboratory 2

National Center for Atmospheric Research 3

PO Box 3000 4

Monaghan et al.: Energy balance Boulder, CO 80307 5

model for water-holding containers Phone: (303) 497 8424 6

Fax: (303) 497 8386 7

E-mail: [email protected] 8

9

WHATCH'EM: An Energy Balance Model for Determining Water Height and 10

Temperature in Container Habitats for Aedes aegypti and Aedes albopictus 11

12

ANDREW J. MONAGHAN,1,2 DANIEL F. STEINHOFF,1 MICHAEL J. BARLAGE,1 13

THOMAS M. HOPSON,1 ISAAC TARAKIDZWA3, KARIELYS ORTIZ-ROSARIO,4 14

SAUL LOZANO-FUENTES,5 MARY H. HAYDEN,1 AND LARS EISEN5 15

16 1National Center for Atmospheric Research, P.O. Box 3000, Boulder, Colorado 80307 17

2Corresponding author, e-mail: [email protected] 18

3African Risk Capacity, 11 Naivasha Rd, SunningHill, 2157, Johannesburg, South Africa. 19

4Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 20

of Turabo, P.O. Box 3030, Gurabo, Puerto Rico, 00778 21

5Department of Microbiology, Immunology and Pathology, Colorado State University, 22

3195 Rampart Road, Fort Collins, Colorado 80523 23

24

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Abstract 25

The mosquito arbovirus vectors Aedes aegypti (L.) and Aedes albopictus (Skuse) 26

exploit a wide range of containers as sites for oviposition and development of the 27

immature stages, yet approaches for modeling container water dynamics have been 28

limited. We introduce WHATCH'EM, a state-of-the-science, physically-based energy 29

balance model of water height and temperature in containers that may serve as 30

development sites for mosquitoes or other container-inhabiting arthropods. We also 31

employ WHATCH'EM to model container water dynamics in three cities along an 32

elevation and climate gradient in México ranging from sea level, where Ae. aegypti is 33

highly abundant, to ~2,100 m, where Ae. aegypti is rarely found. WHATCH’EM is 34

driven with field-derived meteorological data from May-September 2011 and evaluated 35

for three commonly-encountered container types with volumes of 3.8, 18.9 and 208.2 36

liters. WHATCH’EM simulates the highly non-linear manner in which air temperature, 37

humidity, rainfall and clouds interact with container characteristics (shape, size, and 38

color) to determine water temperature and height, leading to results that are not always 39

intuitive and likely not simulated by standard empirical models. In general, simulated 40

water temperatures are higher for containers that are larger, darker, and that receive more 41

sunlight. While air temperature drives differences in the magnitude and daily range of 42

container temperatures among the three cities, sunlight exposure (which is modulated by 43

clouds and shading from nearby objects) also plays a first order role. WHATCH'EM 44

simulations will be helpful in understanding the limiting climatic and container-related 45

factors for proliferation of Ae. aegypti and Ae. albopictus.46

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Keywords: Aedes aegypti, Aedes albopictus, container, energy balance model, water 47

temperature 48

49

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The mosquitoes Aedes aegypti (L.) and Aedes albopictus (Skuse), the primary 50

vectors of dengue, yellow fever and chikungunya viruses, exploit a wide range of 51

containers as sites for oviposition and development of the immature stages (Gratz 1999, 52

2004; Gubler 2004; Focks and Alexander 2006). These containers can range in size from 53

small trash items (e.g., bottles and cans) to medium-sized buckets and tires to large water 54

storage containers such as barrels or drums, tanks and cisterns (Morrison et al. 2004, 55

Tun-Lin et al. 2009, Bartlett-Healy et al. 2012). Proliferation of the mosquitoes is aided 56

by the presence of containers that hold water of suitable temperature and nutrient content 57

for eggs to hatch and immatures to develop. Using Ae. aegypti as an example, successful 58

larval development can be impeded by water temperatures that are too low for 59

development to occur (8-12°C) or high enough to cause physical harm, through heat 60

stress, to the larvae (36-44°C) (Bar-Zeev 1958, Smith et al. 1988, Tun-Lin et al. 2000, 61

Kamimura et al. 2002, Chang et al. 2007, Richardson et al. 2011, Muturi et al. 2012). In 62

the field, Hemme et al. (2009) found that Ae. aegypti immatures were absent from water 63

storage drums, which are key productive containers in Trinidad, in which water 64

temperatures exceeded 32°C. The temperature optimum for Ae. aegypti larval and pupal 65

development, with short development times and high survival rates, is in the range of 24-66

34°C (Bar-Zeev 1958; Rueda et al. 1990; Tun-Lin et al. 2000; Kamimura et al. 2002; 67

Mohammed and Chadee 2011; Padmanabha et al. 2011a, 2012; Richardson et al. 2011; 68

Farjana et al. 2012). There also is a growing recognition that the magnitude of the daily 69

temperature range (i.e., fluctuations over the course of a 24-hour period) impact life 70

history traits of Ae. aegypti, including larval development time (Lambrechts et al. 2011, 71

Mohammed and Chadee 2011, Carrington et al. 2013). Other factors that can have 72

negative effects on larval development time or survival include poor nutrient content of 73

the water and intraspecific or interspecific resource competition (Braks et al. 2004, 74

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Juliano et al. 2004, Padmanabha et al. 2011b, Walsh et al. 2011). For rain-filled 75

containers, there are also distinct risks of a container drying out before the immature 76

stages can complete their development or of the container over-flowing and the 77

immatures being flushed out (Koenraadt and Harrington 2008, Bartlett-Healy et al. 2011). 78

Weather-driven simulation models for Ae. aegypti populations -- such as CIMSiM 79

(Container Inhabiting Mosquito Simulation Model) and Skeeter Buster -- are strongly 80

influenced by water temperature, which impacts several important components of the 81

models including the development times and survival rates of eggs, larvae and pupae 82

(Focks et al. 1993a, b; Cheng et al. 1998; Magori et al. 2009; Ellis et al. 2011). CIMSiM 83

simulates the dynamics of immature Ae. aegypti and water dynamics within user-84

specified container categories, accounting for shape (circular or rectangular), dimension, 85

presence or absence of lid, fill method (manual or rain), fill frequency (daily, weekly, or 86

monthly), drawdown frequency (daily, weekly, or monthly), if it was located under the 87

edge of a roof or similar device to capture rain water, and if it was in shade or sun (Focks 88

et al. 1993a, Ellis et al. 2011). The original version of CIMSiM used default values for 89

key characteristics of a given container category (Focks et al. 1993a), whereas a more 90

recent version allows the user to input data for the container categories to represent the 91

average characteristics and density of that container category in the focal location (Ellis 92

et al. 2011). The Skeeter Buster model is based on the general characteristics of CIMSiM 93

but operates at the level of individual containers and also incorporates stochastic events, 94

e.g., survival of individuals of Ae. aegypti within a cohort (Magori et al. 2009). 95

