Wind Speed and Direction Drive Assisted Dispersal of Asian Citrus Psyllid
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Environmental Entomology, XX(XX), 2021, 1–8
https://doi.org/10.1093/ee/nvab140
Research
Behavioral Ecology
Wind Speed and Direction Drive Assisted Dispersal of
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Asian Citrus Psyllid
Carlos A. Antolínez,1,4, Xavier Martini,2, Lukasz L. Stelinski,3, and Monique J. Rivera1
1
Department of Entomology, University of California Riverside, Riverside, CA 92521, USA,2North Florida Research and Education
Center, Department of Entomology and Nematology, University of Florida, Quincy, FL 32351, USA,3Citrus Research and Education
Center, Department of Entomology and Nematology, University of Florida, Lake Alfred, FL 33850, USA, and 4Corresponding author,
e-mail: carlosa@ucr.edu
Subject Editor: Matthew Ginzel
Received 25 August 2021; Editorial decision 11 November 2021
Abstract
Wind directly influences the spread of vector-borne plant pathogens by driving the passive dispersal of vectors to
potentially new areas. Here, we evaluated the effect of wind speed and direction on the dispersal of the Asian citrus
psyllid (ACP), Diaphorina citri (Kuwayama) (Hemiptera: Psyllidae), the vector of the bacteria causing huanglongbing
(HLB), a lethal disease of citrus. The effect of different wind speeds on short or long-distance dispersal of ACP
was investigated using a high-speed wind tunnel under laboratory conditions. The effect of wind direction on ACP
dispersal under field conditions was evaluated using custom-made wind vane-style traps. In wind tunnel assays,
ACP remained on plants until wind treatments reached ≥48 km/h when psyllids were mostly dislodged from plants
and moved by the wind. For a short-distance, wind-driven movement (movement by the wind from one plant to
another), the effect of wind speed was not significant at any of the wind speed treatments tested. Wind vane traps
placed in a Florida citrus grove captured significantly more ACP on the windward side, suggesting that ACP were
moved with the wind.The number of ACP found on the windward side of traps was significantly higher from May to
August. These results indicate that ACP is likely to disperse with prevailing wind direction and that settled ACP may
become dislodged and moved at random by high wind speeds occurring in areas of significant citrus production
(southern California, Florida, or Texas).
Key words: dispersion, citrus greening, high wind, flight capability, wind vane trap
Vector-borne pathogens depend on their insect vectors to spread or increase dispersal distance (Pedgley 1983, Kennedy 1990, Haine
to new areas or hosts (Fereres 2015). Therefore, understanding 1955, Compton 2002). The overall effect of wind on flight behavior
vector dispersal is essential to understanding the epidemiology of is also dependent on insect characteristics such as size, mass, shape,
vector-transmitted diseases. Vector dispersal is difficult to measure and flight capacity (Pasek 1988). Despite the importance of under-
and predict because it is potentially affected by a complex suite of standing how wind contributes to the dispersal capacity of vectors of
environmental factors such as temperature, humidity, precipitation, plant diseases, few studies have focused on the wind as a driver for
barometric pressure, and wind (Hall and Hentz 2011, Martini et al. variation in vector dispersion, probably due to the difficulty to study
2018, Tomaseto et al. 2018, Stelinski 2019, Antolinez et al. 2021). small insects while they disperse.
Among these environmental factors, the wind is especially important The Asian citrus psyllid (ACP) Diaphorina citri: Kuwayama
for flying insects because it may modify flight behavior at different (Hemiptera: Psyllidae) is an invasive pest that has spread into citrus
levels (Compton 2002). Wind affects the direction and distance production regions throughout the world. ACP is the vector of
of the flight and can also impact dispersal behaviors by influenc- Candidatus Liberibacter asiaticus (CLas), the presumed causal agent
ing early stages of flight, such as take-off (Verdonschot and Besse- of huanglongbing (HLB), a lethal bacterial disease of citrus. HLB
Lototskaya 2014). Depending on wind intensity and the flight stage has caused massive economic loss to the citrus industry in the most
where the wind is perceived, the wind has the potential to decrease important citrus-producing countries, including the United States
© The Author(s) 2021. Published by Oxford University Press on behalf of Entomological Society of America.
