Agent-Based Modeling of Physical Factors That May Control the Growth of Coccidioides (Valley Fever Fungus) in Soils

Mark Gettings U.S. Geological Survey, 520 N. Park Ave. Rm 355 Tucson, AZ 85719, USA. (mgetting@usgs.gov) Frederick S. Fisher U.S. Geological Survey, 520 N. Park Ave. Rm 355 Tucson, AZ 85719, USA. (sher@email.arizona.edu)

Abstract

A model of the spread and survival of the fungus Coccidioides in soil via wind-borne spore transport has been completed using public domain agentbased modeling software. The hypothetical model posits that to successfully establish a new site that has never hosted the fungus previously, four factors must be simultaneously satised. 1) There must be transport of spores from a source site to sites with favorable soil geology, texture, topographic aspect, and lack of biomass competition (favorable ground). 2) There must be sucient moisture for fungal growth. 3) The temperature of the surface and soil must be favorable for growth. Finally, 4) the temperature and moisture must remain in favorable ranges for a long enough time interval for the fungus to grow down to depths at which spores will survive subsequent heat, aridity, and ultraviolet radiation of the hot, dry climate typical of the Southwest U.S. Using agent-based modeling software, a model was built so that the eects of combinations of these controlling factors could be evaluated using realistic temperature, rain and wind models. The rain probability and amount, temperature annual and diurnal variation, and wind direction and intensity were based on the weather records at Tucson, Arizona for the 107-year period from 1894 to 2001. Favorable ground was dened using a fractal tree algorithm that emulates a drainage network in accordance with observations that favorable sites are often adjacent to drainage channels.

Numerous model runs produced the following ve conclusions. 1) If any property is not isotropic, for example wind direction or narrow paths of rainstorms, parts of the favorable areas will never become colonized no matter how long the model runs. 2)The spread of new sites is extremely sensitive to moisture duration. The amount of wind and temperature after a rain event controls the length of time before a site becomes too dry. 3) The distribution of wind and rainstorm direction relative to that of the favorable sites is a strong control on the spread of colonization. East-west winds across an area that has mostly north-south favorable sites restricts spread strongly. 4) Soil temperature was the least sensitive control in the model, although it does control the ultimate dormancy of a site. And 5), the model results cover the spectrum of complete colonization of all favorable sites from a few source sites to none, one, or two new sites in three years of model simulation. This implies the probability of new sites depends on the four factors in a Bayesian way. These results indicate that the complexity introduced in the model from site favorableness, temperature, moisture, and duration of favorable temperature and moisture conditions produces a set of model distributions that are adequate to explain what is known of the distributions of real sites. Although the actual distribution of real sites is unknown, the properties of the set of model distributions cover the known properties of real site distributions.

Introduction

The fungus Coccidioides is prevalent in the American southwest and in other areas with similar climatic conditions (Bultman, et al 2005; Fisher et al, 2007) and is a source of the potentially life-threatening disease commonly referred to as Valley Fever (Bultman et al, 2004b). This dimorphic fungus spends a portion of its life cycle in soils (Papagianis, 1980, 1988), and thus the application of geologic techniques for the discovery of spatial and temporal occurrence relationships is a method of investigation that might lead to new means of disease mitigation. Although there are two known species of Coccidioides, Coccidioides immitis and Coccidioides posadasii (Fisher et al, 2002), both are believed to cause human Coccidioides infections (Fisher et al, 2001; 2002a), and thus for this study, the genus Coccidioides will be used rather than a species-specic term. The fungus has two forms that can be airborne, the artroconidia that does not survive for long periods of time and relatively extreme conditions of temperature, humidity, and ultraviolet radiation, and the spherule, which is much more resistant and can survive long periods of time, especially in the soil (Pappagianis, 1988). For brevity in this report, we will refer to the spherules as spores. The purpose of this work was to evaluate the complex interactions between temperature, precipitation, wind and favorable soil properties as possible controls on the survival and growth of the fungus Coccidioides in the soil. Models of fungal growth have been discussed by Knudsen and Stack (1991) among others, and Bengtsson and Ekere (2001) have developed models useful for evaluating 2

