Xavier Martini

Seasonal Movement Patterns and Long-Range Dispersal of Asian Citrus Psyllid in Florida Citrus

ABSTRACT The Asian citrus psyllid, Diaphorina citri Kuwayama, is the vector of the bacterial pathogen, Candidatus Liberibacter asiaticus, which is the causal agent of huanglongbing (HLB) in the United States. Both short-range and long-range dispersal of D. citri adults affect the spread of HLB; however, little is known about the long-range dispersal capabilities of D. citri in the field or the seasonality of flight behavior. In the present study, an in situ protein marking technique was used to determine the dispersal of D. citri by trapping marked adults under natural field conditions. D. citri movement from abandoned citrus groves to adjacent managed citrus groves was greatest during the spring and summer months and decreased significantly during the colder months (September–March). D. citri were able to traverse potential geographic barriers such as roads and fallow fields. In an experiment conducted to determine long-range dispersal capacity in the absence of severe weather events, D. citri were able to disperse at least 2 km within 12 d. Wind direction was not correlated with the number of marked psyllids captured, indicating substantial flight capability by D. citri. Finally, the number of marked psyllids captured increased with the density of emerging young leaves on surrounding trees. The results confirm that abandoned citrus groves in Florida serve as reservoirs for D. citri, which can disperse across long distances despite geographical barriers.

Volatiles from the symbiotic fungus Raffaelea lauricola are synergistic with Manuka lures for increased capture of the Redbay ambrosia beetle Xyleborus glabratus

Redbay ambrosia beetle Xyleborus glabratus is an invasive wood boring beetle that has become established in the southeastern U.S.A. and transmits a fungus Raffaelea lauricola that causes lethal laurel wilt. Among susceptible Lauraceae hosts are redbay Persea borbonia and avocado Persea americana. There is a crucial need for detection of this pest as it moves into new areas. Consequently, our goal was to create a better lure for the monitoring and control of redbay ambrosia beetle. We analyzed volatile emissions of R. lauricola, created a synthetic odour blend based on this analysis and tested this odour blend as a potential attractant in a redbay forest infested with X. glabratus. The synthetic Raffaelea odour blend was not attractive to the beetles by itself. However, it synergistically increased attraction to host‐mimic volatiles. We tested four commercial release devices for dispensing Raffaelea odour at various release rates. Two prototypes with the highest release rate, when paired with commercial manuka oil lures, captured more beetles than manuka oil lures alone. These results indicate that a synthetic blend of volatiles based on the odour of the symbiotic fungus of X. glabratus may be useful for the development of more sensitive monitoring lures for this invasive pathogen vector.

Abdominal Color of the Asian Citrus Psyllid (Hemiptera: Liviidae) Is Associated With Flight Capabilities

ABSTRACT We examined the propensity for flight initiation and flight capability of the Asian citrus psyllid (Diaphorina citri Kuwayama, Hemiptera: Liviidae) with a flight mill. We measured continuous flight by D. citri for up to 3 h, which equated to a distance of ≈2.4 km. We compared the flight capability of D. citri depending on their sex and morphotype (color of abdomen). Two general morphotypes exist within this species: green-blue and gray-brown. We observed that ≈32% of psyllids from the green-blue morphotype tested exhibited long durations of flight (>60 s); whereas <5% of psyllids from the gray-brown morphotype performed such long duration flights. There was no significant difference in flight performance between the two sexes within both the gray—brown and green—blue morphotypes. Furthermore, psyllids from the gray—brown morphotype were characterized by smaller pronotums and shorter wings than psyllids from the green—blue morphotype. In addition, males, in general, were characterized by smaller pronotums and shorter wings than females. However, neither pronotum nor wing size were associated with flight capability of D. citri. Our results may help explain dispersal behavior of D. citri with respect to practical management on an area-wide scale.