All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
12 Environmental Entomology, 2021, Vol. XX, No. XX (Jagoueix et al. 1994, Bové 2006). Typical symptoms of HLB include wind gusts. Similarly, there has been a lack of congruence between blotchy-mottle patterns on leaves and deformed and off-flavor fruits, different investigations on the effect that wind speed imposes on causing a significant reduction in yield and marketable fruit for the the likelihood of ACP movement. While no correlation between fresh market (Bassanezi et al. 2009, Spreen et al. 2014). Infected wind speed and dispersion has been observed under field conditions trees may die within 5 to 10 yr after initial infection as a result of (Croxton 2015), a more direct assessment of ACP behavior using phloem blockage and impaired sugar transport (Bové 2006, Baldwin flight tunnels and flight mills suggested that ACP dispersion may be et al. 2010, Dala-Paula et al. 2018). Citrus trees become infected highly correlated with wind speed (Martini et al. 2018). However, when ACP harboring CLas inoculate them with the pathogen via the later study has been conducted with a wind tunnel with relatively salivary secretion while feeding in phloem tissues (Luo et al. 2015, low speed (
Environmental Entomology, 2021, Vol. XX, No. XX 3
frame was built for the rear end of the rectangular cage and a white 29.21 cm width, length, and height. Next, two additional squares
polyester sweep net (BioQuip Products, Rancho Dominguez, CA), of corrugated plastic of 22.86 × 22.86 were obtained and glued by
1.2 m long, was attached to the frame to catch those ACP that be- adding two-part epoxy (JB Weld, Sulphur, TX) to cover the top and
came airborne and were expelled by the wind velocity treatment. the bottom to form a closed rectangular box. The two squares added
The frame on the front end of the rectangular cage was attached to at the top and bottom were secured to the sides of the box with duct
the frame of the high-speed wind tunnel. Two circular holes 15 cm tape. Later, yellow sticky cards (24.5 cm × 13.2 cm) (Great Lakes
in diameter were made in the polycarbonate sheet at the floor of the IPM, Vestaburg, MI) were attached to the four lateral sides of the
rectangular box to insert two pots that each contained a 1-yr-old box. Then, two holes, 1.27 cm and 15.24 cm from the base were
Citrus limon ‘Eureka’ tree (Supp Fig. S1 [online only]). The first drilled centrally through the complete box and two fiber tent poles
lemon tree was placed inside the cage at 30 cm from the jet of the (43.18 cm) were inserted through the holes. One corrugated plastic
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wind tunnel. trapezoid (22.86 cm × 17.78 cm) wind catch was inserted at one end
The first tree (plant number 1) was infested with 150 ACP 24 and approximately 11.43 cm away from the box. At the opposite
hours before the start of the experiment. At the initiation of the ex- side away from the poles, a corrugated plastic sheet (22.86 × 3.81)
periment, a second tree (noninfested) (plant number 2) was intro- with five metal washers (Everbilt/Home Depot, Atlanta, GA) painted
duced into the cage 30 cm behind (downwind) the infested tree, and white was added as a counterbalance. Thereafter, the flat surface of
immediately thereafter, the wind tunnel was turned on to generate a swivel caster (Everbilt/Home Depot, Atlanta, GA) was glued to
the windspeed treatment. After two hours of the desired constant the ventral side of the trap and affixed to a 152 cm wooden pole
airflow, the assay was terminated and the following outcomes were (Douglas fir wood, Everbilt/Home Depot, Atlanta, GA). In Florida,
recorded: 1) number of insects settled in plant number 1, 2) number the pole was inserted directly into the ground. In California, the pole
of insects that migrated to plant number 2 (short-distance move- was placed in the center of an 18.92 L bucket (Everbilt/Home Depot,
ment) 3) number of insects on the walls, roof and floor of the Atlanta, GA) filled with cement (Quickrete, The Quickrete company,
tunnel and 4) the number of insects moved downwind to the net Atlanta, GA). An image of the wind vane trap installed in California
(long-distance movement). ACP movement was assessed under dif- is provided in (Supp Fig. S2a [online only]). A total of four traps
ferent wind speeds according to Beauford scale (Table 1). The wind were deployed in the field per location. Each trap was placed at least
speed produced by the tunnel was measured with a digital anemom- 100 m away from one another. To measure wind speed and direc-
eter (HoldPeak (HP-866B), Zhuhai, China). A total of six replicates tion, a sensor (S-WCF-M003 Davis Wind speed and direction sensor,
per treatment were performed and all replicates were conducted on Onset computer corporation, Bourne, MA) connected to a HOBO
different days from 10:00 to 15:00 h. This time frame was selected to micro station (H21-USB, Onset computer corporation, Bourne, MA)
conduct assays because ACP have are most active during these hours was placed near each wind vane trap. Data from the wind station
of the day (Wenninger and Hall 2007). The percentage of recovered and the number of ACP captured at each side of the trap were re-
insects in each of the four outcomes was calculated and compared corded biweekly.
