Modelling interference between vectors of non-persistently transmitted plant viruses to identify effective control strategies

Aphids are the primary vector of plant viruses. Transient aphids, which probe several plants per day, are considered to be the principal vectors of non-persistently transmitted (NPT) viruses. However, resident aphids, which can complete their life cycle on a single host and are affected by agronomic practices, can transmit NPT viruses as well. Moreover, they can interfere both directly and indirectly with transient aphids, eventually shaping plant disease dynamics. By means of an epidemiological model, originally accounting for ecological principles and agronomic practices, we explore the consequences of fertilization and irrigation, pesticide deployment and roguing of infected plants on the spread of viral diseases in crops. Our results indicate that the spread of NPT viruses can be i) both reduced or increased by fertilization and irrigation, depending on whether the interference is direct or indirect; ii) counter-intuitively increased by pesticide application and iii) reduced by roguing infected plants. We show that a better understanding of vectors’ interactions would enhance our understanding of disease transmission, supporting the development of disease management strategies.

[1]  Alan E. Wilson,et al.  When do herbivorous insects compete? A phylogenetic meta-analysis. , 2019, Ecology letters.

[2]  L. Mailleret,et al.  Durable strategies to deploy plant resistance in agricultural landscapes. , 2012, The New phytologist.

[3]  J. Pickett,et al.  Plant volatile-mediated signalling and its application in agriculture: successes and challenges. , 2016, The New phytologist.

[4]  W. Price,et al.  Winter wheat (Triticum aestivum) response to Barley yellow dwarf virus at various nitrogen application rates in the presence and absence of its aphid vector, Rhopalosiphum padi , 2019, Entomologia Experimentalis et Applicata.

[5]  Nik J. Cunniffe,et al.  Optimising Reactive Disease Management Using Spatially Explicit Models at the Landscape Scale , 2019, Plant Diseases and Food Security in the 21st Century.

[6]  N. Cunniffe,et al.  An eco-physiological model coupling plant growth and aphid population dynamics , 2019, bioRxiv.

[7]  S. Eigenbrode,et al.  Transmission mechanisms shape pathogen effects on host–vector interactions: evidence from plant viruses , 2012 .

[8]  Christopher A. Gilligan,et al.  Cost-Effective Control of Plant Disease When Epidemiological Knowledge Is Incomplete: Modelling Bahia Bark Scaling of Citrus , 2014, PLoS Comput. Biol..

[9]  M. Hassell,et al.  Models for Interspecific Competition in Laboratory Populations of Callosobruchus Spp. , 1984 .

[10]  S. Eigenbrode,et al.  Plant-mediated interactions between a vector and a non-vector herbivore promote the spread of a plant virus , 2019, Proceedings of the Royal Society B.

[11]  M. Fuchs,et al.  TRANSMISSION SPECIFICITY OF PLANT VIRUSES BY VECTORS , 2005 .

[12]  C. Gilligan,et al.  Pathogenic modification of plants enhances long‐distance dispersal of nonpersistently transmitted viruses to new hosts , 2019, Ecology.

[13]  Nanditta Banerjee,et al.  Mechanisms of Arthropod Transmission of Plant and Animal Viruses , 1999, Microbiology and Molecular Biology Reviews.

[14]  D. Stenger,et al.  Roguing with replacement in perennial crops: conditions for successful disease management. , 2013, Phytopathology.

[15]  B. Falk,et al.  Virus-vector interactions mediating nonpersistent and semipersistent transmission of plant viruses. , 2006, Annual review of phytopathology.

[16]  Ian Kaplan,et al.  Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. , 2007, Ecology letters.

[17]  N. Desneux,et al.  Potential for insecticide-mediated shift in ecological dominance between two competing aphid species. , 2019, Chemosphere.

[18]  J. Woodford,et al.  Some epidemiological approaches to the control of aphid-borne virus diseases in seed potato crops in northern Europe. , 2000, Virus research.