the interaction of fungus with soil particles. Several studies have enumerated possible factors that might be important in the growth of the fungus (Maddy, 1957, 1957a, 1965; Maddy et al, 1961; Lacy and Swatek, 1974, and Papagianis, 1980, 1988). Among those factors are soil temperatures, humidity, and composition. The present study was undertaken to model the interactions among these three physical factors together with wind-borne transport to evaluate possible controls on the distribution in space and time of sites that might harbor the fungus. Gettings and Fisher (2003) and Gettings et al (2005) have presented poster versions of this modeling eort. A model of the spread and survival of the fungus Coccidioides in soil via windborne spore transport has been completed using public domain agent-based modeling software (NetLogo, Wilenskey, 1999). The hypothetical model supposes that for a successful new site to become established, four factors must be simultaneously satised. First, there must be transport of spores from an active source site to locations on ground possessing soil chemistry, texture, topographic aspect, and lack of biomass competition such that the fungus can thrive, termed favorable ground in this report. Second, there must be sucient moisture for fungal growth. Third, the temperature of the surface and soil must be favorable for growth. Fourth, the temperature and moisture must remain in favorable ranges for a long enough time interval for the fungus to grow down to depths at which spores at least will survive subsequent heat, aridity and ultraviolet radiation of the hot, dry season. Using agent-based modeling software, a model was built so that the eects of combinations of the controlling factors could be evaluated using realistic temperature, precipitation, and wind models. The precipitation probability and amount, temperature annual and diurnal variation, and wind direction and intensity were based on the weather records at Tucson, Arizona, for the 107-year period from 1894 to 2001. Favorable ground was dened on a rectangular grid as a simple binary relation. Grid cells are either favorable or unfavorable and were chosen arbitrarily using a fractal tree algorithm that emulates a drainage network. Maddy (1965) and Maddy and Crecelius (1967) have reported establishment of a persistent site of Coccidioides for at least 7 years following burial of infected tissues, and detection of the fungus in previously negative soil 64 m away within the 7 year study period. Ajello et al (1965) have recovered Coccidioides from the air 3-4 days after a windstorm in the Phoenix, Arizona area. Egeberg and Ely (1956) noted that during the dry season, many more positive cultures were obtained from samples taken at soil depths of 10-30 cm compared to surface samples, showing that the fungus survival was much lower in near surface soil. Pappagianis (1988) reviewed considerable evidence suggesting that neither the growing fungus nor its spores can survive for long periods in dry, hot soil nor in ultraviolet light. Temperatures in excess of 50deg C for periods of 2 weeks kill spores but temperatures of 15deg C-37deg C have survival times of 6 months or more provided some moisture is present (relative humidities of 10% or more)

(Stewart and Meyer, 1932; Pappagianis, 1988). Swatek et al (1967), among others, have shown that banks of dry stream beds and washes often host the fungus, and this observation is the basis for our use of a drainage network as model for the distribution of favorable ground. The model assumes that an existing site, located in a favorable ground grid cell, has at least viable spores surviving at soil depths of about 20 cm, deep enough to avoid ultraviolet radiation and temperature and moisture extremes. If an existing site does not have proper moisture and temperature for growth to occur, it remains dormant and is termed a dormant site. When sucient moisture reaches the spores and temperatures are in a favorable range, the spores begin to grow, and the fungus grows upward toward the surface. If the temperature and moisture conditions remain favorable, the fungus grows to the surface, produces arthrocondidia that can become windborne, and is then termed a sporing site. Windborne arthroconidia can then be blown to other grid cells, and if they are on favorable ground, the fungus can start to grow in that cell, which is termed colonized or a colonized site. If the temperature and moisture at the colonized site remain favorable long enough for the fungus to grow down to depths of approximately 20 cm, the cell becomes a new (sporing) site. If it dries up and (or) gets too hot, the fungus dies and the cell returns to just being favorable ground. When temperature and moisture become unfavorable at a sporing site, it again becomes dormant. Thus, once a cell becomes a sporing site, it will henceforth always be either dormant or sporing. The extrinsic parameters controlling the model are therefore the time to grow from depth in the soil to the surface and produce arthroconidia, the time to grow from the surface down to depth and produce spherules (spores), the maximum number of grid cells an arthroconidia can be blown by the wind, the temperature above which the fungus cannot survive, and the minimum amount of moisture for growth to or from the surface. Growth time from depth to the surface and from the surface to depth are assumed equal in this model. Because a grid cell is either favorable or unfavorable, the model makes no allowance for partially favorable conditions.

Temperature Model

Temperature and precipitation models for this study were based on the 107year daily record for Tucson, Arizona for the period September 1894 through August 2001 downloaded from the National Climate Data Center (NOAA, 2007). The data included date, maximum temperature, minimum temperature, precipitation, snowfall, and snow depth. The dataset was processed to eliminate records with missing data or bad data (impossible values), estimate the mean daily temperature as the average of the maximum and minimum, snowfall was converted to precipitation as water using the factor of 10 in. of snow equal to 1 in. of water, and time values convenient for plotting were added. Trace amounts were entered as 0.01 in. rain to obtain an entirely numerical dataset. 4