Perhaps the greatest limitation of these complex simulation models is the 96

continued use of simplistic empirical relationships to predict water temperature in and 97

water loss from containers based on ambient air temperature (daily maximum and 98

minimum), sunlight exposure, precipitation, relative humidity, and saturation deficit 99

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(Focks et al. 1993a, Cheng et al. 1998). Recent work has shown that physics-based 100

approaches toward modeling container water properties are promising for resolving the 101

complexities of container water dynamics (Tarakidzwa 1997, Kearney et al. 2009). In the 102

present study, we introduce a state-of-the-science, physically-based novel model, as 103

opposed to an empirical approach, to explore water dynamics in container habitats of 104

relevance for Ae. aegypti and Ae. albopictus. The model calculates the height and 105

temperature of water in a specified container at hourly (or sub-hourly) intervals by 106

solving the system of equations that governs the energy balance (i.e., heat and moisture 107

budget) of the container as a function of meteorological and user-prescribed inputs. This 108

approach allows a user to examine the highly non-linear manner in which air temperature, 109

humidity, rainfall and clouds or shading interact with a specified container to determine 110

the height and temperature of the water it contains. The model, henceforth called 111

"WHATCH'EM" -- the Water Height And Temperature in Container Habitats Energy 112

Model -- is designed to be driven by readily-available meteorological observations and 113

user-specifiable container characteristics, so that it can be easily applied by a variety of 114

users, and potentially integrated into other weather-driven modeling frameworks such as 115

CIMSiM and Skeeter Buster. 116

We recently conducted a field study to determine the abundance of Ae. aegypti 117

immatures in containers in twelve communities located along an elevation and climate 118

gradient in central México (Lozano-Fuentes et al. 2012). Three representative 119

communities along this gradient are Veracruz City at sea level with highly favorable 120

climatic conditions for the mosquito, Rio Blanco along the eastern slopes of the Sierra 121

Madre Oriental (~1,250 m) where the mosquito is moderately abundant, and Puebla City 122

in the central highlands (~2,100 m) where a few specimens of Ae. aegypti were 123

encountered but the climate appears to prevent the mosquito from proliferating. 124

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Mosquito abundance was strongly correlated with weather parameters along this 125

elevation and climate gradient, including positive correlations with average minimum 126

daily ambient air temperature, average daily minimum relative humidity, and total 127

rainfall, and negative correlations with daily ambient air temperature range, during the 128

30-d period preceding the mosquito survey in a given community (Lozano-Fuentes et al. 129

2012). These findings led us to speculate that low or greatly fluctuating water 130

temperatures in containers may be limiting factors for population build-up of Ae. aegypti 131

at the higher elevations. Therefore, we apply WHATCH'EM to explore water dynamics 132

in three commonly encountered container types – small buckets (3.8 liters), medium-133

sized buckets (18.9 liters) and large drums (208.2 liters) – at the three cities noted above. 134

WHATCH'EM is used to examine the impacts of shading, clouds, and container color on 135

the water height and temperature in the three container types and three locations. The 136

model is driven by meteorological observations taken in each city during our field season 137

from May-September 2011, the time of year during which environmental conditions are 138

best suited (i.e., with combined high temperature and substantial rainfall) for the 139

proliferation of Ae aegypti in the study area. 140

141

Materials and Methods 142

WHATCH'EM and Its Energy Balance Equations. WHATCH'EM calculates 143

the water height (analogous with water volume) and water temperature of a specified 144

container, based on the energy balance of the water and the container. The full model 145

documentation and source code can be obtained from Steinhoff et al. (2013). 146

The energy balance method is used to calculate heat and moisture exchanges 147

between the surface and atmosphere in numerical weather prediction models in order to 148

estimate the surface temperature and evaporation. A similar method is used here, 149

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adjusted for container geometries and thermodynamic characteristics. WHATCH'EM 150

requires as input a minimal amount of commonly-available meteorological data 151

(temperature, relative humidity, and rainfall) to produce water temperature and level 152

estimates. WHATCH'EM takes into account variable factors such as cloudiness, shading, 153

container size and thermal characteristics, and any manual container filling that may 154

occur. The energy balance is calculated for both the water and the container. The energy 155

balance for water is based on the following equation: 156

157

WS CSW LW LW H L CQ Q Q Q Q Q Q Q →↓ ↓ ↑ ↑ ↑ ↓= + − − − − − (1), 158

159

where WSQ is heat storage in water (representing the change of temperature of the water), 160

QSW↓ is downward shortwave radiation, QLW↓ is downward longwave radiation, QLW↑ is 161

upwards longwave radiation, QH↑ is sensible heat transfer, QL↑ is latent heat transfer 162

(evaporation), QC↓ is conduction between the container bottom and water, and QC→ is 163

conduction between the container side walls and water. The energy balance for the 164

container is 165

166

CS SW LW LW H CG CQ Q Q Q Q Q Q Q→ → ← ← →↓ ↓= + − − − + + (2), 167

168

where CSQ is heat storage in the container, QSW→ is sideways inbound shortwave 169

radiation, QLW→ is sideways inbound longwave radiation, QLW← is sideways outbound 170

longwave radiation, QH← is sideways sensible heat transfer, QG↓ is conduction between 171

the ground and the container bottom, and QC↓ and QC→ are the same as in (1). Figure 1 is 172

a schematic showing the terms in equations (1) and (2) relative to the water and 173

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container. All terms are in units of power (Watts), and the sign convention is that all 174

radiation terms are positive into the container or its water, sensible, latent and ground 175

fluxes are positive out of the container or its water; and conduction terms are positive into 176

the container. 177

QSW↓ is the downward solar radiation absorbed by the water through the top 178

opening of the container. The shortwave radiation absorbed into the water is that 179

component not reflected by water or blocked by shade or clouds. QSW↓ is calculated as 180