[19]  Andrea F. Huberty,et al.  Consequences of nitrogen and phosphorus limitation for the performance of two planthoppers with divergent life-history strategies , 2006, Oecologia.

[20]  W. Otten,et al.  A fungal growth model fitted to carbon-limited dynamics of Rhizoctonia solani. , 2008, The New phytologist.

[21]  L. Madden,et al.  Plant Virus Epidemiology: Applications and Prospects for Mathematical Modeling and Analysis to Improve Understanding and Disease Control. , 2017, Plant disease.

[22]  P. Berger,et al.  Is the concept of short retention times for aphid-borne nonpersistent plant viruses sound. , 1990 .

[23]  T. Bellows The Descriptive Properties of Some Models for Density Dependence , 1981 .

[24]  R. Almeida,et al.  Factors Affecting the Initial Adhesion and Retention of the Plant Pathogen Xylella fastidiosa in the Foregut of an Insect Vector , 2013, Applied and Environmental Microbiology.

[25]  J. Holt,et al.  A model of plant virus disease dynamics incorporating vector population processes: its application to the control of African cassava mosaic disease in Uganda. , 1997 .

[26]  C. Gilligan,et al.  Invasion, persistence and control in epidemic models for plant pathogens: the effect of host demography , 2010, Journal of The Royal Society Interface.

[27]  C. Gilligan,et al.  Time-dependent infectivity and flexible latent and infectious periods in compartmental models of plant disease. , 2012, Phytopathology.

[28]  O. Diekmann,et al.  On the definition and the computation of the basic reproduction ratio R0 in models for infectious diseases in heterogeneous populations , 1990, Journal of mathematical biology.

[29]  Y. Elad,et al.  A generic theoretical model for biological control of foliar plant diseases. , 2009, Journal of theoretical biology.

[30]  G. Vercambre,et al.  Nitrogen and water supplies affect peach tree–green peach aphid interactions: the key role played by vegetative growth , 2016 .

[31]  Laurence V. Madden,et al.  A model for analysing plant-virus transmission characteristics and epidemic development , 1998 .

[32]  E. Borer,et al.  Species interactions affect the spread of vector-borne plant pathogens independent of transmission mode. , 2019, Ecology.

[33]  W. Weisser,et al.  Mechanisms of species‐sorting: effect of habitat occupancy on aphids' host plant selection , 2014 .

[34]  Robert M. May,et al.  Dynamics of metapopulations : habitat destruction and competitive coexistence , 1992 .

[35]  D. Ragsdale,et al.  Aphid-transmitted potato viruses: The importance of understanding vector biology , 2002, American Journal of Potato Research.

[36]  A. Fereres,et al.  Behavioural aspects influencing plant virus transmission by homopteran insects. , 2009, Virus research.

[37]  R. Harrington,et al.  Aphids as crop pests , 2007 .

[38]  G. Powell Intracellular salivation is the aphid activity associated with inoculation of non-persistently transmitted viruses. , 2005, The Journal of general virology.

[39]  L. Nault Arthropod Transmission of Plant Viruses: a New Synthesis , 1997 .

[40]  S. Soubeyrand,et al.  Sharka epidemiology and worldwide management strategies: learning lessons to optimize disease control in perennial plants. , 2015, Annual review of phytopathology.

[41]  D. Paini,et al.  Pesticide-mediated interspecific competition between local and invasive thrips pests , 2017, Scientific Reports.

[42]  Allison K. Shaw,et al.  Vector population growth and condition-dependent movement drive the spread of plant pathogens. , 2017, Ecology.

[43]  J. Holt,et al.  Epidemiology of insect‐transmitted plant viruses: modelling disease dynamics and control interventions , 2004 .

[44]  O Diekmann,et al.  The construction of next-generation matrices for compartmental epidemic models , 2010, Journal of The Royal Society Interface.

[45]  L. Madden,et al.  A theoretical assessment of the effects of vector-virus transmission mechanism on plant virus disease epidemics. , 2000, Phytopathology.

