Trail Chemicals of the Convergens Ladybird Beetle, Hippodamia convergens, Reduce Feeding and Oviposition by Diaphorina citri Hemiptera: ...
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J Insect Behav (2018) 31:298–308
https://doi.org/10.1007/s10905-018-9680-2
Trail Chemicals of the Convergens Ladybird Beetle,
Hippodamia convergens, Reduce Feeding and Oviposition
by Diaphorina citri (Hemiptera: Psyllidae)
on Citrus Plants
Meeja Seo 1 & Monique J. Rivera 1 &
Lukasz L. Stelinski 1
Revised: 11 April 2018 / Accepted: 11 April 2018 /
Published online: 17 April 2018
# Springer Science+Business Media, LLC, part of Springer Nature 2018
Abstract We investigated feeding and oviposition behavior of the Asian citrus
psyllid, Diaphorina citri, when exposed to the foraging trails of the convergens
ladybird beetle, Hippodamia convergens. Diaphorina citri females feeding on
citrus leaves directly exposed to the ladybird adults or treated with trail extract
excreted significantly less honeydew droplets than controls. The trail chemicals
of the ladybird beetle also decreased oviposition by D. citri females on citrus.
In a no-choice experiment, D. citri females preferred to oviposit on control
flush and plants than those with ladybird trail-extract treatments. In two-choice
experiments, 68.0% of D. citri released into cages exhibited strong selection
preference for settling and eventual oviposition on control plants than plants
treated with ladybird trail extract. Diaphorina citri eggs were found on all new
leaf flush of control plants, whereas only 29.5% of flush on treatment plants
were selected for oviposition. The trail chemical deposited by the convergens
ladybird beetle elicits repellency of D. citri feeding and oviposition. Therefore,
the trail chemicals my contain components that could be useful for behavior-
based management of D. citri and HLB disease by reducing psyllid feeding
and oviposition.
Keywords Hippodamia convergens . Coccinellidae . huanglongbing (HLB) . feeding
inhibition . oviposition inhibition . Diaphorini citri
* Lukasz L. Stelinski
stelinski@ufl.edu
1
Entomology and Nematology Department, Citrus Research and Education Center, University of
Florida, 700 Experiment Station Road, Lake Alfred, FL 33850, USAJ Insect Behav (2018) 31:298–308 299 Introduction Herbivores are able to detect and respond to the presence of natural enemies such as predators or parasitoids (Ninkovic et al. 2013). Detection of predators and parasitoids allows herbivores to avoid feeding or ovipositing in areas where there is evidence of enemy presence (Nakashima et al. 2004). Utilizing predator chemical trails to manage herbivorous insect pests may be a potentially new method to alter insect behavior for plant protection. Asian citrus psyllid, Diaphorina citri Kuwayama, is a herbivore that relies primarily on visual and olfactory cues for host plant selection (Patt and Sétamou 2010). Adult D. citri preferentially feed on the phloem and xylem of newly unfurled leaves (termed flush shoots) of rutaceous host plants (Patt and Sétamou 2010; Sétamou et al. 2016; George et al. 2017), which is also the only location for egg laying and nymph development (Grafton-Cardwell et al. 2013; Inoue et al. 2009; Pelz- Stelinski et al. 2010; Ammar et al. 2016). Diaphorina citri acquire and transmit the phloem-limited bacterium, Candidatus Liberibacter asiaticus (CLas), which is the presumed causal agent of citrus greening disease or huanglongbing (HLB) (Bové 2006; Gottwald 2010). Although both nymphs and adults can transmit CLas, nymphs that feed on infected citrus plants acquire it more frequently than adults and thus, most adults transmitting CLas to uninfected plants had acquired it as nymphs rather than in the adult stage (Inoue et al. 2009; Pelz-Stelinski et al. 2010). After acquisition, only five to seven hours of continuous feeding are needed to successfully transmit CLas (Roistacher 1991). Thus, repelling D. citri adult feeding and oviposition could reduce spread of HLB. Many predators of D. citri such as lacewings (Neuroptera: Chrysopidae), hoverflies (Syrphidae), and ladybird beetles (Coleoptera: Coccinellidae) have been identified in Florida citrus groves (Michaud 2001; Michaud and Olsen 2004). Among them, ladybird beetles are voracious predators of D. citri nymphs in citrus groves (Michaud 2004). Ladybird