181

( )( )1 1t t wSWQ S A a β↓ = − − (3), 182

183

where St is the total downward shortwave radiative flux (based on solar zenith angle at 184

the user-specified coordinates for the site of interest, and the transmission of solar 185

radiation through the atmosphere which is a function of cloud cover), At is container top 186

opening area, aw is the reflectivity (albedo) coefficient of water (a function of the solar 187

zenith angle per Cogley 1979), and β is the shade fraction. 188

QSW→ is the solar radiation absorbed by the container side walls. It is composed 189

of two components -- solar radiation directly striking the container side walls and diffuse 190

solar radiation -- not reflected by the container. QSW→ is calculated as 191

192

( )( )1SW c b dQ a Q Q→ = − + (4), 193

194

where ac is the reflectivity coefficient of the container, Qb is the direct component 195

(accounting for the zenith angle of the sun), and the diffuse component Qd is a 196

combination of solar radiation reflected from the ground onto the container side walls and 197

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atmospheric scattering. Similar to (3), the Qb and Qd terms take into account the surface 198

area of the container and shading effects. 199

QLW↓ is longwave radiation absorbed by water through the top opening of the 200

container, emitted by the atmosphere, clouds, and any shading surface. The emitted 201

longwave radiation is dependent on the fourth power of temperature (through the Stefan-202

Boltzmann law) and properties of the emitting body. QLW↓ is calculated as 203

204

4(1 )t a a s sLWQ A T Tβ ε σ βε σ↓ = − + (5), 205

206

where εa is emissivity of the atmosphere -- itself a time-variable function of air 207

temperature, vapor pressure and cloud fraction per Prata (1996) and Crawford and 208

Duchon (1999) -- σ is the Stefan-Boltzmann constant, εs is emissivity of the shading 209

surface, and Ts is the temperature of the shading surface (assumed equal to the air 210

temperature). 211

QLW↑ is the longwave radiation emitted by water in the container into the 212

atmosphere above. It depends on the temperature and emitting properties of water. QLW↑ 213

is calculated as 214

215

4t w wLWQ A Tε σ↑ = (6), 216

217

where εw is emissivity of water and Tw is water temperature (from the previous time step). 218

QLW→ is longwave radiation absorbed by the container side walls, assumed to be 219

half each of the longwave radiation emitted by the atmosphere and ground. It is 220

calculated as 221

Page 11: 1 Journal of Medical Entomology Andrew Monaghan 5 Monaghan · 20 4Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 21 of Turabo, P.O. Box 3030,

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222

( )4 40.5 0.5LW s g g a aQ A T Tε σ ε σ→ = + (7), 223

224

where As is surface area of the container side walls, εg is emissivity of the ground surface, 225

and Tg is the ground (soil) temperature. 226

QLW← is longwave radiation emitted by the container side walls to the surrounding 227

air and ground. It is calculated as 228

229

4LW s c cQ A Tε σ← = (8), 230

231

where εc is emissivity of the container and Tc is the temperature of the container (assumed 232

equal to the water temperature). 233

QH↑ is the sensible heat transfer (primarily from convection) between the water in 234

the container and the air above. We assume that in the sheltered areas where most 235

containers are found, wind speeds are low, and free convection dominates; this 236

assumption breaks down as the container becomes more exposed to wind. QH↑ is 237

calculated from Monteith and Unsworth (2008) (p. 161): 238

239

( )t a w aH

H

AC T TQ

r↑

−= (9), 240

241

where Ca is the heat capacity of air and rH is heat transfer resistance, itself a time-variable 242

function of the Nusselt number (Steinhoff et al. 2013). QH← is the sensible heat transfer 243

between the container and surrounding air. It is calculated similar to (9), except that it is 244

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computed based on the surface area and temperature of the container sides, and rH 245

employs a different Nusselt number representing the geometry of the container sides: 246

247

( )s a c aH

H

A C T TQ

r←

−= (10). 248

249

QL↑ is the latent heat transfer, associated with phase changes of water. 250

Specifically for this application, it is the heat supplied to vaporization of water in the 251

container to the air above, and represents a heat sink for the water in the container. It is 252

calculated from 253

254

( )t a sL

W

AC e eQ

rγ↑

−= (11), 255

256

where es is saturation vapor pressure, e is vapor pressure, γ is the Psychrometer constant, 257

and rW is the water vapor transfer resistance, which is assumed equal to rH used to 258

calculate QH↑ in (9) (Arya 2001, p. 247). 259

QG↓ is heat conduction between the bottom of the container and the underlying 260

soil and depends primarily on calculation of the temperature gradient between the soil 261

and the container: 262

263

( )b c gG

A T TQ

zk

−=

∑ (12), 264

265

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where Ab is the container bottom area, ∆z is the differential layer depth, and k is thermal 266

conductivity. The ratio of the last two terms is summed for the half the thickness of the 267

ground layer (zg, kg) and half the thickness of the container (zc, kc), under the assumption 268

that Tc and Tg occur at the middle of each volume. The default value of zg is 50 mm 269

because it is the midpoint of the 0-100 mm upper soil layer for which temperature data 270

are commonly available. 271

Qc↓ is the heat conduction between the water and the bottom of the container: 272

273

( )b w cC

A T TQ

zk

−=

∑(13), 274

275

where notations are as before, with the ratio of the last two terms summed for half of the 276

thickness of the container and half of the depth of the water. Similarly, Qc→ is the heat 277

conduction between the water and the sides of the container Qc→ is calculated as 278

279

( )s w cC

A T TQ

zk

−=

∑(14), 280

281

with the ratio of the last two terms summed for half of the thickness of the container and 282

the half the diameter (i.e., the radius) of the water. 283

Once the heat storage terms QSW and QSC have been calculated using the water 284

container energy balance equations (1) and (2), the water height in the container and the 285

water and container temperatures are updated. First, the accumulated evaporation of 286

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water from the container is calculated from the latent heat transfer, QL↑, following 287

Monteith and Unsworth (2008, p. 255): 288

289

L

t w

Q tE

Aλρ↑∆= (15), 290

291

where ∆t is the time period of the accumulated evaporation, λ is the latent heat of 292

vaporization, and ρw is the density of water. The water height change is then calculated 293

based on the difference of evaporation and precipitation over the time period ∆t: 294

295

( )1 ( / )w t bh P A A MF Eβ∆ = − + − (16), 296

297

where ∆hw is the water height change, P is precipitation accumulated over the time period 298