The dataset is available in appendix 1. Figure 1 shows the average daily temperature for each day of the year with a least squares cosine t superimposed. From this t, the mean annual temperature variation is 38deg F (21.1deg C). Figure 2 shows the daily temperature range plotted as a function of the amount of precipitation. The mean daily temperature range is 29.8deg F (16.6deg C) for these data. Figure 3 shows hourly mean temperature data for the month of July 2002 and 1 February to 12 March 2003 plotted normalized to the maximum and minimum. These data were downloaded from the University of Arizona weather site (2007) and taken to be representative of summer and winter diurnal variations. Figure 4 show that the average normalized winter and summer temperatures are nearly identical. The least squares t cosine line shown on Fig. 3 shows that there is assymmetry in the heating and cooling parts of the diurnal cycle; the warming part of the cycle is more rapid than predicted by the cosine whereas the cooling is slower. For this study, the cosine function was assumed to be adequate, and the assymmetry was ignored. The temperature model used is that of an innite half-space with a boundary condition of a cosine shaped boundary temperature. Two periods are used, one with a 24 hour period, and one with a 365 day period. Rainstorm cooling is modeled by adding the solution for a linear temperature variation with time for the 4-8 days needed to recover from a rainstorm. By the principle of superposition we have T (x, t) = T0 + Ta (x, t) + Td (x, t) + Tr (x, t) (1)

Where T0 , Ta , Td , and Tr are respectively the constant mean temperature, the annual cyclic temperature, the diurnal cyclic temperature, and the temperature drop due to a rain event. The mean temperature T0 for the 1894-2001 Tucson, Arizona dataset is 68.65deg F (20.36deg C). Carslaw and Jaeger (1959) give the solution for temperature at soil depth x and time t in an innite half-space with harmonic surface temperature as T (x, t) = Aekx cos(t kx ) where T (0, t) = Acos(t ) and k = (/2)1/2 (4) Here, is the thermal diusivity, = 2/T is the frequency with period T , and is the phase shift to t the data relative to clock time. A is an amplitude constant. The annual variation is then Ta (x, t) = Aa ek1 x cos( 2t k1 x a ) 365(24)(3600) 5 (5) (3) (2)

and the daily variation is Td (x, t) = Ad ek2 x cos( k2 = ( 2t k2 x d ) (24)(3600) (6) (7)

2 )1/2 k1 = k2 /(365)1/2 (2)(24)(3600)

From the 1894-2001 data above, Aa is 19deg F (10.6deg C) and Ad is 14.9deg F (8.3deg C), noting the cosine function varies from +1.0 to -1.0. From the 1894-2001 dataset, Figure 5 shows the average temperature versus the amount of precipitation on that day, and Figure 6 shows the temperature drop the day after precipitation measured as the dierence in the average temperature the day after precipitation and the day of precipitation. The approximate mean drop is about 5deg F (2.8deg C). Figure 7 shows the temperature for June and July, 2002, along with the precipitation record. Study of this and numerous other records shows that there is a temperature drop of at most approximately 1/3 of the daily temperature range immediately after the precipitation event, followed by an approximately linear increase as the ground dries out (Fig. 7). The minimum daily temperature is least aected by the rain, and the maximum the most. Recovery time varies from about 2 days for events of less than 3mm precipitation to about 6 days for precipitation greater than 3mm. For these conditions, the temperature distribution for a half-space with initial temperature zero and surface temperature Td t increasing with time we obtain (Carslaw and Jaeger, 1959) x2 x xex /4t T d t (1 + )erf c( ) 1 / 2 D 2t 2(t ) (t )1/2
2

Tr (x, t ) = Td +

(8)

where D is the duration of the recovery from rain cooling and t is the time since the rain event. The rain cooling term is only evaluated during the recovery period D. An example of the combined temperature model for a rain event of 6 days is shown in Figure 8 and and its eect in an annual cycle in Figure 9. Although the model is too regular, it nevertheless reproduces the essential features of the temperature record.

Precipitation Model

Precipitation (including snow converted to rain) for the daily record 18942001 is shown as a function of time in Figure 10. At this scale, the distribution is rather uniform with no strong trends, implying that for this study the preciptitaion can be modelled on the basis of day of the year with no need for a long 6

term trend. Figure 11 shows the same data plotted as a function of day of the year. The winter wet season (approximately days 320 to 110) and the summer monsoon (approximately days 180 to 260) are quite obvious. The spring dry season from days 110 to 180 is well delineated, but the fall dry season (days 260 to 320) is less obvious in the record. The frequency distribution of precipitiation amplitude is shown in Figure 12 and shows a smooth exponential-like decay. The probability of precipitation of any amplitude versus day of the year calculated from the data of Fig. 11 is shown in Figure 13. Note this pattern is similar to that of fractional brownian motion with persistence (Feder, 1988), a clear demonstration of the fractal or multifractal nature of the likelihood of precipitation (Schertzer et al, 2002). Figure 14 shows the model probability functions for precipitation as a function of amplitude of precipitation for the two wet and two dry seasons derived from the 1894-2001 dataset. Histogram versions of these functions, together with the probability of precipitation (Fig. 13) were used in the model to determine the occurrence of precipitation and, if nonzero, its amplitude.