beetle larvae and adults are aggressive predators of hemipteran insects in general and they consume large numbers of prey during their development (Dixon et al. 1997). Ladybird beetles deposit chemical trails composed of alkanes and alkenes on plants during foraging (Hemptinne et al. 2001). The oviposition inhibitory effect of these ladybird trails on conspecifics was first reported in Adalia bipunctata (Hemptinne and Dixon 1991). Ladybird trail chemicals can be cues in enemy detection and these trails may also provide valuable information for prey species by indicat- ing presence of natural enemies (Swihart et al. 1991; Ferrero et al. 2001). These trails are also used for preventing egg cannibalism by conspecific larvae (Doumbia et al. 1998; Martini et al. 2013). Furthermore, trails of Coccinella septempunctata (Coleoptera: Coccinellidae) reduce aphid settling by 40~53% which affects aphid population development through disturbance and avoidance of the trails (Ninkovic et al. 2013). Ladybird beetle trails can also influence herbivore avoidance behavior in host plant or oviposition choice. The trails are also ecologically important reducing cannibalism and increasing survival rates of their offspring by causing avoidance of other conspecific and heterospecific individuals (Oliver et al. 2008). In our
300 J Insect Behav (2018) 31:298–308 previous study, Hippodamia convergens trails affected D. citri host plant selection by reducing settling on plants that had been exposed to ladybird trails. Trail chemicals deposited by ladybird beetles are mainly composed of long-carbon chain alkenes and alkanes dominated by methyl-branched and straight chain hydrocarbons (Hemptinne et al. 2001; Magro et al. 2007). These known trail components are nonvolatile which suggest that effects of ladybird trails on be- havior of D. citri are unlikely mediated by olfaction. Instead, our previous investigation suggests that the repellent effect of ladybird trails is mediated by nonvolatile, gustatory cues detected upon contact (Seo et al. 2018). Several management programs for HLB have been established such as intensive insecticide use, removal of HLB-infected citrus trees, and re-planting of disease- free nursery stock (Grafton-Cardwell et al. 2013). For D. citri management, insecticide use is expensive, harmful to beneficial insects, and unsustainable due to insecticide resistance (Hall et al. 2013; Tiwari et al. 2011). Behavior modifying chemicals for management of D. citri have also been investigated, but implemen- tation of an effective formulation is yet to occur (reviewed in Grafton-Cardwell et al. 2013). To explore the potential practical utility of ladybird beetle trail chemicals for D. citri management, we hypothesized that they may reduce feeding and/or oviposition behavior of this phytopathogen vector. The purpose of this investigation was to quantify the feeding and oviposition behavior of D. citri as influenced by trail chemicals deposited by H. convergens. Materials and Methods Experimental Insects and Plants Adult D. citri used in this study were collected from a laboratory culture maintained at the University of Florida, Citrus Research and Education Center (Lake Alfred, FL). This culture was established in 2000 from field populations in Polk County, FL (28.0’N, 81.9’W) before HLB was discovered in the state. This culture was maintained on Curry (Bergera koenigii) in an air-conditioned greenhouse (27 ± 1°C, 63 ± 2% RH, and L14:D10 photoperiod) without exposure to insecticides. Trails of H. convergens were used in this study. The beetles were purchased from Hirt’s Gardens Co. (Medina, Ohio, USA) and were reared on pea aphids, Acyrthosiphon pisum developing on faba broad pea plant, Vicia faba (Vermont Bean Seed Co., Randolph, WI, USA) in an incubator (25 ± 1°C, RH, 56 ± 5%, L14:D10 photoperiod). Approximately 12 month old ‘Swingle’ (Rutaceae: Swinglea glutinosa) citrus plants 20 cm in height were used in this study. The plants were pruned at least 2 weeks before bioassays to promote growth of new flush. Plants were maintained under the conditions described for insect rearing above. Establishing of H. convergens Trails on Citrus Plants Diaphorina citri were offered plants treated with ladybird beetle trails as whole plants and as leaf discs. Plants were exposed to the trails by two different methods.