∆t, ϐ is the shade fraction (precipitation received in the container is dependent on the 299

shade fraction), the ratio At/Ab accounts for the amount of rainfall that can enter through 300

the container top relative to the size of the container body, and MF is any manual fill. 301

Currently, the minimum water height allowed in the program, for numerical stability 302

reasons, is 15 mm. Below this, water temperature and all energy balance terms are set to 303

a missing value, and a constant evaporation rate is set (default is 0.02 mm/hour). If, 304

through precipitation or manual filling, water height returns above 15 mm, then 305

calculations are restarted with water temperature set to the initial water temperature 306

specified at the beginning of the simulation. 307

With updated water height, the change to the temperature of the water in the 308

container is calculated as 309

310

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WSw

t w w

Q tTt A h C

∆∆=

∆ (17), 311

312

where ∆Tw is the water temperature change, QSW is the heat storage term, hw is the 313

updated water height (note that t wA h is the water volume), and Cw is the heat capacity of 314

water. Similarly, the container temperature is calculated as 315

316

CSc

c c

Q tTt V C

⋅∆∆=

∆ (18), 317

318

where ∆Tc is the container temperature change, QSC is the heat storage term, Vc is the 319

volume of the container material, and Cc is the heat capacity of the container material. 320

Input Data. There are three required meteorological variables, and two optional 321

variables for input to WHATCH'EM at hourly intervals. Required variables are: air 322

temperature (°C), relative humidity (%) and rainfall (mm hr-1). For this study, 323

temperature and relative humidity were obtained from low cost HOBO data loggers 324

(Onset Computer Corporation, Bourne, MA) installed in Veracruz City, Rio Blanco, and 325

Puebla City. For a map showing the locations of these cities in Veracruz and Puebla 326

States, México, see Lozano-Fuentes et al. (2012). Rainfall data were obtained from the 327

0.07° gridded Climate Prediction Center Morphing technique (CMORPH) dataset (Joyce 328

et al. 2004), which uses precipitation estimates derived exclusively from low orbiter 329

satellite microwave observations and features transported via spatial propagation of 330

information obtained from geostationary satellite infrared imagery. CMORPH provides 331

some of the most reliable estimates for tropical summer rainfall compared to other 332

satellite- and model-based rainfall products (Ebert et al. 2007). CMORPH data, which 333

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cover the globe from 60oS - 60oN, were bilinearly interpolated from the four surrounding 334

gridpoints to each HOBO site. 335

Optional variables include cloud fraction (low, middle, and high) and soil 336

temperature (°C). For this application, cloud fraction and soil temperature estimates are 337

obtained from the National Centers for Environmental Prediction North American 338

Regional Reanalysis (NARR, Mesinger et al. 2006). Gridded output with 32 km spacing 339

is bilinearly interpolated to each observation site and soild temperature is adjusted 340

(assuming a standard atmospheric lapse rate of 0.0065oC/m) for elevation differences 341

between the NARR topographic elevation and the observed elevation. Soil temperature 342

estimates are made at 50 mm depth. If cloud fraction data are not provided, then low, 343

middle, and high cloud fraction estimates are user-specified for both daytime and 344

nighttime conditions. If ground temperature data are not provided, then ground 345

temperature is estimated by the model using the near-surface air temperature 346

observations, based on the daily (24-hour) thermal wave, which is dampened and delayed 347

in time compared to the near-surface temperature daily cycle (Arya 2001). 348

Simulations. WHATCH'EM simulations were performed for Veracruz City 349

(19.2oN, 96.1oW), Rio Blanco (18.8oN, 97.2oW) and Puebla City (19.0oN, 98.2oW) for 350

three sets of experimental conditions. First, we used three container types: small buckets 351

(3.8 liters, 1 gallon), medium-sized buckets (18.9 liters, 5 gallons) and large drums (208.2 352

liters, 55 gallons) (Figure 2). For each container type the height, radius, thickness, and 353

thermal conductivity is user-specified to WHATCH'EM. Second, we evaluated three 354

colors for the containers: black, gray and white, corresponding to container albedos (ac) 355

of 0.1, 0.5 and 0.9, respectively. Container color is important primarily for the amount of 356

solar radiation absorbed by the container side walls. Third, we examined three levels of 357

shade: no shade, half shade, and full shade. Shade from natural objects (e.g., trees) or 358

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human-made structures (e.g., walls or roofs) affect both the long wave and short wave 359

energy balance and the precipitation received. 360

The simulations were run for two different scenarios with regards to containers 361

being filled with water: 1) with weekly manual container filling enabled (i.e., the 362

containers are topped off by human action every 168 hours), and 2) with manual filling 363

disabled (i.e., the containers only receive water through rainfall). For each of these 364

scenarios, the full set of combinations of the three experimental conditions described 365

above was performed, such that there are 3 x 3 x 3 = 27 total experiments per scenario. 366

The simulations were initialized for 0000 Coordinated Universal Time (UTC) on 1 May 367

2011, because May is near the end of the dry season in the study area but still precedes 368

the onset of the rainy season (in June or July) when Ae. aegypti populations are expected 369

to begin increasing. For the scenario in which there is no manual filling, the containers 370

are assumed to be dry at initialization on 1 May, after months of little or no rainfall. 371

Initial values for water temperature are also user-specified for the simulations with 372

manual filling since the containers are full from the onset. WHATCH'EM is integrated 373

once-per-minute from the initial time point through 0000 UTC on 15 September 2011 in 374

our simulations. This is an arbitrarily chosen time point that likely represents the latter 375

part of the active season for Ae. aegypti at the highest elevation examined, where the 376

climate in the winter is cold enough to prevent activity by this mosquito. Table 1 lists the 377

values of the constants and parameters that are used in WHATCH'EM. 378

379

Results 380

Climate Observations. The climates of Veracruz City, Rio Blanco and Puebla 381

City for May-September 2011 are compared in Figure 3. Monthly and total average 382

temperatures (Figure 3a) follow the elevation gradient between the cities, with Veracruz 383

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City, near sea level, being the warmest overall (29.0oC for the May-September average), 384

followed by Rio Blanco (~1,250 m above sea level; 21.3oC) and Puebla (~2100 m; 385

18.5oC). The average daily temperature range (Figure 3b) increases markedly along the 386

elevation gradient, being much lower in Veracruz City (3.9oC) versus the higher elevation 387

environments of Rio Blanco (9.0oC) and Puebla City (10.9oC). In contrast, relative 388

humidity does not exhibit marked variability between the cities during the May-389