Wind and Favorable Ground Model

Figure 15 is a record of wind direction and speed for the period 24 October - 20 November, 2003, at the University of Arizona, Tucson, Arizona. From the records reviewed, Fig. 15 is fairly typical for the Tucson area for the last decade. Note that there is generally an approximately 90 degree band for a given day, and that speed is most frequently 0-5 m/sec range, and least frequently 15-20 m/sec. Thus, similar distributions were used in the model to select wind direction and speed. Within the model one can choose a preferred wind direction and range to model trade wind type behavior, or isotropic wind directions can be chosen. Within the selected range, the wind direction is chosen from a uniform random distribution. Favorable ground (as dened above) in the model was chosen arbitrarily using a fractal L-system tree of four iterations (Wilensky, 1999). This models a drainage network, corresponding to the observation that sites known to produce Coccidioides often occur adjacent to local watercourses (Swatek et al, 1967). At this stage of modeling, we only distinguish favorable ground in a binary sense, that is, a patch is either favorable or not favorable. An important extension of the model will be to incorporate a favorableness function so that patches that are only partially favorable will allow the fungus to grow only at a slower rate. Bultman et al (2004, 2004a, 2005) have created a mosaic of favorable ground based on fuzzy adaptive maps combining criteria known to control the incidence of Coccidioides. Fisher et al (2007) have given a careful review of factors that may control favorable ground and conclude that temperature range and ne sandy or silty soils are important factors at known sites of Coccidioides. These

results were not available until well after this model study (2003), but they will be incorporated in any future modeling.

Agent-Based Model

The model was developed using NetLogo software, a publicly available agentbased modeling software package from Northwestern University (Wilensky, 1999). This software combines simple and exible coding to keep track of agent sets with the ability to do fairly complex calculations. The Coccidioides ecosystem model is fairly complex and involves several criteria for all agents. The model extent is usually a 100x100 cell grid with east-west measured by columns and rows increasing north-south. Thus, north is the top of the grid as in a normal map view in the screenshots of the following gures. Moisture content of a grid cell of the ground (patch in NetLogo) is variable for every grid cell. Moisture content is modeled by keeping track of the amount of rain on each grid cell and calculating the heat ow from the grid cell. The moisture content of a grid cell is thus increased by rain on the cell and decreased by heat ow causing evaporation. All grid cells have xed soil thermal properties. A uniform temperature distribution for all grid cells was adopted because the inclusion of the temperature drop equations dened above made the model run unacceptably slow. In this model, the grid cells are the immobile agent set of favorable ground (yellow, Figure 16) or unfavorable ground (black) with the same daily and annual temperature variations. The model keeps track of the temperature at the surface, 1 cm and 20 cm depths. Heat ow is calculated using the thermal gradient dened by the surface and 1 cm depth temperatures and subject to a boundary condition of 3 times the surface conductive heat ux to simulate the eect of forced convection at the soil surface. Mobile agent sets (turtles in NetLogo) are wind and precipitation. Wind can have a preferred azimuth and range of azimuths to simulate trade winds. Precipitation in the model occurs as a rainstorm with an azimuth and a specied width. Rainstorm azimuths were isotropic in this model. Wind occurrence, direction, and intensity are chosen randomly from the observed probability distributions for the Tucson, Arizona area, as are precipitation occurrence and amplitude. The parameters that are set by the user for a model run are as follows together with typical values. The number of existing dormant sites on favorable ground is typically 20. The maximum temperature for long term survival at 20 cm depth in the soil is usually chosen as 40deg C. The maximum number of grid cells a spore (arthroconidia) can jump with maximum wind velocity is chosen, usually in the range of 1 to 5 grid cells. The minimum moisture content for growth is chosen, usually in the range of 0.2 to 0.5 in (0.5 to 1.2 cm). The minimum time for growth to the surface from 20 cm or growth down from the surface to 20 cm (they are assumed equal in this simple model) is specied in days, usually 14-30 days based on observations at some sites (Pappagianis, 1988). Finally the preferred azimuth for wind direction blown to and the angular range about that direction are specied. Typical values are 0, for winds from south to north and a 90deg

angle gives winds from southeast to southwest. An angle range of 360deg gives isotropic wind directions. The width in grid cells of a rainstorm swath is also specied; 15 grid cells is a typical width. Finally, the fade rate for rainstorm swaths on the map display is specied so that older rainstorm paths vanish; otherwise, the map display gets unacceptably cluttered. The model starts with a given number of dormant sites that will become active sources of spores when they receive enough moisture and have the correct temperature for a growth period corresponding to growth from spores beneath 20 cm in the soil up to the surface. When this occurs for a dormant site (shown as brown in the model) it becomes a sporing site (shown as red in the model). A site becomes colonized when the wind blows from a sporing site to a site on favorable ground, and there is at least a minimum amount of moisture in the ground at that site and the temperature must be below the maximum for growth of the fungus. The colonized site will continue to grow until it runs out of moisture or the temperature becomes too warm for growth. If the site has grown long enough for the fungus to penetrate the soil to 20 cm or deeper, the colonized site becomes a sporing site, that is, a site that will reactivate and after a growth interval produce spores at the surface. A colonized site dies (goes back to yellow) if it does not have enough moisture or gets too hot before the growth interval to become a permanent site passes. A sporing site becomes dormant when there is too little moisture or the temperature gets too high, killing the fungus down to 20 cm in the soil. The code for the netlogo model is attached as appendix 2.