J Insect Behav (2018) 31:298–308 301 The first was through direct exposure which was a period of beetle foraging and secondly, the trail was extracted and dissolved in solvent and then, applied to the plant or leaf disc as the treatment. These methods are explained below. Direct Exposure with H. convergens Adults Five H. covergens adults were caged for ten days within fine mesh bags per individual citrus plant consisting of several flush shoots to establish trails on leaf surfaces. During this period, released ladybird beetles were replaced daily to avoid death from starvation and to maintain a constant number of adult beetles foraging per individual plant. Directly before experiments with D. citri, all beetles were removed. Collection and Application of H. convergens Trail In order to collect H. convergens trail chemicals, ladybird adults were first starved for 24 h and each adult was then carefully inserted into a glass vial (15 mm diameter; 45 mm height) to prevent exposure to other contaminants including reflex blood, which could be released if beetles interacted. The glass vials were sealed with a Parafilm®, which was punctured with a minuten pin creating fine holes for air exchange. The tubes were kept in an incubator at constant temperature, light, and humidity (25 ± 1 °C. 60 ± 5%, L14:D10 photoperiod). Ladybird beetles were highly active when confined in tubes and trails were deposited as they continuously walked on the walls of the vials. After 24 h, beetles were removed and the vials were stored at −20°C until extraction. A total of 30 glass tubes were washed twice with 2 mL hexane (Sigma-Aldrich, HPLC grade). The same 2 mL of hexane was used to wash each of the 30 tubes to obtain a concentrated trail extract (Magro et al. 2007). After transferring between tubes, the 2 mL was placed into a new clean vial and then evaporated under a stream of nitrogen to further concentrate the sample for use in experiments. To apply ladybird beetle trail extracts onto plants, the residue was dissolved in 12 mL of hexane and 8 mL of acetone to obtain 20 mL of extract solution. All surfaces of each treatment plant were thoroughly covered with the 20 mL extract solution using an airbrush (H&HS-695, single action, External mix airbrush, Paasche Airbrush Co., IL, USA). The control plants were treated with 20 mL of 2 acetone: 3 hexane v/v solution. After treatment, all tested plants were dried under fume hood for 30 min. No phytotoxicity symptoms were observed on the citrus leaves during or after the appli- cation of the solution. Feeding Experiment Diaphorina citri were exposed to trails by two different methods. In the first method, the trail was deposited directly by a ladybird adult onto a 35 mm (diam) leaf disc for 24 h. After removing the ladybird beetle, leaf discs were used as a treatment in this experiment. Leaf discs that did not receive exposure to ladybird beetles served as the negative control. In the second exposure method, the ladybird trail extract (as obtained by the method described above) was applied in solvent onto 35 mm Valencia leaf discs by the airbrush
302 J Insect Behav (2018) 31:298–308
sprayer. The complimentary negative control consisted of treating leaves with solvent
(2 acetone: 3 hexane) alone. After the spray application, the leaf discs were dried in a
fume hood for 30 min and then, transferred to 35 mm Petri dishes with a layer of agar
lining the bottom to maintain moisture (Tiwari et al. 2011). Treatments were replicated
five times when applications were made by airbrush and three times when applications
were made by direct beetle foraging exposure. The entire experiment was repeated
three times on different dates.
We used the ninhydrin procedure to quantify honeydew excretion by psyllid
adults as an indirect measure of D. citri feeding (Boina et al. 2009; Tiwari et al.