September period (Figure 3c). In fact, the highest average relative humidity occurs in 390

Rio Blanco, where temperatures are cooler than in Veracruz City but the influence of 391

humid air from the Gulf of Mexico is still strong. However, the specific humidity (a 392

measure of absolute humidity that is independent of temperature) clearly shows that 393

Veracruz City is more humid than Rio Blanco, and that Puebla City is the least humid of 394

all the cities (Figure 3d). Likewise, the highest overall rainfall totals and cloud amounts 395

occur in Veracruz City (although the onset of rains is later there), followed by Rio Blanco 396

and Puebla City, which have similar rainfall totals and cloud amounts (Figures 3e-f). In 397

summary, during May-September Veracruz City is comparatively warm and humid with 398

a small daily temperature range and the greatest rainfall, whereas Puebla City is 399

comparatively cool and arid with a large daily temperature range and lower rainfall. Rio 400

Blanco’s climate is intermediate between Veracruz City and Puebla City. 401

Energy Balance Example for Rio Blanco. The results from WHATCH'EM for 402

the average May-September 2011 daily cycle of the components of the energy and 403

radiation balances are exemplified in Figure 4 for Rio Blanco, which has an intermediate 404

climate among the cities examined. The results are shown for a container with 405

intermediate values across our experiments: a gray, medium-sized (18.9 liter) bucket that 406

is located in half shade. Weekly manual filling was enabled in the presented scenario, so 407

the bucket is always full or nearly full of water. In Figure 4a, Bal stands for the WSQ term 408

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(equation (1)) and represents the heat gain or loss by the water that is manifested as a 409

change in temperature via equation (17). Short wave (solar, SW) radiation is the primary 410

driver of the energy balance during the day, while long wave (infrared, LW) radiation and 411

conduction (COND) between the container walls and water primarily drives heat loss at 412

night (Figure 4a). If the components of the LW and SW radiation are examined (Figure 413

4b), it is apparent that the horizontal components of both terms -- those that affect energy 414

exchange through the sides of the bucket -- are for this case on the same order of 415

importance as the vertical components that act through the top of the container. Figure 5 416

shows the average daily range (5a) and daily means (5b) for water, air and ground 417

temperature for the same gray, medium-sized bucket in Rio Blanco. The temperature of 418

the water in the container exceeds that of the air temperature on average due to the solar 419

radiation that is absorbed through the container sides during daytime, which is not 420

completely compensated by long wave and conductive heat losses at nighttime. The 421

magnitude of the SW and LW energy exchanges with the bucket are heavily influenced 422

by clouds and shading. During clear-sky periods (e.g., June in Figure 5b) the difference 423

between water and air temperatures is generally higher than during cloudy or rainy 424

periods (e.g., July) due to more solar absorption. 425

Experimental Results for Rio Blanco. Next we examine the results of the three 426

sets of experiments for Rio Blanco: comparisons of the average water temperatures and 427

water temperature fluctuations among (a) different types of containers with uniform color 428

and shading (Figure 6), (b) different colors of containers with uniform type and shading 429

(Figure 7) and (c) different levels of shading for containers with uniform type and color 430

(Figure 8). Manual filling was enabled for all experiments at Rio Blanco in the presented 431

scenarios in order to facilitate comparisons by minimizing the differences among the 432

containers that can arise due to water availability (in the manual filling experiments the 433

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containers are always nearly full). As shown in Figure 6, smaller containers, because 434

they have larger area-to-volume ratios -- i.e., more surface area available to exchange 435

heat with their surroundings compared to larger containers -- have the largest daily 436

temperature ranges. In this example, during drier conditions (May and June) the water in 437

the small bucket has an average daily temperature range of about 12oC, compared to 438

about 3oC for the water in the large drum. Counter-intuitively, the smaller containers 439

tend to have cooler average temperatures than larger containers, especially during clear 440

periods (e.g., June) because a greater fraction of the volume is exposed to nighttime heat 441

losses that are not fully compensated for by daytime heat gains. 442

As shown in Figure 7, the differences in reflectivity (albedo) among the various-443

colored containers cause substantial differences in daytime heating due to enhanced solar 444

absorption for darker colors; these differences are not fully compensated for during 445

nighttime since the albedo only impacts the solar (daytime) radiation balance. This 446

means that, compared to an otherwise identical white container, a black container will 1) 447

have a larger daily temperature range and 2) have a higher average water temperature. In 448

our example, the water in the black container is about 4oC warmer than the white 449

container on average. Differences in average daily temperatures between the no shade 450

and full shade cases are substantial: on the order of 10oC during clear-sky conditions 451

(May and June), and less (2oC) during cloudy conditions (July) (Figure 8). Additionally, 452

the no-shade containers have a much larger daily temperature range compared to shaded 453

containers (12oC versus 2oC) due to enhanced absorption of solar radiation. 454

Comparison of Results Among Cities. We also examined the differences 455

among cities for several experiments (Figures 9-11). Manual filling was disabled in the 456

presented scenarios to better understand the role of water availability in driving the 457

differences among containers, and therefore missing values represent times when water 458

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levels were <15 mm due to lack of rainfall. Figure 9 shows the May-September 2011 459

daily average, maximum and minimum water temperatures, and cumulative water 460

heights, for a gray, medium-sized (18.9 liter) bucket located in half shade for the three 461

cities. Figure 10 is a summary plot showing the May-September averages of water 462

temperature and the number of days with water heights >15 mm, by type of containers 463

and city. As expected, the daily water temperature decreases with elevation from 464

Veracruz City to Puebla City (Figure 9a). Conversely, the daily water temperature range 465

increases with elevation (Figure 9a), which is due to less cloudy conditions (Figure 3f) 466

and smaller volumes of water in containers due to lower rainfall (Figure 9b), in Rio 467

Blanco and Puebla City compared to Veracruz City. The May-September average water 468

temperatures in the containers (Figure 10a) are similar to the average air temperatures for 469

the same period (Figure 3a); this holds true for all three container types (all gray and in 470

half shade). However, it is noteworthy that the average temperatures become larger with 471

increasing container size (3.8 liter bucket versus 208.2 liter drum), with decreasing 472

albedo (black versus white), and with decreasing shade or cloudiness, as demonstrated in 473

Figures 6-8. 474

Moreover, the number of days with water heights >15 mm (Figure 10b) is 475

noteworthy because Puebla City, which receives the least rain (Figure 3e) and therefore 476

has the lowest cumulative water heights (Figure 9b), has the most days with water heights 477