Infection of an Insect Vector with a Bacterial Plant Pathogen Increases Its Propensity for Dispersal

The spread of vector-transmitted pathogens relies on complex interactions between host, vector and pathogen. In sessile plant pathosystems, the spread of a pathogen highly depends on the movement and mobility of the vector. However, questions remain as to whether and how pathogen-induced vector manipulations may affect the spread of a plant pathogen. Here we report for the first time that infection with a bacterial plant pathogen increases the probability of vector dispersal, and that such movement of vectors is likely manipulated by a bacterial plant pathogen. We investigated how Candidatus Liberibacter asiaticus (CLas) affects dispersal behavior, flight capacity, and the sexual attraction of its vector, the Asian citrus psyllid (Diaphorina citri Kuwayama). CLas is the putative causal agent of huanglongbing (HLB), which is a disease that threatens the viability of commercial citrus production worldwide. When D. citri developed on CLas-infected plants, short distance dispersal of male D. citri was greater compared to counterparts reared on uninfected plants. Flight by CLas-infected D. citri was initiated earlier and long flight events were more common than by uninfected psyllids, as measured by a flight mill apparatus. Additionally, CLas titers were higher among psyllids that performed long flights than psyllid that performed short flights. Finally, attractiveness of female D. citri that developed on infected plants to male conspecifics increased proportionally with increasing CLas bacterial titers measured within female psyllids. Our study indicates that the phytopathogen, CLas, may manipulate movement and mate selection behavior of their vectors, which is a possible evolved mechanism to promote their own spread. These results have global implications for both current HLB models of disease spread and control strategies.

Eucalyptol is an attractant of the redbay ambrosia beetle, Xyleborus glabratus.

The redbay ambrosia beetle, Xyleborus glabratus, is an invasive wood-boring beetle that has become established in the southeastern United States. The beetle transmits the causal pathogen of lethal laurel wilt to susceptible host trees, which include redbay, an important forest community species, and avocado, a valuable food crop. By examining odors of redbay wood, we developed an artificial lure that captured X. glabratus in redbay forests. Eucalyptol was a critical component of the blend for beetle attraction, and eucalyptol alone in large quantities attracted X. glabratus. Furthermore, eucalyptol stimulated boring by X. glabratus into paper arenas. The results suggest that eucalyptol contributes to host selection behavior of X. glabratus and may be useful for management of this pathogen vector.

Plant volatiles and density-dependent conspecific female odors are used by Asian citrus psyllid to evaluate host suitability on a spatial scale

We investigated how chemical cues derived from female Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae) and their host plants affect host acceptance choices by conspecifics. In four-choice cage and two-choice olfactometer assays, female psyllids avoided conspecific female cues in a density-dependent manner. However, odors from citrus plants actively damaged by psyllid feeding were attractive to conspecific females. When odors from feeding-damaged plants were presented simultaneously with odors from female D. citri, attraction of female conspecifics was no longer observed as compared with a clean air control in olfactometer assays. In subsequent experiments, D. citri females were released within arenas that contained actively feeding-damaged or non-damaged (control) citrus plants, each with previously psyllid-infested and uninfested young leaves. D. citri development is linked to the presence of these newly emerging leaves which is the only site of nymphal development. Female D. citri were initially attracted by the actively damaged plants as compared with non-damaged controls. After acceptance of plants that were actively damaged by feeding, D. citri females preferentially chose and settled on uninfested young leaves as compared with previously infested young leaves. A herbivore-induced plant volatile attractant and a female-specific odor repellent appear to be complementary foraging cues providing psyllids with information at two spatial scales: (1) the whole plant level for choosing a plant potentially harboring male conspecifics for mating, and (2) the within plant level to reduce intra-conspecific competition by identifying previously exploited resources.

Occurrence of Diaphorina citri (Hemiptera: Liviidae) in an Unexpected Ecosystem: The Lake Kissimmee State Park Forest, Florida

SUMMARY The current investigation describes the capture of Asian citrus psyllid (ACP), Diaphorina citri, in an unexpected ecosystem, the Lake Kissimmee State Park forest. In this forest, occurrence of citrus is particularly rare, and no Rutaceae were found within the trapping locations or in nearby (≈500 m) areas. In addition to trap capture data, complementary laboratory no-choice feeding bioassays suggest that ACP may have a broader alternative plant feeding range than previously thought, which may allow for significant dispersal even through dense forests in Florida up to 2.3 km from large-area plantings of citrus.