2011). Three D. citri female were placed in each treatment and control dish when
evaluating D. citri feeding on leaves established by each method. Thereafter, each
Petri dish was closed with a lid lined with 35 mm filter paper (Whatman Interna-
tional Ltd., Maidstone, UK). The dishes were then placed upside down in an
incubator (25 ± 1°C, RH, 56 ± 5%, L14:D10 photoperiod) to collect excreted hon-
eydew droplets onto the filter paper as described in Boina et al. (2009). After 48 h,
filter papers were collected and submerged into 1% (w/v) ninhydrin (Sigma-
Aldrich, St Louis, MO) solution in acetone for three min. After removing, the filter
papers were placed on a paper towel and left to dry for at least 30 min. The number
of purple dots per filter paper was counted to quantify variation in honeydew
production (Tiwari et al. 2012).
Oviposition Experiments
No-Choice Experiment
The effect of the ladybird trails on D. citri oviposition was investigated using
adult psyllids 4–6 d post emergence. D. citri are reproductively mature at 4 d post
emergence and females typically begin laying eggs on the day of mating
(Wenniger and Hall 2007). Three pairs of male and female D. citri were released
onto each plant. Each plant was then covered with a translucent plastic cylinder
with a fine mesh screen side and lid. Adult psyllids were allowed to lay eggs. Five
days after release, all psyllids released were removed and the total number of eggs
per flush shoot per plant was counted using a steromicroscope. Direct leaf
exposure to beetles and exogenous extract application by airbrush treatments were
both applied to five individual plants. For each experiment, there were five
complementary negative control plants prepared as described above. These exper-
imental comparisons were repeated on three (direct exposure) and two (spray
application) different dates for a sum total of 15 and 10 plants per mode of
treatments and comparative controls, respectively. All experiments were conduct-
ed under controlled conditions (25 ± 2 °C, 50 ± 5% RH, L14:D10 photoperiod). .
Two-Choice Experiment
In oviposition choice tests, treatments and solvent controls were applied to plants
by airbrush as described previously. Both control and ladybird extract-treated
plants were placed approximately 25 cm apart within individual screen cagesJ Insect Behav (2018) 31:298–308 303 (55 × 42 × 38 cm). Thereafter, five pairs of D. citri were introduced into the center of cages between the two plants. Psyllids were four days post-emergence and all plants had 3 to 4 new leaf flush shoots. Five days after release, the number of psyllids that settled on each plant and number of eggs per unit of flush and whole plant were counted using a stereomicroscope. This choice experiment was repeat- ed five times (5 cages in total). All experiments were performed under controlled conditions (25 ± 2°C, 50 ± 5% RH, L14:D10 photoperiod). Statistical Analysis All analyses were conducted with SAS version 9.4 and data were checked for normality before analysis using PROC Univariate. Honeydew droplets data were pooled from 3 or 5 replicates by treatment. Mean number of droplets was compared among three treatments using a one-way analysis of variance (ANOVA) followed by Duncan test to determine differences among treatment means. For the no-choice oviposition experiment, the mean number of eggs laid per flush or plant among three treatments was compared using one-way ANOVA with a subsequent Duncan test for separation of means. The oviposition choice tests were assessed with paired t-tests. Results Effect of H. convergens Trail on D. citri Adult Feeding Fewer honeydew droplets were excreted by female D. citri feeding on leaves exposed to ladybird beetle adults or that were treated with an application of the trail extract compared with those feeding on the negative control (Fig. 1). However, there was no difference between the number of honeydew droplets excreted from psyllids feeding on leaves directly exposed to the beetles versus those that were sprayed with the trail extract (df = 2, 47; F = 36.42; p < .0001) (Fig. 1). Effect of H. convergens Trail on D. citri Oviposition The average number of eggs deposited by female D. citri per 5 days on plants or leaf flush treated with ladybird trails was significantly lower than that quantified in the negative controls (No. of eggs per flush: df = 2,63; F = 25.74; p < .0001; No. of eggs per plant: df = 2,27; F = 25.81; p < .0001; Fig. 2). There was no overall difference in the number of eggs laid per plant or flush by D. citri on plants that received direct exposure to adult beetles versus the exogenous extract spray treatment (Fig. 2). However, significantly more eggs were laid on control plants than either of the two ladybird beetle trails treatments (Fig. 2). In two-choice experiments, 100% of leaf flushes were infested with D. citri eggs on control plants; whereas, only 29.5% flush contained eggs on extract- treated plants (t = 3.78, df = 4, p = 0.0195). Also, the majority (68.0%) of D. citri released into cages settled on control plants as compared with those treated with