> 15 mm. This is partly due to Puebla City receiving more rain earlier in the season 478

(May and June) in 2011. Therefore, despite having lower temperatures, water availability 479

does not appear to be a limiting factor for containers in Puebla City. Finally, the 480

histogram for number of days during May-September 2011 with daily water temperatures 481

falling within 2oC increments, based on a gray 18.9 liter bucket located in half shade, 482

illustrates the shift in typical water temperatures from low to high elevations (Figure 11). 483

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For example, water temperatures in the specified container commonly were projected to 484

exceed 24-26oC in Veracruz City but only very rarely in Puebla City. Conversely, water 485

temperatures commonly were projected to be <22oC in Puebla City, whereas this did not 486

occur in Veracruz City. 487

488

Discussion 489

We introduce WHATCH'EM, a state-of-the-science, physically-based energy 490

balance model of water height and temperature in containers. The model requires only 491

readily-available meteorological data from weather stations or atmospheric models and 492

user-specifiable container characteristics for input. It accounts not only for basic 493

container characteristics such as size and color, but also for shading, lidded containers 494

(not explored here), and mode of filling (rainfall only versus regular filing through human 495

action). WHATCH'EM complements, and ultimately should enhance, existing weather-496

driven simulation models for Ae. aegypti populations -- such as CIMSiM and Skeeter 497

Buster -- in that it greatly increases the realism of the estimates for the critically 498

important water temperature factor, which directly influences development times for the 499

immature stages of the mosquito and thus also the potential for population growth. 500

Although the main reason for developing WHATCH'EM was to support efforts to 501

determine the limiting factors for population growth of container-inhabiting mosquito 502

vector species, the model should prove broadly applicable to studies on other container-503

inhabiting organisms or physical processes related to the temperature of the water in a 504

container (e.g., the performance of chemicals added to the water, such as pesticides). 505

In our initial simulations, WHATCH'EM was applied to project water dynamics 506

in three commonly encountered container types (small buckets, medium-sized buckets 507

and large drums) at three representative cities located along an elevation and climate 508

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gradient that ranges from Veracruz City at sea level, where Ae. aegypti is highly 509

abundant, to the high elevation Puebla City at ~2,100 m, where Ae. aegypti is rarely 510

found (Lozano-Fuentes et al. 2012). Specifically, WHATCH'EM was used to examine 511

the impacts of container type, shading and clouds, and container color on the water 512

temperature and height, driven by meteorological observations taken in each city from 513

May-September 2011. We found that our energy balance modeling approach adds an 514

important level of complexity and non-linearity to water temperature variability, leading 515

to results that are not always intuitive and are likely not simulated by models that use 516

standard empirical approaches. To confirm this assertion, we ran the Cheng et al. (1998) 517

model which is currently used in CIMSiM to simulate water temperatures in a medium 518

bucket in no-shade conditions for our May-September 2011 study period (results not 519

shown). The Cheng et al. (1998) model, which does not account for cloud dynamics or 520

container color, simulates an increase in average daily water temperature range of 4oC 521

between Veracruz and Puebla versus an increase in WHATCH'EM of 10oC for a white 522

bucket, and 13oC for a black bucket. The greater sensitivity of the WHATCH'EM results 523

among cities is largely due to including cloud dynamics in WHATCH'EM. Accounting 524

for clouds in such models is also important from a climate change perspective: even if air 525

temperatures become warmer in a given location -- as they have nearly everywhere 526

globally and are projected to continue to do so (Intergovernmental Panel on Climate 527

Change 2007) -- changes in cloudiness (for which climate projections are highly 528

uncertain) have strong potential to amplify or dampen the corresponding changes in the 529

magnitude and daily range of water temperature in containers at that location. Changes 530

in the frequency and magnitude of rainfall also impact container water temperatures (by 531

modulating the volume) and the number of days in which adequate water is available for 532

development of mosquito immatures. In summary, climate change may have variable 533

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and unexpected impacts on the water characteristics in containers used by Ae. aegypti and 534

Ae. albopictus for oviposition and development of immatures. 535

The WHATCH'EM results for water characteristics in containers in the three 536

examined cities also provided insights into the mechanisms potentially underlying the 537

field observation that Ae. aegypti immatures are abundant at lower elevations (<1,300 m; 538

Veracruz City and Rio Blanco) but only rarely encountered at high elevations (>2,000 m; 539

Puebla City) (Lozano-Fuentes et al. 2012). Previous studies have shown that the 540

temperature optimum for Ae. aegypti larval and pupal development, with short 541

development times and high survival rates, is in the range of 24-34°C (Bar-Zeev 1958, 542

Rueda et al. 1990, Tun-Lin et al. 2000, Kamimura et al. 2002, Mohammed and Chadee 543

2011, Padmanabha et al. 2011a, Richardson et al. 2011, Farjana et al. 2012). We found 544

that model-projected water temperatures from May-September 2011 in a representative 545

container (gray, medium-sized bucket located in half shade) consistently exceeded 24°C 546

in Veracruz City and commonly exceeded 24oC in Rio Blanco, but very rarely did so in 547

Puebla City (Figure 11). Moreover, the model projected much greater daily temperature 548

ranges of the water in the containers in Puebla compared to Veracruz City (Figure 9a), a 549

factor that recently was demonstrated to be negatively associated with development time 550

of Ae. aegypti larvae (Mohammed and Chadee 2011, Carrington et al. 2013). 551

Consequently, we speculate that sub-optimal temperature conditions for Ae. aegypti 552

immatures in containers in Puebla City presently inhibits potential for population growth 553

of the mosquito in this high elevation city. 554

A somewhat surprising model result, given that Puebla City is located in the 555

comparatively cool and dry central highlands of México, was that Puebla City has the 556

most days with water heights > 15 mm for the simulated container under a rainfall-only 557

container fill scenario (Figure 9b) despite receiving the lowest total rainfall and having 558