by analysis of variance (ANOVA) on ranks as the data were not nor- The experiment was deployed in two geographically separate
mally distributed. Data were analyzed using the SPSS v 24 statistical locations. The experiment in Florida was conducted from 1 May
software (IBM Corp 2016, Armonk, NY). to 31 August 2017 in a 30 ha ‘Hamlin’ sweet orange grove under
standard agricultural practices for citrus, including mowing and fer-
Effect of Wind Direction tilization, located in Lake Alfred (28.116646, −81.710514). Trees
In the field, the angle of exposure of a yellow sticky trap commonly were planted on 3 × 6 m (3 m between each individual tree within
used to sample ACP varies as wind direction changes during the day. the row and 6 m between each row) and were 4–5 yrs old. The four
To overcome this problem, we mounted yellow sticky cards on a traps were placed between rows. In California, the experiment was
cube-shaped, rotating, wind vane-style trap that shifted with the pre- deployed in a plot consisting of 145 navel orange trees (5.575 m2) lo-
vailing wind direction (Supp Fig. S2a [online only]). Thus, one side of cated in Agricultural Operations University of California, Riverside
the trap (the windward side of the trap) was exposed to the oncoming (33.972110, −117.318213). This plot has never been treated with
wind at all times, while the opposite side was positioned at all times insecticides. Notably, the trees in the California experiment were 35
against the oncoming wind (leeward side of the trap) (Supp Fig. S2b yrs old and fully grown large trees. Traps were placed on the outer
[online only]). To build the trap, a corrugated plastic sheet (white edge of the grove since the canopy of the trees was closed, not al-
corrugated plastic sheet, Columbus, OH) of 29.21 cm × 91.44 cm lowing for the traps to be placed between trees on the interior of the
(width × length) was cut to obtain four 22.86 cm × 29.21 cm (width grove. The experiment was established in California from 1 October
× length) sections. These sections were bent 90 degrees at the site of 2020 to 27 July 2021.
each cut to form a rectangular prism with 22.86 cm × 22.86 cm × Captures on different sides of the wind vane were analyzed using
an ANOVA on ranks, as the data were not normally distributed. We
conducted a multiple linear correlations with the number of ACP
Table 1. Wind speeds tested in the wind tunnel experiment and captures per day as the response variable and wind speed and tem-
their classification according to the Beauford wind scale perature as explanatory variables. Finally, we conducted a nonlinear
Wind speed treatment (km/h) Beaufort wind scale regression between wind speed and ACP captured on the whole wind
vane.
No wind Calm
8 Light breeze
24.1 Moderate breeze Results
35.4 Fresh breeze Effect of High-Velocity Wind
48.2 Strong breeze
Wind speed significantly affected the percentage of settled insects
64.4 Gale
on plant 1 (H = 32.28, df = 6, P < 0.01) but not plant 2 (H = 6.98,
96.5 Storm
df = 6, P = 0.32) (Fig. 1a and b). There were no significant differences4 Environmental Entomology, 2021, Vol. XX, No. XX
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Fig. 1. Mean percentage (±SE) of: (a) settled Asian citrus psyllids, Diaphorina citri, (ACP) on infested Lemon trees, (b) ACP dispersed to plant 2, (c) ACP dispersed
into the net, or (d) ACP located on the walls, roof and floor of the tunnel two hours after exposure to various wind speeds in a wind tunnel. Means followed by
different letters are significantly different. *There were no insects on plant 2 at wind speeds of 64.4 and 96.5.