Model Results

Models were initially run for about 1 year (Fig. 16), but we soon realized more information was gained by running the model for multiple years, so most models were run for 10 to 20 years. A twenty-year model simulation takes about 10 hours on a 1.5 GHz PC. Nearly 100 models have been run. Output consists of: 1) an image (jpeg format) of the Graphical User Interface showing the parameter values, the state of the favorable ground, and plots over model time of the numbers of dormant sites, active (sporing) sites, colonized sites, precipitation, and temperature; and 2) a comma-delimited le of the plots that denes all parameter setting and contains the numerical data used to generate the plots. The present netlogo software only allows runs up to about 23 years because of memory limitations. Fig. 16 shows an approximately one year long simulation with winds blowing from the south in an 89deg wide band (used in most simulations), that is, in random directions from 135deg through north to 224deg azimuth. Note that the branches of the favorable ground tree aligned approximately north-south experienced the largest number of new sites. Branches perpendicular to the 9

prevailing wind experienced only little growth of number of sites. Parameters in this simulation were set so that the fungus survival rates would be high, that is a high soil temperature that kills the fungus, a relatively small amount of soil moisture for survival, and a fairly high growth rate to form a site. This results in an order of magnitude increase in the number of sporing or dormant sites from 20 to about 200 within a year (note the red sporing and brown dormant lines on the plot in Fig. 16), much higher than the rate at which the evidence suggests the fungus spreads (Pappagianis, 1988). Figure 17 shows a three year simulation with more stringent temperature and moisture survival conditions, and winds prevailing from the west, resulting in only about a ve-fold increase in sites in three years. Figure 18 shows a 17 year simultion with similar temperature and moisture survival conditions and westerly winds again. The number of sporing or dormant sites increases from 20 to about 175 over the entire period, but mainly only in four events when moisture, favorable ground, temperature, and wind combined optimally. Figure 19 shows a 9 year simulation with favorable conditions: high temperature and low moisture for survival and wind from the south maximizing favorable ground availability to wind-borne colonization. The total number of sporing or dormant sites increases approximately as a logarithmic function of time. Figure 20 shows a 20 year simulation with fairly restrictive temperature and moisture conditions for fungus survival and in addition a wind direction restricted to a 60deg wide band centered on south. This case exhibits again the staircase behavior of the increase in number of sporing or dormant sites, with long periods of no change in total number of sites. Figure 21 shows a similar case but with less restrictive temperature and moisture conditions and wind in a 90deg band from the east. In this case, two events at about 1.7 and 2.7 years dominate the growth of sporing or dormant sites, with a slow staircase growth for the rest of the period. Note also that the growth is mainly in an east-west direction (brown, green and red cells of the favorable ground tree in Fig.21), illustrating the relation between the geometry of the favorable ground relative to existing sites and the wind direction, since it is the vector for growth. Finally, Figure 22 shows another 20 year simulation with somewhat less restrictive survival parameters than Fig. 20, but only a 60deg range of winds from the south. The total number of new sporing or dormant sites is about the same, but the growth pattern is much more linear because of the occurrence of more favorable wind, rain and temperature events, emphasizing the stochastic nature of these occurrences. For analysis, output images are cataloged on a website in a table with the image name linked. Thus one can scan the table for desired parameter combinations and see the image instantly. Using several browsers at once allows quick visual comparisons and enables detailed study of the model runs in a convenient way.