[46]  S. Thoyer,et al.  Improving Management Strategies of Plant Diseases Using Sequential Sensitivity Analyses. , 2019, Phytopathology.

[47]  Effects of Soil Nitrogen and Atmospheric Carbon Dioxide on Wheat streak mosaic virus and Its Vector (Aceria tosichella Kiefer). , 2015, Plant disease.

[48]  R. Levins,et al.  Regional Coexistence of Species and Competition between Rare Species. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Laurence V. Madden,et al.  The study of plant disease epidemics , 2007 .

[50]  S. Soubeyrand,et al.  Assessing the Mismatch Between Incubation and Latent Periods for Vector-Borne Diseases: The Case of Sharka. , 2015, Phytopathology.

[51]  Robin N. Thompson,et al.  Some reasons why the latent period should not always be considered constant over the course of a plant disease epidemic , 2018 .

[52]  S. Soubeyrand,et al.  PESO: a modelling framework to help improve management strategies for epidemics - application to sharka , 2017 .

[53]  X. Nie,et al.  Effects of Crop Management Practices on Current-Season Spread of Potato virus Y. , 2014, Plant disease.

[54]  L. Allen,et al.  Modelling Vector Transmission and Epidemiology of Co-Infecting Plant Viruses , 2019, Viruses.

[55]  A. Agrawal,et al.  Salicylate-mediated interactions between pathogens and herbivores. , 2010, Ecology.

[56]  K. Perry,et al.  Transmission of plant viruses by aphid vectors. , 2004, Molecular plant pathology.

[57]  C. Gilligan,et al.  Thirteen challenges in modelling plant diseases. , 2015, Epidemics.

[58]  Takehiko Yamanaka,et al.  Model analysis for plant disease dynamics co-mediated by herbivory and herbivore-borne phytopathogens , 2012, Biology Letters.

[59]  S. Gils,et al.  Drought and soil fertility modify fertilization effects on aphid performance in wheat , 2018, Basic and Applied Ecology.

[60]  Christos Dordas,et al.  Role of nutrients in controlling plant diseases in sustainable agriculture. A review , 2011, Agronomy for Sustainable Development.

[61]  Christopher A Gilligan,et al.  Epidemiological models for invasion and persistence of pathogens. , 2008, Annual review of phytopathology.

[62]  D. Stenger,et al.  Disentangling Effects of Vector Birth Rate, Mortality Rate, and Abundance on Spread of Plant Pathogens , 2015, Journal of Economic Entomology.

[63]  N. Cunniffe,et al.  Spatiotemporal dynamics and modelling support the case for area‐wide management of citrus greasy spot in a Brazilian smallholder farming region , 2020 .

[64]  V. Brown,et al.  Effects of host plant drought stress on the performance of the bird cherry‐oat aphid, Rhopalosiphum padi (L.): a mechanistic analysis , 2003 .

[65]  A. Agrawal,et al.  Mechanisms and evolution of plant resistance to aphids , 2016, Nature Plants.

[66]  M. Jeger The Epidemiology of Plant Virus Disease: Towards a New Synthesis , 2020, Plants.

[67]  T. Perring,et al.  Management of plant viral diseases through chemical control of insect vectors. , 1999, Annual review of entomology.

[68]  Christopher A. Gilligan,et al.  CHAPTER 12: Use of Mathematical Models to Predict Epidemics and to Optimize Disease Detection and Management , 2020 .

[69]  J. Maynard Smith,et al.  The Stability of Predator‐Prey Systems , 1973 .

[70]  J A P Heesterbeek,et al.  The type-reproduction number T in models for infectious disease control. , 2007, Mathematical biosciences.

[71]  J. Hardie,et al.  The role of nutrition, crowding and interspecific interactions in the development of winged aphids , 2001 .

[72]  V. Brault,et al.  Aphids as transport devices for plant viruses. , 2010, Comptes rendus biologies.