Attraction of Redbay Ambrosia Beetle, Xyleborus Glabratus, To Leaf Volatiles of its Host Plants in North America

The redbay ambrosia beetle, Xyleborus glabratus, is an important pest of redbay (Persea borbonia) and swamp bay (P. palustris) trees in forests of the southeastern USA. It is also a threat to commercially grown avocado. The beetle is attracted to host wood volatiles, particularly sesquiterpenes. Contrary to other ambrosia beetles that attack stressed, possibly pathogen-infected, and dying trees, X. glabratus readily attacks healthy trees. To date little is known about the role of leaf volatiles in the host selection behavior and ecology of X. glabratus. To address this question, an olfactometer bioassay was developed to test the behavioral response of X. glabratus to plant leaf volatiles. We found that X. glabratus was attracted to the leaf odors of their hosts, redbay and swamp bay, with no attraction to a non-host tree tested (live oak, Quercus virginiana), which served as a negative control. Gas chromatography–mass spectrometry (GS/MS) analysis of leaves revealed the absence of sesquiterpenes known to be attractive to X. glabratus and present in host wood, suggesting that additional leaf-derived semiochemicals may serve as attractants for this beetle. An artificial blend of chemicals was developed based on GC/MS analyses of leaf volatiles and behavioral assays. This blend was attractive to X. glabratus at a level that rivaled currently used lures for practical monitoring of this pest. This synthetic redbay leaf blend also was tested in the field. Baited traps captured more X. glabratus than unbaited controls and equivalently to manuka oil lures. We hypothesize that leaf volatiles may be used by X. glabratus as an additional cue for host location.

The Influence of Learning on Host Plant Preference in a Significant Phytopathogen Vector, Diaphorina citri

Although specialist herbivorous insects are guided by innate responses to host plant cues, host plant preference may be influenced by experience and is not dictated by instinct alone. The effect of learning on host plant preference was examined in the Asian citrus psyllid, Diaphorina citri; vector of the causal agent of citrus greening disease or huanglongbing. We investigated: a) whether development on specific host plant species influenced host plant preference in mature D. citri; and b) the extent of associative learning in D. citri in the form of simple and compound conditioning. Learning was measured by cue selection in a 2-choice behavioral assay and compared to naïve controls. Our results showed that learned responses in D. citri are complex and diverse. The developmental host plant species influenced adult host plant preference, with female psyllids preferring the species on which they were reared. However, such preferences were subject to change with the introduction of an alternative host plant within 24–48 hrs, indicating a large degree of experience-dependent response plasticity. Additionally, learning occurred for multiple sensory modalities where novel olfactory and visual environmental cues were associated with the host plant. However, males and females displayed differing discriminatory abilities. In compound conditioning tasks, males exhibited recognition of a compound stimulus alone while females were capable of learning the individual components. These findings suggest D. citri are dynamic animals that demonstrate host plant preference based on developmental and adult experience and can learn to recognize olfactory and visual host plant stimuli in ways that may be sex specific. These experience-based associations are likely used by adults to locate and select suitable host plants for feeding and reproduction and may suggest the need for more tailored lures and traps, which reflect region-specific cultivars or predominate Rutaceae in the area being monitored.

Disruption of Vector Host Preference with Plant Volatiles May Reduce Spread of Insect-Transmitted Plant Pathogens

Plant pathogens can manipulate the odor of their host; the odor of an infected plant is often attractive to the plant pathogen vector. It has been suggested that this odor-mediated manipulation attracts vectors and may contribute to spread of disease; however, this requires further broad demonstration among vector-pathogen systems. In addition, disruption of this indirect chemical communication between the pathogen and the vector has not been attempted. We present a model that demonstrates how a phytophathogen (Candidatus Liberibacter asiaticus) can increase its spread by indirectly manipulating the behavior of its vector (Asian citrus psyllid, Diaphorina citri Kuwayama). The model indicates that when vectors are attracted to pathogen-infected hosts, the proportion of infected vectors increases, as well as, the proportion of infected hosts. Additionally, the peak of infected host populations occurs earlier as compared with controls. These changes in disease dynamics were more important during scenarios with higher vector mortality. Subsequently, we conducted a series of experiments to disrupt the behavior of the Asian citrus psyllid. To do so, we exposed the vector to methyl salicylate, the major compound released following host infection with the pathogen. We observed that during exposure or after pre-exposure to methyl salicylate, the host preference can be altered; indeed, the Asian citrus psyllids were unable to select infected hosts over uninfected counterparts. We suggest mechanisms to explain these interactions and potential applications of disrupting herbivore host preference with plant volatiles for sustainable management of insect vectors.