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When all four conditions are satised, an increase in the number of sites is observed. Each of these events represents a case of self-organized criticality (SOC) (Jensen, 1998). The frequency of SOCs depends upon the values of the controlling parameters (principally minimum moisture, number of days required, and maximum tolerable temperature) relative to the climate (precipitation and temperature) of the model. The model achieves climatic variability very similar to that observed in the climate dataset for Tucson for the period 1894-2001. There are dry years, wet years, and multi-year wet and dry periods. This is likely due to the use of probability distributions from the observed data for precipitation occurrence and amplitude. It is unlikely that the actual numbers of sporing or dormant sites or growth rates produced by the model are correct because of the simplied nature of the model. However, the relative increases and decreases from dierent model runs provide insight into the controls of the possible spread of new dormant sites by the mechanisms of this model. Known infectious sites are relatively scarce (Bultman et al, 2005; Fisher et al, 2007) whereas the model predicts quite a large number of sites. Jammalamadaka et al (2007), using more realistic favorable ground models and growth rates, report a much reduced rate of increase of sites. The model SOC events tend to occur in early spring and post-monsoon periods, similar to the observed time of maximal occurrence of Valley Fever (Pappagianis, 1988). This is not built into the model in any way that we are aware of, and represents an encouraging result. We believe this behavior is due to increased probability of simultaneous satisfaction of the four criteria during these two periods. Figure 23 shows a plot of the total number of sporing or dormant sites for most of the model runs. Note the Devil Staircase appearance of each of the curves for each model run, suggesting fractal behavior as a generalized multiplicative process (Feder, 1988). There is an appearance of clustering at times longer than 10 years in Fig. 23, suggesting that bifurcation (Turcotte, 1997) may be occurring but there is an insucient number of model runs to establish this.

Conclusions

Any anisotropy (distribution of favorable ground, prevailing wind direction, etc.) reduces the rate of formation of new dormant or sporing sites. Moreover, the anisotropy causes certain parts of the area to never be subject to new site formation. This is a robust conclusion shown by every long term model computed. Models generally exhibit Devil Staircase behavior, that is, they persist with a xed number of dormant or sporing sites for several years, and then a SOC event occurs and more dormant or sporing sites are produced.

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The rate of increase of number of sites (dormant or sporing) is sensitive to moisture duration and maximum temperature for survival. The correspondence between the pattern or distribution of favorable ground and wind and rain direction is a strong control on the rate of increase of sites. A mechanism for limiting the spread of new dormant or sporing sites must exist; otherwise all favorable ground would be a site after a few decades. We model this by the maximum temperature value, which is a proxy for the combination of high temperature and, possibly ultraviolet radiation. Future modeling will include dierent patterns of favorable ground based on fuzzy logic models of known factors (Bultman et al, 2005), continuous rather than binary growth rates on favorable ground, and using actual temperature and precipitation records for each year rather than probability distributions. Jammalamadaka et al (2005 and 2007) have reported results of eorts to implement versions of the model incorporating some of these improvements on a computer cluster in order to speed up the model runs suciently for parameter variation studies. Ultimately, we will test whether Bayesian probability models can be used to set limits on the rate of new dormant or sporing sites, that is, whether the product of the prior probabilities for wind, precipitation, favorable ground and duration can predict rates of new site formation. Based on the model results presented here, we believe the Bayesian probability approach will dene maximum rates of site formation.

Acknowledgments

The work described here was carried out under the medical geology task of the the Complex Systems Applied to Basin Margins of the American Southwest Project, Mineral Resources Program, U. S. Geological Survey. This manuscript has beneted greatly from discussions and technical reviews by M. Bultman and F. Gray, U.S. Geological Survey. Publication of this report has been approved by the Director of the U. S. Geological Survey. Note Added in Proof Subsequent to completion of this report R. Jammalamadaka completed his dissertation, Jammalamadaka (2008), which includes further modelling of the scenario presented here. His modeling included continuously variable favorable ground rather than binary as used in this report, and a diusion-controlled model of soil moisture calibrated by observations of soil wetting and drying in the Tucson, Arizona area.

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[] Ajello, L., K. Maddy, G. Crecelius, P.G. Hugenholtz, and L.B. Hall (1965), Recovery of Coccidioides immitis from the air, Sabouraudia 4, 92-95. [] Bentgsson, G., and L. Ekere (2001), Predicting sorption of groundwater bacteria from size distribution, surface area, and magnetic susceptibility of soil particles, Water Res. Research. vol. 37(6), 1795-1812. [] Bultman, M.W., F.S. Fisher, and M.E. Gettings (2004), Modeling the habitat of a soil-borne human pathogen: Coccidioides, USGS Fifth Biennial GIS Workshop, Denver Colorado, March 29-April 2, 2004. [] Bultman, M.W., F.S. Fisher, M. E. Gettings (2004a), Mapping the Distribution of a Soil-Borne Human Pathogen: Coccidioides [abstract], http://www.wolframscience.com/conference/2004/presentations/. [] Bultman, M.W., F.S. Fisher, and M.E. Gettings (2004b), Coccidioidomycosis: Mitigating the Risk, in USGS GeoHealth News, Vol. 3, No. 1, U. S. Geological Survey, Reston, Virginia, http://energy.er.usgs.gov/medical geology.htm [] Bultman, M.W., F.S. Fisher, and D. Pappagianis (2005), An overview of the ecology of soil-borne human pathogens, in Essentials of Medical Geology: Impacts of the Natural Environment on Public Health, Elsevier Academic Press, New York. pp. 481-511. [] Carslaw, H.S., and Jaeger, J.C., 1959, Conduction of Heat in Solids, second ed., Oxford Univ. Press, 510 p. [] Egeberg, R.O., and A.F. Ely (1956), Coccidioides immitis in the soil of the southern San Joaquin Valley, Am. J. Med. Sci. V23, 151-154. [] Feder, J. (1988), Fractals, 283pp., Plenum Press, New York. [] Fisher, F.S., M.W. Bultman, S.M. Johnson, D. Pappagianis, and E. Zaborsky (2007), Coccidioides niches and habitat parameters in the Southwestern United States, a matter of scale, Ann. N.Y. Acad. Sci. 1111, 47-72. [] Fisher, M.C., G.L. Koenig, T.J. White, G. San-Blas, R. Negroni, A.I. Gutierez, B. Wanke, and J.W. Taylor (2001), Biogeographic range expansion into South America by Coccidioides immitis mirrors New World patterns of human migration, Proc. Nat. Acad. Sci. USA 98(8), National Academy of Sciences, Washington, D.C. [] Fisher, M.C., G.L. Koenig, T.J. White, and J.W. Taylor (2002), Molecular and phenotypic description of Coccidioides posadasii sp. nov., previously recognized as the non- California population of Coccidioides immitis, Mycologia 94(1) 73-84.

