Delphastus catalinae and the silverleaf whitefly, Bemisia tabaci biotype B, on tomato: modeling predation across spatial scales DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Diego Fernando Rincon Rueda Graduate Program in Entomology The Ohio State University 2015 Dissertation Committee: Luis A. Cañas, Advisor Casey W. Hoy, Co-advisor P. Larry Phelan Laurence V. Madden Robin A. J. Taylor Copyright by Diego F. Rincon 2015 Abstract Ecological models are developed to gain understanding and generate predictions about ecosystems. Predator-prey models, for example, are used to integrate information on the biology and ecology of predators and prey with the aim of predicting the dynamics of the system over time. Model predictions are often used to guide the management of production systems, such as the application of biological control of pests in agriculture. One important component of the theory on predator-prey interactions is the predator functional response, which is a mathematical description of predation rates based on the number of prey available. Functional responses are important components of predator- prey models because they are often used as a link between predator and prey population sub-models. Thus, the accuracy of predictions derived from predator-prey models depend upon the accuracy and precision of estimates derived from functional responses. However, functional responses are often estimated through small-scale laboratory experiments, which are then used to model dynamics of larger natural systems, leading to biased estimations of the predation capabilities of natural enemies. Understanding behavioral traits that determine the ability of predators to suppress pest populations at spatial scales larger than those evaluated in the laboratory may help in selecting the right species and release rates for biological control programs. My thesis is ii that predation rates within whole plants are driven by the interaction between prey distribution, individual predator patch-to-patch behavior and consumption rates within patch units. I propose that results derived from simple laboratory settings can be useful to predict predation rates within whole plants, if they are combined with spatially explicit descriptions of prey distribution and predator movement patterns. I assume that the leaflet is a spatial scale at which predators and prey behave as in laboratory settings, at least in experiments without replacement of consumed prey. My study extended from the leaflet to the plant scale, encompassing both the relatively homogeneous prey patch unit, leaflet, and the more structurally complex combination of leaflets, leaves, branches and main stem. My study system consisted of the silverleaf whitefly (SWF), Bemisia tabaci biotype B and the coccinellid predator Delphastus catalinae inhabiting tomato plants in a greenhouse environment. The SWF is a significant worldwide pest of a variety of production systems including field and greenhouse tomato. Because of persistent application of chemical insecticides, the SWF has developed resistance to an array of chemical pesticides. For this reason, alternative control methods, such as the use the beneficial insects, have been encouraged but few have shown success. The predator D. catalinae is currently the only coccinellid predator that is commercialized in the USA for whitefly control. However, the use of D. catalinae as biological control agent has been limited because of its variable degree of success suppressing SWF populations. Despite the relatively high predation rates that have been reported for D. catalinae in laboratory iii settings, its consumption capacity in more realistic scenarios, whole plants or fields, remains largely unknown. To support my thesis, I reviewed the functional response theory emphasizing the most accepted methods to scale up laboratory results. I also explored what is known about the biology of the tomato-SWF-D. catalinae system (Chapter 1). I then evaluated key predator behavioral patterns by modeling the interaction between the spatial distribution of the SWF and the search behavior of D. catalinae. First, I developed an algorithm to generate within-plant spatial distributions of the SWF, based on aggregation patterns observed within and among tomato leaves (Chapter 2). Second, I described the spatial interaction between the SWF and D. catalinae at the within-plant scale and examined its effects on D. catalinae predation rates and functional response. I found that prey and predator prefer different regions within plants and that predation rates and the functional response at the scale of a leaflet are comparable to what have been observed in the laboratory. In contrast, I observed that predation rates are lower and that the functional response changes qualitatively when the scale of observation is increased from the leaflet to the plant (Chapter 3). To gain understanding of the processes that drive such a change in predation rates and functional response with scale transition, I developed an individual-based model that incorporates the observed behavioral patterns of D. catalinae individuals when preying on SWF nymphs within tomato plants (Chapter 4). I found that the number of leaflets visited per plant by predators and the degree of spatial alignment between predator and prey distributions impact predation rates significantly at the spatial scale of the whole plant. Also, I demonstrated that simple measures of prey distribution iv and predator foraging patterns can be used to scale up functional responses estimated through small, homogeneous laboratory settings. Altogether, my research shows that non- random distributions and movement patterns of prey and predators can be predicted, at least within plant structures, and that simple measures of such patterns can be used to accurately model predation rates within plants using observations from laboratory settings. My thesis can be applied to overcome current limitations in the extrapolation of data collected in the laboratory to the field, which ultimately will help fine-tune release procedures of biological control programs. v Dedicated to Said, Stella, Andrea, Ana Maria and Emilia vi Acknowledgments I would like to thank my advisors, Dr. Luis Canas and Dr. Casey Hoy, who knew how to make the perfect fit with my expectations and guided me patiently through this long process. I appreciate the tons of things they have taught me but, especially, that they always made me feel in family. I thank my committee members, Dr. Larry Phelan, Dr. Larry Madden and Dr. Robin Taylor who stimulated my critical thinking and with whom I enjoyed sharing my thoughts and receiving their always refreshing points of view. Especial thanks to Dr. Larry Phelan for his enthusiasm teaching science and for being such a great instructor in the journal clubs. I enjoyed the company of excellent lab mates during my first years. Claudia Kuniyoshi and Karla Medina made my life easier during my years in Wooster (OH). Especially, I would like to thank Alfredo Rios who became my friend and who taught me a great portion of what I have learnt. I served as a Teaching Associate for several years, and was lucky enough to have worked with Dr. Carol Anelli with whom I learn to love education. Not only is she an outstanding instructor, but also a wonderful human being. vii I want to thank Aristóbulo López, my first research advisor at Corpoica, who introduced me to science and showed me the value of knowledge and creativity. Funding for my dissertation project was received from Corpoica, Colciencias, The Fulbright Program, the development fund contributed by K. W. Zellers and Sons Farms, and the Department of Entomology at The Ohio State University. Research support was also provided by state and federal funds appropriated to the Ohio Agricultural Research and Development Center, through SEEDS Research Enhancement Competitive Grants Program (Grant OHOA1006). The result of this work would not have been possible without the company and support of friends that knew how to keep me sane and healthy. I am thankful for the great memories I share with Santiago Sanchez, Constanza Echaiz, Wilmer Rodriguez, Ben Phillips, Silvia Duarte and Agus Muñoz. I am fortunate to have met Carolina Camargo a long time ago because she has repeatedly made me understand how valuable a true friendship is. viii Vita 2005 ...............................................................B.S. Biology, Pontificia Universidad Javeriana (Colombia) 2008 to present ..............................................Research Scientist, Corpoica (Colombia) 2009 to 2012 .................................................Fulbright fellow, Department of Entomology, The Ohio State University. 2012 to present ..............................................Graduate Teaching Associate, Department of Entomology, The Ohio State University. Publications Rincon, D. F., C. W. Hoy, and L. Canas. 2015. Generating within-plant spatial distributions of an insect herbivore based on aggregation patterns and per-node infestation probabilities. Environmental Entomology. DOI: 10.1093/ee/nvu022 Rincon, D. F.; C. Camargo, E. Valencia, and A. López-Avila. 2010. Localización de hospedero por larvas neonatas de Tecia solanivora (Lepidoptera: Gelechiidae). Corpoica Ciencia y Tecnologia Agropecuaria 11: 5 -10. ix Rincon, D. F., and J. Garcia. 2007. Frecuencia de cópula de la polilla guatemalteca de la papa Tecia