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the lowest average relative and specific humidity (Figures 3c-e). This paradox is largely 559

due to greater early-season rainfall (Figure 9b) in Puebla City in 2011. Notably, the 560

indication from the model results that water availability in containers was not a limiting 561

factor for Ae. aegypti in Puebla City during the examined time period agrees with our 562

field observations, which produced similar numbers of water-filled containers per 563

examined premises in Puebla City versus a grouping of lower elevation communities 564

including Veracruz City and Rio Blanco (Lozano-Fuentes et al. 2012). 565

In conclusion, the WHATCH'EM model to estimate water height and temperature 566

in containers should prove a useful tool, separately and in combination with simulation 567

models for mosquito population dynamics, to further our understanding of the bionomics 568

of Ae. aegypti and Ae. albopictus. This paper focused on presenting the model itself and 569

our initial simulation results. To further demonstrate the realism of the WHATCH'EM 570

model estimates, a follow-up field validation study is underway in México. We also note 571

that WHATCH'EM simulations may prove useful for examining how human-572

environment-container interactions impact Ae. aegypti, for example by providing 573

information on which containers (by size, color and shading) have the most favorable 574

conditions for the mosquito and thus should be specifically targeted in source reduction 575

campaigns enacted by vector control programs or via community participation. Toward 576

this end, future work will more comprehensively assess the impacts of water storage 577

practices (i.e., manual filling) and container placement, shapes and types on water 578

characteristics. Finally, we also hope to be able to explore how WHATCH'EM, or a 579

related model building upon WHATCH'EM, could be applied to natural water bodies of 580

limited size, which may harbor a variety of mosquitoes of medical importance including 581

culicine arbovirus vectors and anopheline malaria vectors. 582

583

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Acknowledgments 584

We thank Carlos Welsh-Rodriguez, Carolina Ochoa-Martinez, Berenice Tapia-585

Santos, and Eric Hubron for field assistance. This study was funded by a grant from the 586

National Science Foundation to the University Corporation for Atmospheric Research 587

(GEO-1010204). The National Center for Atmospheric Research is funded by the 588

National Science Foundation. 589

590

591

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Edition. Academic Press, San Diego, CA. 692

Morrison, A. C., K. Gray, A. Getis, H. Astete, M. Sihuincha, D. Focks, D. Watts, J. 693

D. Stancil, J. G. Olson, P. Blair, and T. W. Scott. 2004. Temporal and geographic 694

patterns of Aedes aegypti (Diptera: Culicidae) production in Iquitos, Peru. J. Med. 695

Entomol. 41: 1123-1142. 696

Muturi, E. J., A. Nyakeriga, and M. Blackshear. 2012. Temperature-mediated 697

differential expression of immune and stress-related genes in Aedes aegypti larvae. J. 698

Am. Mosq. Contr. Assoc. 28: 79-83. 699

Padmanabha, H., C. C. Lord, and L. P. Lounibos. 2011a. Temperature induces trade-700

offs between development and starvation resistance in Aedes aegypti (L.) larvae. Med. 701

Vet. Entomol.25: 445-453. 702

Padmanabha, H., B. Bolker, C. C. Lord, C. Rubio, and L. P. Lounibos. 2011b. Food 703

availability alters the effects of larval temperature on Aedes aegypti growth. J. Med. 704

Entomol. 48: 974-984. 705

Padmanabha, H., F. Correa, M. Legros, H. F. Nijhout, C. C. Lord, and L. P. 706

Lounibos. 2012. An eco-physiological model of the impact of temperature on Aedes 707

aegypti life history traits. J. Insect Physiol. 58: 1597-1608. 708

Prata, A. J. 1996. A new long-wave formula for estimating downward clear-sky 709

radiation at the surface. Quart. J. R. Meteor. Soc. 122: 1127-1151. 710

Richardson, K., A. A. Hoffmann, P. Johnson, S. Ritchie, and M. R. Kearney. 2011. 711

Thermal sensitivity of Aedes aegypti from Australia: empirical data and prediction of 712

effects on distribution. J. Med. Entomol. 48: 914-923. 713

Rueda, L. M., K. J. Patel, R. C. Axtell, and R. E. Stinner. 1990. Temperature-714

dependent development and survival rates of Culex quinquefasciatus and Aedes aegypti 715

(Diptera: Culicidae) J. Med. Entomol. 27: 892-898. 716

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Smith, G. C., D. A. Eliason, C. G. Moore, and E. N. Ihenacho. 1988. Use of elevated 717

temperatures to kill Aedes albopictus and Aedes aegypti. J. Am. Mosq. Contr. Assoc. 4: 718

557-558. 719

Steinhoff, D. F., A. J. Monaghan, M. J. Barlage, T.M. Hopson, I. Tarakidzwa, K. 720

Ortiz-Rosario, S. Lozano-Fuentes, M. H. Hayden, and L. Eisen. 2013. The Water 721

Height And Temperature in Container Habitats Energy Model (WHATCH'EM). 722

http://rap.ucar.edu/staff/steinhoff/WHATCHEM. 723

Tarakidzwa, I. 1997. Evaporation from class-A pans: measurements and modeling. 724

Masters Thesis. University of Zimbabwe. 109 pp. 725

Tun-Lin, W., T. R. Burkot, and B. H. Kay. 2000. Effects of temperature and larval diet 726

on development rates and survival of the dengue vector Aedes aegypti in north 727

Queensland, Australia. Med. Vet. Entomol. 14: 31-37. 728

Tun-Lin, W., A. Lenhart, V. S. Nam, E. Rebollar-Tellez, A. C. Morrison, P. 729

Barbazan, M. Cote, J. Midega, F. Sanchez, P. Manrique-Saide, A. Kroeger, M. B. 730

Nathan, F. Meheus, and M. Petzold. 2009. Reducing costs and operational constraints 731

of dengue vector control by targeting productive breeding places: a multi-country non-732

inferiority cluster randomized trial. Trop. Med. Int. Health 14: 1143-1153. 733

Walsh, R. K., L. Facchinelli, J. M. Ramsey, J. G. Bond, and F. Gould. 2011. 734

Assessing the impact of density dependence in field populations of Aedes aegypti. J. 735

Vector Ecol. 36: 300-307. 736

737

Page 33: 1 Journal of Medical Entomology Andrew Monaghan 5 Monaghan · 20 4Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 21 of Turabo, P.O. Box 3030,

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Table 1. List of constants and parameters used in the WHATCH'EM model. 738

739

740

Page 34: 1 Journal of Medical Entomology Andrew Monaghan 5 Monaghan · 20 4Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 21 of Turabo, P.O. Box 3030,

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Figure Legends 741

742

Figure 1. Schematic showing terms of energy balance model introduced in equations (1) 743

and (2). Terms are described in the text. (Online figure in color.) 744

745

Figure 2. Photos and dimensions (diameter x height) of containers used in the 746