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[] Fisher, M.C., B. Rannala, V. Chaturvedi, and J.W. Taylor (2002a), Disease surveillance in recombining pathogens: Multilocus genotypes identify sources of human Coccidioides infections, Proc. Nat. Acad. Sci. USA 99 9067-9071. [] Gettings, M.E., and F.S. Fisher, (2003), Agent-Based Modeling of Physical Factors That May Control the Growth of Coccidioides immitis (Valley Fever Fungus) in Soils: Eos Trans. AGU, 84(46), Fall Meet. Suppl., Abstract B21B0713. [] Gettings, M. E., F.S. Fisher, and M.W. Bultman (2005), Agent-Based Modeling of Physical Factors That May Control the Growth of Coccidioides (Valley Fever Fungus) in Soils: 1st All-USGS Modeling Conference, 15-17 November, 2005, Port Angeles, WA. [] Jammalamadaka, R. (2008),Multilevel Methodology for Simulation of SpatioTemporal Systems with Heterogeneous Activity: Application to Spread of Valley Fever Fungus: PhD dissertation, Electrical and Computer Engineering Dept., University of Arizona. [] Jammalamadaka, R., J. Nutaro, M. Gettings, B. Zeigler (2005), DEVS ReImplementation of an Agent-Based Valley Fever Model, 2005 DEVS Integrative Modeling and Simulation Symposium, 2005 Spring Simulation Multiconference, SpringSim05, San Diego. [] Jammalamadaka, R., M. Gettings, M. Bultman,B. Zeigler, and Ming Zhang (2007), Complex System Simulation: DEVS Implementation of the valley fever model: 2007 DEVS Integrative Modeling and Simulation Symposium (DEVS07) Spring Simulation Multiconference 2007 (SpringSim07), March 25 - 29, 2007, Norfolk, Virginia, USA, http://www.scs.org/confernc/springsim/springsim07/nalProgram/nalProgram.htm [] Jensen, H.J. (1998), Self-Organized Criticality, Emergent Complex Behavior in Physical and Biological Systems, 153p., Cambidge Univ. Press. [] Knudsen, G., and J. Stack (1991), Modeling growth and dispersal of fungi in natural environments, in Handbook of Applied Mycology, vol. 1: Soils and Plants, Eds. D.K. Arora, B. Rai, K. Mukerji, and G. Knudsen, 625-645, Marcel Dekker, Inc., New York. [] Lacy, G. H. and F.E. Swatek (1974), Soil ecology of Coccidioides immitis at Amerindian middens in California, Appl. Microbiol. 27, 379-388. [] Maddy, K. T. (1957), Ecological factors of the geographic distribution of Coccidioides immitis, J. Am. Vet. Med. Assoc.130, 475-476. [] Maddy, K.T. (1957a), Ecological factors possibly relating to the geographic distribution of Coccidioides immitis, Proceedings of the Symposium on Coccidioidomycosis. U.S. Public Health Service, Pub. no. 575, 144-157, CDC, Atlanta, GA. 14