304 J Insect Behav (2018) 31:298–308
30
No. honeydew droplet per fliter disc 25 a
20
15
b b
10
5
0
control Direct exposure Extract
Fig. 1 Effect of adult ladybird beetle, Hippodamia convergens, trail constituents on Diaphorina citri feeding
on citrus leaf discs as measured by number of honeydew excretion. Control leaf discs were treated with solvent
solution. Direct exposure was achieved by allowing ladybird adult to forage on leaf discs for 24 h prior to
assays
ladybird beetle extract (t = 3.09, df = 4, p = 0.0184). Both the mean number of eggs
counted per flush and per plant was significantly lower on plants treated with
ladybird beetle extract than on negative control plants (Fig. 3).
Discussion
Ladybird beetle trails reduced feeding by D. citri adults on citrus foliage, as
indirectly measured by honeydew excretion. This effect occurred both when trails
were directly deposited by foraging ladybird beetles and when previously collect-
ed extract of the trails were re-applied to citrus leaves via exogenous spray.
Fig. 2 Comparison of Diaphorina citri oviposition on plants directly exposed to ladybird adult foraging or
trail extract in no-choice experiments. One-way ANOVA, number of eggs per flush: df = 2,63; F = 25.74;
p < .0001; number of eggs per plant: df = 2,27; F = 25.81; p < .0001)J Insect Behav (2018) 31:298–308 305 Fig. 3 Comparison of Diaphorina citri oviposition on citrus plants treated with ladybird adults trail extract in choice experiments as compared with untreated control. Paired t-test with SAS. (No. of eggs per flush: df = 19; t = 12.60; p < .0001; No. of eggs per plant: df = 4; F = 8.99 p = 0.0004). *** P < 0.001 Similar feeding reduction, as measured by honeydew excretion, has been reported for the aphids Myzus persicae and Myzus nicotianae when exposed to a sublethal concentration of the synthetic insecticide, imidacloprid, on plant tissue (Nauen 1995; Nauen and Elbert 1997). Upon release onto leaf discs treated with ladybird trails, D. citri adults spent most of their time searching for an adequate feeding location. Therefore, they were not able to feed normally and their honeydew excretion was consequently decreased. The amount of honeydew excreted by D. citri was not different between the two modes of treatment. This suggests that the amount of extract re-applied following in our manipulative experiment was comparable in effect to that deposited by actual foraging ladybird beetle adults. D. citri females exclusively oviposit on newly flushing and unexpanded citrus leaves because those are the only sites where early instar nymphs of this species can feed and develop (Inoue et al. 2009; Pelz-Stelinski et al. 2010). Both D. citri nymphs and adults can transmit CLas in a persistent and propagative manner (Ammar et al. 2016). However, nymphs are more efficient in acquiring CLas from infected citrus plants than adults (Inoue et al. 2009; Pelz-Stelinski et al. 2010). Therefore, deterring both settling and oviposition on citrus flush by adult D. ctri should promote the reduction of HLB spread. Hippodamia. convergens trails reduce D. citri settling behavior (Seo et al. 2018). However, D. citri adults are highly mobile and move frequently between and within plants during selection of feeding, resting, mating, and oviposition sites (Boina et al. 2009). Selection of flush shoots for oviposition by D. citri is a critical step for survival and fitness of their progeny (Wenninger et al. 2009; Martini et al. 2014). Therefore, we inves- tigated the effects of ladybird trails on D. citri oviposition behavior. Our current results demonstrate that ladybird beetle trails reduced D. citri oviposition on trail-marked plants. Although D. citri reproduced on citrus flush treated with ladybird beetle trail extract under no-choice test conditions, adults preferentially selected control plants for oviposition and avoided extract-treated plants in choice tests. In a similar no-choice assay investigating suitability of
