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Prediction of Mosquito Abundance in Temperate Regions, Using Ecological, Hydrological and Remote Sensing Models by Yun Jian Department of Environment Duke University Date:_______________________ Approved: ___________________________ Marco Marani, Supervisor ___________________________ William Pan, Co- supervisor ___________________________ Sonia Silvestri ___________________________ Song S. Qian ___________________________ Gabriel Katul Dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Environment in the Graduate School of Duke University 2014 ABSTRACT Prediction of Mosquito Abundance in Temperate Regions, Using Ecological, Hydrological and Remote Sensing Models by Yun Jian Department of Environment Duke University Date:_______________________ Approved: ___________________________ Marco Marani, Supervisor ___________________________ William Pan, Co- supervisor ___________________________ Sonia Silvestri ___________________________ Song S. Qian ___________________________ Gabriel Katul An abstract of a dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophyin the Department of Environment in the Graduate School of Duke University 2014 Copyright by Yun Jian 2014 Abstract New and old mosquito-borne diseases have emerged and re-emerged in temperate regions over the recent past, but an understanding of mosquito population dynamics, a fundamental step toward disease control, remains elusive. In particular, we are still lacking reliable predictive models of mosquito abundance in temperate areas due to the subtle links between the fluctuation of mosquito population and highly heterogeneous environmental drivers. Hence, this doctoral dissertation presents an interdisciplinary approach towards an improved understanding and prediction of the fluctuations in mosquito abundance in temperate regions. In the first part of this dissertation a hierarchical Gompertz-based model is used to assess the relative importance of endogenous (density dependence) and exogenous (environmental forcings) controls and their interactions in regulating the dynamics of a West Nile Virus vector (Culex pipiens) in the Po River delta in Italy. The results clearly detect the effects of density-dependence in the observed population dynamics for the mosquito species analyzed and highlight the controls exerted by environmental forcings and habitat conditions. Subsequently, the characteristic scales of temporal variability in mosquito populations, and the representativeness of observations at different sampling resolutions, are investigated using a 10 year daily mosquito sample from Brunswick County, North Carolina. The species present in the sample (among which Aedes vexans and Culiseta melanura are addressed in greater detail, as vectors of East Equine Encephalitis and West Nile Virus) iv are investigated using a combination of time series analysis, individual based simulations, and density-dependent modeling approaches. Significant population fluctuations with characteristic periodicity between 2 days and several years are found in response to different regulation mechanisms. In particular, the observed fast fluctuations are importantly determined by a varying mosquito activity, rather than by reproduction/mortality processes, driven by rapid changes in meteorological conditions. Finally, in the third part of this study, a state space reconstruction (SSR) approach is used to understand how the predictability of mosquito abundance varies with aggregation time scale and with the prediction horizon, and how much can the prediction of mosquito abundance be improved by using daily observations compared to the commonly used once-per-week samples. The results show that the predictability of mosquito abundance decreases as the time scale of the models increases from one week to one month, while the predictability of per capita growth rate increases together with the modeling scale. It is also shown that the prediction of mosquito per capita growth rate can be improved using daily abundance observations. Furthermore, many mosquito models compare the observed and predicted abundance as a measure of model performance. However, my results suggest that short term forecasts of mosquito abundance may appear to have a significant capability due to the positive autocorrelation between abundance in subsequent time steps, even when the model’s v ability to predict the abundance change is low. Model capability should thus be evaluated comparing observed and modelled per capita rates of change. vi Contents Abstract .................................................................................................................................... iv Contents ................................................................................................................................. vii List of Tables............................................................................................................................. x List of Figures ......................................................................................................................... xii Acknowledgements .............................................................................................................. xvi 1. Introduction .......................................................................................................................... 1 1.1 Mosquito – borne diseases in temperate regions: an emerging challenge .............. 1 1.2 An overview of our current understanding of mosquito population dynamics .... 3 1.3 Density dependence in mosquito population dynamics .......................................... 8 1.4 Hydrologic controls in mosquito population dynamics ......................................... 11 1.5 The representativeness of adult mosquito observations ......................................... 13 1.6 Dissertation Objectives and Organization ............................................................... 16 2. Environmental Forcing and Density-dependent controls of Culex pipiens Abundance in a Temperate Climate (Northeastern Italy) ........................................................................... 21 2.1 Introduction ................................................................................................................ 21 2.2 Materials and methods .............................................................................................. 24 2.1.1 Study area and data collection ............................................................................. 24 2.1.2 Modeling Approach .............................................................................................. 27 2.1.2.1 Soil moisture dynamics ................................................................................. 28 2.1.2.2 Mosquito population modeling .................................................................... 29 2.2 Results ......................................................................................................................... 37 2.3 Discussion and conclusions ....................................................................................... 45 vii 3. The Temporal Spectrum of Adult Mosquito Population Fluctuations: Conceptual and Modeling Implications ........................................................................................................... 52 3.1 Introduction ................................................................................................................ 52 3.2 Materials and methods .............................................................................................. 54 3.2.1 Study area and data .............................................................................................. 54 3.2.2 Data analysis .......................................................................................................... 