[] Maddy, K.T. (1965), Observations on Coccidioides immitis found growing naturally in soil, Arizona Medicine 22, 281-288. [] Maddy, K.T., and G.T. Crecelius (1967), Establishment of Coccidioides immitis in negative soil following burial of infected animals and animal tissues, in Coccidioidomycosis, L. Ajello, Ed., University of Arizona Press, Tucson, Arizona, 309-312. [] Maddy, K.T., H.G. Crecelius, and R.G. Cornell (1961), Where can coccidioidomycosis be acquired in Arizona, Ariz. Med. 18, 184-194. [] NOAA (2007), National Climatic Data Center, National Oceans and Atmospheres Administration, U.S. Department of Commerce, URL:http//www.ncdc.noaa.gov, data downloaded October 18, 2001. [] Pappagianis, D. (1980), Epidemiology of coccidioidomycosis. In Coccidioidomycosis D.A. Stevens, Ed. Plenum Medical Book Company, New York. 63-85. [] Pappagianis, D. (1988), Epidemiology of coccidioidomycosis. In Current topics in Medical Mycology, V2 Springer Verlag, New York, 199-238. [] Schertzer D., S. Lovejoy, and P. Hubert (2002), An Introduction to Stochastic Multifractal Fields, in Mathematical Problems in Environmental Science and Engineering, A. Ern and L. Weiping, editors, Series in Contemporary Applied Mathematics, pp. 106-179, Higher Education Press, Beijing. [] Stewart, R.A., and K.F. Meyer (1932), Isolation of Coccidioides immitis (Stiles) from the soil, Proc. Soc. Exp. Biol. Med. V 29, 937-938. [] Swatek, F.E., D.T. Omieczynski, and O.A. Plunkett (1967), Coccidioides immitis in California, in Coccidioidomycosis, L. Ajello, Ed., University of Arizona Press, Tucson, Arizona, 255-264. [] Turcotte, D.L. (1997), Fractals and Chaos in Geology and Geophysics, Second ed., 398p., Cambridge Univ. Press. [] University of Arizona (2007), Atmospheric Sciences, weather page, URL:http://www.atmo.arizona.edu/, data downloaded October 6, 2003. [] Wilensky, U. (1999), NetLogo. http://ccl.northwestern.edu/netlogo/. Center for Connected Learning and Computer-Based Modeling, Northwestern University. Evanston, IL.

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Figure 1: Average daily temperature for day of the year, 1894-2001, Tucson Arizona, with cosine t.

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Figure 2: Daily temperature range versus amount of precipitation, Tucson Arizona, 1894-2001.

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Figure 3: Diurnal variation of temperature, summer (pluses, July, 2002) and winter (diamonds, February-March, 2003), Tucson, Arizona. Green line is least squares cosine t. Temperature range normalized to 1.0

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Figure 4: Average diurnal temperature variation, summer and winter , Tucson, Arizona. Temperature variation normalized to 1.0

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Figure 5: Average daily temperature versus amount of precipitation, Tucson, Arizona, 1894-2001.

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Figure 6: Temperature drop the day after precipitation, Tucson, Arizona, 18942001.

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Figure 7: Plot illustrating temperature drop and approximately linear recovery after precipitation, Tucson, Arizona, 2002.

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Figure 8: Temperature model of temperature and range drop due to precipitation.

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Figure 9: Illustration of one rain event temperature drop at approximate time of 7e+06 in the temperature model for one year.

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Figure 10: Precipitation versus year, Tucson, Arizona, 1894-2001

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Figure 11: Precipitation versus day of the year, Tucson, Arizona 1894-2001.Note the two wet and two dry periods.

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Figure 12: Histogram showing frequency of precipitation amount, Tucson, Arizona, 1894-2001

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Figure 13: Probability of precipitation, versus day of the year, Tucson, Arizona, 1894-2001. This pattern is similar to fractional brownian motion with persistence (Feder, 1988), which demonstrates the fractal or multifractal nature of the likelihood of precipitation.

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Figure 14: Model probability functions for the two wet and two dry seasons.

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Figure 15: Wind direction and speed for the period 24 October - 20 November, 2003, Tucson, Arizona.

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Appendix 1- Temperature and precipitation data for Tucson, Arizona, 1894-2001

Please see supplementary le 1894 2001TUCAZ.dat.

Appendix 2- Netlogo program code

Please see supplementary le coccicosystem.nlogo.

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Figure 16: A typical simulation of a little more than one year resulting in about 240 dormant or sporing sites from the original 20. The red-shaded stripes show the paths of recent rainstorms, and the red spots on the yellow tree of favorable ground are sporing sites while the brown are dormant sites. Below are plots of the variables temperature (green), rain (blue), colonized (green), sporing (red) and dormant (brown) sites, and time in black in 10 day cycles. See text for explanation.

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Figure 17: A three year simulation. See text for discussion.

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Figure 18: A 17 year simulation. Note staircase form of growth of number of dormant sites. See text for discussion.

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Figure 19: A 9 year simulation. Note logarithmic form of growth of number of dormant sites. See text for discussion.

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Figure 20: A 20 year simulation. Note growth along predominant wind direction. See text for discussion.

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Figure 21: A 20 year simulation. Note abrupt growth in the number of sites in the rst four years. See text for discussion.

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Figure 22: A 20 year simulation. Note long periods of little growth in the number of sites. See text for discussion.

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Figure 23: Plot of total number of sites capable of sporing for several models. Note suggestion of clustering of number of sites at about 10 yr and later.

39