in the percentage of insects settled on plant 1 between still air, 8,
24.1, and 35.4, km/h with percentages ranging between 78 and 93%
(Fig. 1a). However, the percentage of insects settled on plant 1 was
significantly lower for 48.2, 64.4, and 96.5 km/h when compared to
the other wind speed treatments evaluated (Fig. 1a). The treatment
with the fewest psyllids settling on plant 1 was 96.5 km/h with only
6.18 % of psyllids remaining on this plant, on average, after 2 h
of continuous wind (Fig. 1a). On the other hand, the percentage of
insects found settled on the net in response to the wind treatments
exhibited an inverse trend to that observed for those settling on plant
1 (Fig. 1a and c). The percentage of insects dispersing to the net
was significantly higher at 96.5 km/h than at all other wind speeds,
except for 64.4 km/h (H = 36.02, df = 6, P < 0.01) (Fig. 1c). There
were no significant differences between 48.2 and 64.4 km/h; signifi-
cantly more psyllids were displaced to the net at 48.2 km/h than that Fig. 2. Mean number (±SE) of Asian citrus psyllids (Diaphorina citri) captured
observed at the lower wind speeds tested. Furthermore, there were in reference to prevailing wind direction as captured by moving wind vane
no significant differences between the wind treatments ranging from trap. Different letters indicate significant (P < 0.05) it captures between the
different sides of the wind vane.
still air to 35.4 km/h (Fig. 1c). Few psyllids were found in the tunnel
and not on plants and wind speed treatments did not affect this out-
come statistically (H = 9.58, df = 6, P = 0.14) (Fig. 1d). respect to prevailing wind direction (H = 32.84, df = 3, P < 0.01)
(Fig. 2). There were no differences in the number of ACP cap-
tured between the leeward, left, or right sides of the trap (Fig. 2).
Effect of Wind Direction The number of ACP captured on the windward side of the traps
In the citrus grove in Florida, significantly more ACP was captured was higher than that found on any of the other orientations during
on the windward side of the trap than any other orientation with all sampling dates (Fig. 3). Furthermore, there were no differencesEnvironmental Entomology, 2021, Vol. XX, No. XX 5
Pedgley 1983, Haine 1955). For small insects, flight initiation de-
creases as wind speed increases (Walters and Dixon 1984, Kennedy
1990, Haine 1955, Isaacs et al. 1999). Flight direction and distance
are under insect control if insect-generated flight speed exceeds wind
speed. Otherwise, insect displacement is primarily influenced by
prevailing wind direction (Kring 1972, Service 1980, Pedgley 1983,
Pasek 1988, Compton 2002). Thus, the interaction between wind
speed and insect flight capacity affects insect displacement in space
and this interaction is both taxon-specific and in some cases, region
specific. Despite the importance of ACP dispersion on HLB spread,
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the effect of wind on ACP dispersal is not completely understood. In
this work, we demonstrated that both wind direction and speed have
a substantial influence on ACP dispersal.
Fig. 3. Mean number (±SE) of Asian citrus psyllids (Diaphorina citri) captured ACP has a strong tendency for a clumped distribution in orchards
in reference to prevailing wind direction on different sides of wind vane traps that is often highly stable (Van der Berg et al. 1988, Kobori et al.
during 4 mo of sampling. Diamond and dotted line represent captures at the 2011); ACP typically move only short distances with a characteristic
leeward side, black squares and solid line represent captures at the right side, jumping and landing behavior or by performing short flights (Aubert
triangles and solid line represent captures at the windward side and circles
and Xia 1990, Martini et al. 2014). Conversely, long-range dispersal
and dashed line represent captures at the left side. Different letters indicate
is only observed when environmental conditions such as flush avail-
a significant differences (P < 0.05) it captures between the different sides of
the wind vane. ability, psyllid density, temperature, humidity or barometric pressure
induce psyllids to engage in long-range flights (Tomaseto et al. 2016,
2018, Martini et al. 2018, Antolinez et al. 2021, Zorzenon et al.
