Asymptomatic spread of huanglongbing and implications for disease control

Abstract

Huanglongbing (HLB) is a bacterial infection of citrus trees transmitted by the Asian citrus psyllid Diaphorina citri. Mitigation of HLB has focused on spraying of insecticides to reduce the psyllid population and removal of trees when they first show symptoms of the disease. These interventions have been only marginally effective, because symptoms of HLB do not appear on leaves for months to years after initial infection. Limited knowledge about disease spread during the asymptomatic phase is exemplified by the heretofore unknown length of time from initial infection of newly developing cluster of young leaves, called flush, by adult psyllids until the flush become infectious. We present experimental evidence showing that young flush become infectious within 15 d after receiving an inoculum of Candidatus Liberibacter asiaticus (bacteria). Using this critical fact, we specify a microsimulation model of asymptomatic disease spread and intensity in a grove of citrus trees. We apply a range of psyllid introduction scenarios to show that entire groves can become infected with up to 12,000 psyllids per tree in less than 1 y, before most of the trees show any symptoms. We also show that intervention strategies that reduce the psyllid population by 75% during the flushing periods can delay infection of a full grove, and thereby reduce the amount of insecticide used throughout a year. This result implies that psyllid surveillance and control, using a variety of recently available technologies, should be used from the initial detection of invasion and throughout the asymptomatic period.asymptomatic huanglongbing | latent period | transmission model | control strategies T he main symptoms of huanglongbing (HLB) in citrus trees are yellow shoots, leaves with blotchy mottle, and small lopsided fruits. Ultimately, infected branches die back and the tree dies. The putative causal agent of HLB is an alpha-proteobacterium, Candidatus Liberibacter asiaticus (Ca. Las), that resides within the phloem and is transmitted by the Asian citrus psyllid Diaphorina citri Kuwayama. The highest concentrations of Ca. Las in infected trees are in the stem and midribs of flush. The flush is a newly developing cluster of very young leaves on the expanding end of a terminal shoot. The bacterium multiplies in both the psyllids and the trees, but the psyllids are essential for the spread of the disease.The dominant control measure currently in use is the combination of insecticidal spraying to limit the psyllid populations and removal of infected trees, an inoculum source, when they are symptomatic. This strategy has had only marginal effect because symptoms appear anywhere from months to years after an initial infection, long after the trees have been active in the transmission process (1). Presymptomatic trees can serve as a source of inoculum for psyllids, but the length of time from initial infection of a tree until it is infective as a source of inoculum is known from experimental measurements only to within coarse bounds (within 60 d) (1). A...

Mathematical models are a powerful method to understand and control the spread of Huanglongbing

“…We review here those models which have been applied to HLB because they demonstrate the major insights models have already provided to this disease system. Recent modeling of HLB includes Jacobsen, Stupiansky & Pilyugin (2013), Parry et al (2014) and Lee et al (2015). These articles elucidate the spread of HLB using three different approaches, namely through differential equation modeling, statistical analysis, and individual-based modeling, respectively.…”

“…Finally, Lee et al (2015) combine experiments and individual-based mathematical models. The main experimental result was that, despite being asymptomatic, the host plant can become infectious in a shorter time than previously thought, within 15 days.…”

“…Thus, if the grower knows that the psyllids were blown in by wind, they should expect that a more intense control strategy is necessary to have any chance of stopping infection. Through mathematical modeling, Lee et al (2015) also found that it is possible for the whole grove to be infected before the first symptoms appear on any tree. From this, they emphasize the need to control psyllid populations regardless of whether any trees have shown symptoms because transmission may already be occurring from asymptomatic trees.…”

“…We use a similar mechanistic modeling approach to Jacobsen, Stupiansky & Pilyugin (2013) while incorporating realistic parameter values and including data on the temperature dependency of psyllid vital rates. Both Parry et al (2014) and Lee et al (2015) include seasonal aspects within their models, but our model is the first to incorporate the role of temperature on psyllid traits for a wide range of temperature values.…”

Protein interaction networks at the host–microbe interface inDiaphorina citri, the insect vector of the citrus greening pathogen

“…The ACP lays its eggs on young flush tissue, and high levels of CLas accumulate locally as infected adults feed during oviposition. Young citrus flush tissue can become infectious as early as 15 days after psyllid inoculation [7], suggesting a model whereby systemic infection of the tree is not necessary for tree-to-tree spread. After emergence from eggs onto infected plants, ACP nymphs begin feeding from the phloem and are exposed to the bacterium, which crosses the first barrier to circulative transmission by acquisition into cells of the insect gut [8].…”