306 J Insect Behav (2018) 31:298–308 native North American Rutaceae as host plants, D. citri also laid eggs on flush of non-host plants that were unable to support immature development (Sétamou et al. 2016). Collectively, these results indicate that D. citri females will deposit eggs on sub-optimal locations that may strongly reduce fitness when no other resource is available. Therefore, an eventual practical application of this ladybird beetle trail pheromone as a psyllid anti-feedant or anti-oviposition treatment may require concurrent establishment of a suitable trap crop location where female D. citri would be given the opportunity to lay eggs that could be removed from the population with additional insecticide. Interestingly, plant flush treated with ladybird beetle trail extract received no eggs in our choice experiment even though those plants were likely initially visited by D. citri during the course of the experiments (Seo et al. 2018). Similarly, the larval tracks of Adalia bipunctata L. (Coleoptera: Coccinellidae) deter oviposition of conspecifics, as well as, the heterospecific, Coccinella septempunctata L., even though they do not completely deter foraging (Martini et al. 2013; Doumbia et al. 1998). Here, we only investigated the trail of one ladybird beetle species, but it is possible that the trail composition of multiple ladybird beetle species foraging on trees could further affect psyllid behavior or similarly, that quantitative variations by individual species could impact behavior differentially (Wheeler et al. 2015). Furthermore, it would be worthwhile to investigate additive effects in field applications or further laboratory study of trail chemicals. For example, in addition to deterrence, the application of trail chemicals or its components could promote an increase in ladybird foraging behavior (Wheeler and Cardé 2014). In that case, trail chemicals would further assist in protecting the sensitive flush shoots of citrus plants by directing the foraging behavior of these highly generalist predators. D. citri relies primarily on vision and olfaction for detecting and orienting to host plants (Patt and Sétamou 2010; Patt et al. 2011). Furthermore, host selection by D. citri for feeding and oviposition can depend on variation among volatile profiles of related host plants (Wenninger et al. 2009; Martini et al. 2014). The chemicals deposited by coccinellid adults and larvae are mainly comprised of long carbon chain alkenes and alkanes dominated by methyl branched and straight chain hydrocarbons (Hemptinne et al. 2001; Magro et al. 2007). Due to non-volatile properties of these molecules, long distance repellency as a mechanism of affecting D. citri behavior is unlikely to occur in the field but it is possible there are some unidentified volatile components of the trails that may be serving as a cue in arenas larger than our laboratory study (Wheeler and Cardé 2013). However, these alkanes can be readily deposited onto hydrophobic surfaces of plants with long-lasting residual activity expected, because they are resistant to oxidation (Crabtree 1985). Generally, D. citri adults must feed for at least thirty minutes continuously to acquire the CLas and they require 5–7 h of subsequent feeding on an uninfected plant for transmission (Roistacher 1991). Therefore, feeding deterrence of disease vectors such as D. citri may function as an effective method for reducing spread of insect-borne disease due to unsuccessful acquisition and/or transmission of the causal phytopathogen (Mowry and Ophus 2002). Our results support potential practical application of ladybird beetle trails constituents as an anti-oviposition agent for managing D. citri, specifically on new flush growth in citrus groves.
J Insect Behav (2018) 31:298–308 307
Acknowledgments We thank Wendy L. Meyer, Angelique B. Hoyte, Kristin A. Racine, and Hunter
Gossett for technical support. We really appreciate Timothy A. Ebert for giving the pea aphid for
rearing ladybird beetles. This project was supported by the Citrus Research and Development Foun-
dation grant number 15-024.
Compliance with Ethical Standards
Conflict of Interest The authors declare that they have no conflict of interest.
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