2021). The data generated by the high-speed wind tunnel assay are
consistent with previous observations, indicating that ACP exhibit a
strong tendency to remain relatively sessile after the initial coloniza-
tion of plant surfaces for feeding (Kobori et al. 2011). Our results
indicated that attachment onto the surface was relatively secure and
only stronger wind velocities (≥48 km/h) were able to dislodge settled
psyllids to cause involuntary dispersion. The remarkable capacity of
ACP adults to remain attached to the plant under considerable wind
speeds was unexpected for an insect of its size. Adult ACP feeds by
putting their head adjacent to their leaf surface and their abdomen
raised at a 45 degree angle from the plant surface. Anecdotally, we
observed ACP lowering themselves closer to the plant surface and/
or moving to the leaves/branches with less exposure to direct wind
during our assays and the position shift behavior may be an add-
itional mechanism of avoiding dislodgement. However, in the assay,
Fig. 4. Nonlinear regression showing the effect of wind speed on the capture the insects were too small to determine whether these behaviors were
of Asian citrus psyllids (Diaphorina citri) on wind vane traps (R2 = 0.28). correlated with specific wind velocities. Presumably, ACP attachment
to plant surfaces occurs via the tarsi and/or stylet formation, and it
between the numbers of insects captured on the leeward, left, or is possible the angled disposition of the abdomen relative to the leaf
right sides of the trap during any sampling date. surface allows the insect to maintain attachment even under rela-
Finally, multiple linear regression showed that the number of tively high wind velocity. The specific mechanisms explaining ACP
insects captured on the traps decreased at higher wind speeds (co- attachment to plant surfaces deserves further investigation. The wind
efficient: −0.23 ± 0.09, P = 0.03) (Fig. 4), while temperature did strength required to dislodge ACP from plant surfaces and forcing
not affect the number of ACP captured (coefficient: −0.10 ± 0.07, passive dispersal, as characterized by the Beaufort wind scale, was a
P = 0.19). The best fit was obtained by applying a nonlinear regres- strong breeze. However, in large, mature trees, ACP may find shelter
sion with a linear decay equation: f(x) = 0.10 + 1.29e−0.39x. Due to within the tree canopy which could reduce their exposure to wind
the very low number of ACP captured in the plot located at UC and thus reduce the likelihood for dislodgement. Consequently, it is
Riverside, data were not used for the statistical analyses but are pre- possible that under field conditions, the wind speed needed to dis-
sented in Supp Table S1 (online only). lodge ACP may be even higher than that measured in the current
wind tunnel investigation.
Insect flight path becomes random if the wind speed is higher
Discussion than maximum insect flight speed (Pedgley 1983, Compton 2002).
Dispersal of flying insects is strongly influenced by wind (Service Therefore, small insects are only capable of performing controlled
1980, Pedgley 1983, Pasek 1988, Haine 1955, Chapman et al. 2010, and directed flights towards specific cues/stimuli near ground level in
2015, Verdonschot and Besse-Lototskaya 2014, Huestis et al. 2019). the boundary layer, where flight speed typically exceeds wind speed.
In still air, flight direction deviates from the random movement be- Above the boundary layer, insects are always moved by wind beyond
cause of taxis in response to environmental cues/stimuli, and distance their control (Taylor 1974). The boundary layer concept is dynamic
flown is determined by flight speed and duration (Pedgley 1983). and varies depending on insect flight capacity but also depending
However, under the continuous wind, take-off propensity as well as on meteorological or biotic conditions such as the presence of dense
direction and distance may be affected by wind speed (Service 1980, plant canopies. ACP is generally considered to be weak flyers based6 Environmental Entomology, 2021, Vol. XX, No. XX
on the size of flight muscles relative to wing size (Husain and Nath When flying outside of the boundary layer, the distance dispersed will
1927, Sakamaki 2005) and field evidence shows that flight activity is depend on the wind speed and the height reached by psyllids when
more pronounced at heights near the apex of the predominant host encountering wind. Dispersal distance is likely to increase if ACP
plant canopy (appx. 1–1.5 m above ground) (Aubert and Xia 1990, moves beyond the boundary layer in a vertical flight or if the insect is
Hall and Hentz 2011). As wind speed increases with aboveground caught in an updraft and thus, propelled into higher atmospheric lay-
height, it is likely that at heights above the host plant canopy, the cap- ers where the wind is stronger, as occurs with aphids (Reynolds and
acity for ACP to perform controlled flights diminishes. This is con- Reynolds 2009, Parry 2013). ACP captures do not typically occur
sistent with our results indicating the highest overall captures on the beyond 8.5 m above the ground (Johnston et al. 2019) suggesting
wind vane traps when wind speeds were between 0.5 and 2 km/h, that movement in higher atmospheric layers is likely uncommon.