WHATCH'EM simulations: (a) small bucket (3.8 liters, 1 gallon), (b) medium-sized 747

bucket (18.9 liters, 5 gallons) and (c) large drum (208.2 liters, 55 gallons). The three 748

colors (black, gray and white) used in the experiments are shown here arbitrarily by 749

container type. Additional container information can be found in Table 1. Photos are 750

reprinted from website of U.S. Plastic Corp., Lima, OH (http://www.usplastic.com). 751

752

Figure 3. Monthly data for selected climate variables for Veracruz City (red), Rio 753

Blanco (green) and Puebla City (blue) during May-September 2011. The “All” column is 754

the seasonal average or total over all months. (Online figure in color.) 755

756

Figure 4. Example from Rio Blanco of the average May-September 2011 daily cycle of 757

the components of the (a) energy balance and (b) radiation balance, based on water in a 758

gray 18.9 liter bucket in half shade. All components are expressed in Watts. Terms in the 759

legend are described in the text. (Online figure in color.) 760

761

Figure 5. Comparison of average daily range (a) and daily mean (b) of temperature, 762

from May to September 2011 in Rio Blanco, for the water in a container (green), the 763

container itself (orange), the air (blue) and the ground (red). This example is based on a 764

Page 35: 1 Journal of Medical Entomology Andrew Monaghan 5 Monaghan · 20 4Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 21 of Turabo, P.O. Box 3030,

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gray 18.9 liter bucket in half shade. Terms in the legend are described in the text. (Online 765

figure in color.) 766

767

Figure 6. Comparison of daily average water temperature (solid lines) and maximum 768

and minimum water temperature (dotted lines), from May to September 2011 in Rio 769

Blanco, for gray containers in the form of 3.8 liter bucket (red), 18.9 liter bucket (green) 770

and 208.2 liter drum (blue) in half shade. (Online figure in color.) 771

772

Figure 7. Comparison of daily average water temperature (solid lines) and maximum 773

and minimum water temperature (dotted lines), from May to September 2011 in Rio 774

Blanco, for white (blue), gray (green) and black (red) 18.9 liter buckets in half shade. 775

(Online figure in color.) 776

777

Figure 8. Comparison of daily average water temperature (solid lines) and maximum 778

and minimum water temperature (dotted lines), from May to September 2011 in Rio 779

Blanco, for a gray 18.9 liter bucket in full shade (blue), half shade (green) and no shade 780

(red). (Online figure in color.) 781

782

Figure 9. Comparison of daily average water temperature -- solid lines -- and maximum 783

and minimum water temperature -- dotted lines (a) and water height (b), from May to 784

September 2011 and based on a gray 18.9 liter bucket in half shade, for Puebla City 785

(blue), Rio Blanco (green) and Veracruz City (red). (Online figure in color.) 786

787

Figure 10. Comparison of daily average water temperature (a) and days with water 788

height >15 mm (b), from May to September 2011 and based on a gray container (all three 789

Page 36: 1 Journal of Medical Entomology Andrew Monaghan 5 Monaghan · 20 4Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 21 of Turabo, P.O. Box 3030,

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types are shown) in half shade, for Veracruz City (red), Rio Blanco (green) and Puebla 790

City (blue). (Online figure in color.) 791

792

Figure 11. Histogram of the total number of days from May to September 2011 with 793

water height >15 mm in a gray 18.9 liter bucket in half shade, by water temperature, for 794

Puebla City (green), Rio Blanco (red) and Veracruz City (blue). (Online figure in color.) 795

Page 37: 1 Journal of Medical Entomology Andrew Monaghan 5 Monaghan · 20 4Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 21 of Turabo, P.O. Box 3030,

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Figure 1.

Page 38: 1 Journal of Medical Entomology Andrew Monaghan 5 Monaghan · 20 4Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 21 of Turabo, P.O. Box 3030,

38

a.

b.

c.

163 x 191 mm

597 x 921 mm

262 x 368 mm

Figure 2.

Page 39: 1 Journal of Medical Entomology Andrew Monaghan 5 Monaghan · 20 4Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 21 of Turabo, P.O. Box 3030,

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05

101520253035

May Jun Jul Aug Sep All

Tem

pera

ture

(o C)

Month

a) Average Temperature (oC)

02468

101214

May Jun Jul Aug Sep AllTem

pera

ture

Ran

ge (o C

)

Month

b) Average Daily Temperature Range (oC)

0

20

40

60

80

100

May Jun Jul Aug Sep All

Rel

ativ

e H

umid

ity (%

)

Month

c) Average Relative Humidity (%)

0100200300400500600700800900

May Jun Jul Aug Sep All

Rai

nfal

l (m

m)

Month

e) Total Rainfall (mm)

VeracruzRio BlancoPuebla

0

0.2

0.4

0.6

0.8

1

May Jun Jul Aug Sep All

Clo

ud F

ract

ion

Month

f) Average Cloud Fraction

0

5

10

15

20

25

May Jun Jul Aug Sep AllSpec

ific

Hum

idity

(g k

g-1)

Month

d) Average Specific Humidity (g kg-1)

Figure 3.

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Figure 4.

Page 41: 1 Journal of Medical Entomology Andrew Monaghan 5 Monaghan · 20 4Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 21 of Turabo, P.O. Box 3030,

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Figure 5.

Page 42: 1 Journal of Medical Entomology Andrew Monaghan 5 Monaghan · 20 4Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 21 of Turabo, P.O. Box 3030,

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Figure 6.

Page 43: 1 Journal of Medical Entomology Andrew Monaghan 5 Monaghan · 20 4Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 21 of Turabo, P.O. Box 3030,

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Figure 7.

Page 44: 1 Journal of Medical Entomology Andrew Monaghan 5 Monaghan · 20 4Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 21 of Turabo, P.O. Box 3030,

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Figure 8.

Page 45: 1 Journal of Medical Entomology Andrew Monaghan 5 Monaghan · 20 4Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 21 of Turabo, P.O. Box 3030,

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Figure 9.

Page 46: 1 Journal of Medical Entomology Andrew Monaghan 5 Monaghan · 20 4Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 21 of Turabo, P.O. Box 3030,

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Figure 10.

Page 47: 1 Journal of Medical Entomology Andrew Monaghan 5 Monaghan · 20 4Institute of Technology of Engineering, Jose D. Perez School of Engineering, University 21 of Turabo, P.O. Box 3030,

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Figure 11.


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