57 3.2.3 Fourier analysis ..................................................................................................... 58 3.2.4 Autocorrelation, partial correlation, and data splitting ..................................... 59 3.2.5 Models .................................................................................................................... 60 3.2.5.1 Individual-Based life cycle simulation model ............................................. 60 3.2.5.2 Density dependent population models ........................................................ 65 3.3 Results ......................................................................................................................... 67 3.4 Discussion and conclusions ....................................................................................... 77 4. Predicting Mosquito Abundance across Temporal Scales .............................................. 82 4.1 Introduction ................................................................................................................ 82 4.2 Methods ...................................................................................................................... 84 4.2.1 Study area and data .............................................................................................. 84 4.2.2 State space reconstruction (SSR) and Simplex Projection (SP) .......................... 84 4.3 Results ......................................................................................................................... 94 4.4 Discussion and conclusions ..................................................................................... 106 5. Dissertation conclusions .................................................................................................. 111 5.1 Overview of the results ........................................................................................... 111 5.2 Major contributions.................................................................................................. 115 viii Appendix A .......................................................................................................................... 118 A1. Conditional plots for per capita growth rate, log of abundance and temperature ......................................................................................................................................... 118 A2. Relationship between rainfall and soil moisture .................................................. 118 A3. WinBUGS model script .......................................................................................... 119 A4. Model evaluation .................................................................................................... 120 Appendix B ........................................................................................................................... 121 B1. IBS model formulation, developmental stages, and processes. ........................... 121 B2. Power spectrum of observed weather data ........................................................... 122 B3. Detailed functions and parameter values used in the IBS models ...................... 123 B4. Empirical relations between activity factor and rainfall ....................................... 126 B5 ACF and PACF of Gompertz models for Ae.vexans with different density dependence (results for the Ricker model, not shown, are analogous) ..................... 127 B6. ACF for observations and for models with different density dependence. ........ 128 B7. Estimated coefficients for density dependent models .......................................... 129 Appendix C .......................................................................................................................... 132 C1. Change of correlation between the predicted and observed values for prediction horizon ............................................................................................................................ 132 C2. Correlation between the predicted and observed values for co-prediction ....... 134 C3. SP results of 7-day-ahead prediction using the once-per-week samples ............ 137 C4. SP results of 7-day-ahead prediction using the daily samples ............................ 138 References ............................................................................................................................. 139 Biography ............................................................................................................................. 153 ix List of Tables Table 1: Model performance when soil moisture or rainfall was used as predictors. ...... 41 Table 2: Mean and standard deviation of multiplicative coefficients of exogenous factors in eq. (4). Soil water content, radiation, hours and wind speed were calculated as the average values one week before mosquito samplings. NDVI was calculated for a 75m x 75m window around each sampling site. (levels of significance are: * p <0.1, ** p<0.05, and *** p<0.01) ........................................................................................................................ 43 Table 3: Density-dependent models (showing lag 0 as examples), where t is index of sample date; N is adult mosquito abundance; r is the maximum per capital growth rate; m K is the carrying capacity ...................................................................................................... 67 Table 4: The correlations and RMSE for the best models at three time scales for Cs.melanura and Ae.vexans ..................................................................................................... 94 Table 5: The variables selected for the best models at three time scales for Cs.melanura and Ae.vexans ........................................................................................................................ 100 Table 6: The correlations and RMSE for the random walk models at three time scales . 106 Table 7: Estimated coefficients for density dependent models for mosquito abundance in the Brunswick County NC .................................................................................................. 129 Table 8: Correlation between the predicted and observed per capital growth rate changes for prediction horizon ........................................................................................... 132 Table 9: Correlation between the predicted and observed abundance changes for prediction horizon ............................................................................................................... 133 Table 10: Correlation for co-prediction at weekly scale. Index for species: 1, Ae.vexans; 2, Cs.melanura; 3, Cx.salinarius; 4, Cx.restuans; 5, Ps.columbiae; 6, Ps.ferox; 7, An.crucians; 8, Oc.atlanticus; 9, Oc.fulvus.pallens; 10, Cx.nigripalpus; 11, Cx.erraticus; 12, Cx.pipiens; 13, Ps.ciliata; 14, An.quadrimaculatus; 15, Ps.howardii; 16, Oc.canadensis .................... 134 Table 11: Correlation for co-prediction at biweekly scale. Index for species: 1, Ae.vexans; 2, Cs.melanura; 3, Cx.salinarius; 4, Cx.restuans; 5, Ps.columbiae; 6, Ps.ferox; 7, An.crucians; 8, Oc.atlanticus; 9, Oc.fulvus.pallens; 10, Cx.nigripalpus; 11, Cx.erraticus; 12, Cx.pipiens; 13, Ps.ciliata; 14, An.quadrimaculatus; 15, Ps.howardii; 16, Oc.canadensis ............................................................................................................................................... 135 x

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fulfillment of the requirements for the degree Hence, this doctoral dissertation presents an interdisciplinary mosquito models compare the observed and predicted abundance as a measure . Environmental Forcing and Density-dependent controls of Culex pipiens .. density of points in the graph.
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