which then decreased as wind speeds increased. Because ACP cap- When reaching those heights, it has been speculated that ACP can
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tures on the yellow sticky traps used in this study depend on visual disperse distances ranging between 0.5 to 4 km depending on wind
attraction to a small area, once ACP locates a trap, they must perform speed (Aubert and Xia 1990, Hall and Hentz 2011). However, more
directed flight towards the trap. At wind speeds exceeding ACP cap- studies are needed to determine the vertical distance of ACP dispersal
acity for directed flight, ACP capture on trap targets should diminish. to fully understand the risk from assisted dispersal in the upper wind
In Florida, ACP was captured in low numbers on wind vane column. Recently and unexpectedly, it was discovered that different
traps from directions perpendicular to and upwind of prevailing species of the Anopheles sp (Diptera: Culicidae) mosquitoes, which
wind direction. However, ACP captures were consistently greatest are also known to be poor fliers, can reach high altitudes and can be
on the windward side of wind vane traps throughout the trapping transported distances up to 300 km (Huestis et al. 2019), and such
period, indicating that wind direction consistently affected the dir- possibilities cannot be ruled out for ACP. Factors that induce ver-
ection of ACP movement in the field. This is congruent with pre- tical flight in ACP also deserve further investigation, since evidence
vious wind tunnel experiments showing downwind movement of suggests vertical flights are more common in spring (Aubert and Xia
ACP (Croxton 2015, Martini et al. 2018) and with previous field 1990) when factors such as temperature, humidity, and flushing have
studies documenting ACP movement in the direction of prevailing been correlated with migration peaks between unmanaged and man-
winds (Kobori et al. 2011, Bayles et al. 2017, Johnston et al. 2019). aged citrus orchards (Zorzenon et al. 2021).
However, it was not possible to identify the effect of wind in the Results from this study highlight the importance of ACP dispersal
trapping investigation conducted in California due to the very low by wind and suggest wind information can be useful for predicting
overall numbers of ACP captured. It is likely that the very high wind ACP movement risk. Special attention to wind patterns should be
speed in California limits ACP ability to control their flight making paid in zones with a high risk of spillover of HLB or in areas where
the landing on a yellow sticky trap a random event. It is also pos- ACP can move from unmanaged to managed areas.
sible that differences in tree age and canopy size between trees in
CA and FL may have affected this outcome. ACP movement may be
affected by the availability of shelter and leaf flush for feeding and Supplementary Data
reproduction, and these resources will differ depending on tree size. Supplementary data are available at Environmental
The effects of shade and shelter provided by dense tree canopies on Entomology online.
spatial distribution and movement of ACP within citrus orchards
deserves further investigation.
The effect of wind speed on ACP dispersion is more difficult to Acknowledgments
interpret since it is speed-dependent and may cause varying out- We would like to thank Hunter Gosset, Angelique Hoyte, Tobias Moyneur,
comes over the course of an overall flight from source to destination. Timo Rohula, Rachel Youngblood, Jose Huerta for their technical assistance
For example, for settled ACP, our data suggest that low or moderate and Dr. Christopher Clark in the Department of Evolution, Ecology, and
wind speeds will discourage flight initiation and thus, limit dispersal. Organismal Biology at UC Riverside for allowing the use of the high-speed
However, if wind speeds are sufficiently strong to dislodge ACP from wind tunnel to generate the presented data.
the tree, passive dispersion will almost certainly occur. Very strong
winds (strong breeze and higher ≥48 km/h) at the canopy level are
Funding
common during certain months of the year in important citrus-pro-
ducing regions in the United States due to tropical storms and hurri- Funding for this work was provided by Citrus Research Board (5500-222)
awarded to M.J.R. and X.M.
canes in Florida or the Santa Ana winds in California. The effect of
Santa Ana winds on ACP dispersal has not been assessed under field
conditions but a mass movement of ACP has been reported after References Cited
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