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Article

Manipulation of Phototactic Responses by Two-Spotted Spider Mites to Improve Performance of Miticides

by
Christian Nansen
1,*,
Patrice Jacob Savi
1,
Tora Ward
1,
Haleh Khodaverdi
1,
Johann Heinrich Lieth
2 and
Anil V. Mantri
1
1
Department of Entomology and Nematology, University of California, Davis, CA 95616, USA
2
Department of Plant Sciences, University of California, Davis, CA 95616, USA
*
Author to whom correspondence should be addressed.
Crops 2024, 4(4), 568-583; https://doi.org/10.3390/crops4040040
Submission received: 25 July 2024 / Revised: 3 November 2024 / Accepted: 7 November 2024 / Published: 8 November 2024
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Abstract

Insight into phototactic responses by herbivorous crop pests may be used to manipulate their vertical distribution in crop canopies. Here, we tested the hypothesis that the deployment of specific light sources elicits positive or negative phototactic responses and can be used to enhance performance of miticide applications. We characterized movement responses by two-spotted spider mites (Tetranychus urticae) (spider mites) to seven light sources [ambient (control), UV-C, UV-B, blue, red, white, and near-infrared (NIR)] under experimental conditions. Separate experiments were conducted with/without the presence of a shelter. An analytical approach based on linear regression coefficients (intercept and slope) from observations in ascending order was used. Linear regression coefficients from UV-B indicated significantly negative phototactic bio-response. We examined settlement of spider mites when exposed to 11 light source configurations and with adaxial leaf sides facing either upwards or downwards. This experiment revealed strong positive and negative phototactic bio-responses to blue light and UV-B light, respectively. As a validation experiment, soybean plants were experimentally infested with spider mites and subjected to one of the following three treatments: (1) no treatment (control), (2) miticide [pyrethrins and Beauveria bassiana (BotaniGard Maxx)] only, and (3) a combination of blue and UV-B for 10 min immediately prior to miticide application. Integration of miticide application with prior deployment of blue and UV-B lights significantly increased the performance of miticide application. Results from this study supported the hypothesis. As a pest management approach, the integration of blue light (to elicit positive phototactic response) and UV-B (to elicit negative phototactic response) is believed to be of particular relevance to organic crop producers and/or to producers of crops for which limited numbers of miticides are registered.

1. Introduction

Phototactic responses (phototaxis) have been described in scientific literature for more than 102 years [1], and has been observed and described in multiple biological kingdoms: Bacteria [2,3,4,5,6], Plantae [3,5,7,8,9], and Animalia [3,10,11,12,13,14,15,16]. Jékely [3] provided a basic definition of phototactic responses as a positive or negative behavioral displacement along a light gradient or vector. This definition implies that phototactic responses are a non-random, directional locomotive response of motile organisms in the presence of a specific light stimulus. Such light-inducing stimuli may be characterized by specific wavelength ranges, intensity, and duration within the electromagnetic spectrum. As a general academic research topic, phototactic responses are of paramount importance as part of understanding ecological and environmental adaptations of motile species [17,18,19,20] and of the physiology of light perception by animals [3,12,21]. Positive phototactic responses have been widely observed across insect orders with most sensitivity at UV (350–390 nm), blue (400–470 nm), and green (505–575 nm) light wavelength ranges of the electromagnetic spectrum [10]. Positive phototactic responses have also been observed across the Arachnid orders of Ixodida at UV (380 nm), blue (480 nm), and green-blue (500 nm) wavelengths [22] and Trombidiformes at white, green-yellow (560 nm), and yellow-orange (600 nm) wavelengths [23,24].
Phototactic responses have considerable potential as an avenue to develop novel and highly innovative approaches to the management of arthropod pests in agricultural cropping systems [10,25,26,27,28]. Crop production in controlled environments often relies on supplementary lighting to maximize crop productivity [27,29,30,31,32]. Light traps are already being used in controlled environments for the monitoring of arthropod pests [25,28]. Furthermore, with increasing adoption of light emitting diode (LED) technologies within controlled environment crop production systems [33], use of artificial lighting for the purpose of arthropod pest management has become more accessible. LEDs are more power efficient and have a longer lifetime compared to traditional incandescent and fluorescent lamps [33,34]. In addition, LEDs are characterized by having a high luminous flux and low radiant heat and can be manufactured to have narrow peak wavelengths [33]. This could allow for use of higher light intensities in pest management applications as LEDs can be placed closer to plants without inducing heat stress to elicit desired phototactic responses [33]. In controlled environment crop production systems with artificial lighting, phototactic responses may be elicited to manipulate arthropod pest populations in ways that aggregate their distribution in top-portions of crop canopies, so that they become more exposed to contact pesticide applications.
Spider mites [Tetranychus urticae Koch (Acari: Tetranychidae)] (here, referred to as “spider mites”) are a serious and challenging pest in a wide range of agricultural systems [35,36,37], including controlled environment production systems [36]. Spider mites have an estimated host range of 800 species of plants, many of which hold high agricultural value [35]. Successful management is hampered by spider mites’ ability to develop resistances to a diverse array of miticides, with known resistances to 96 unique active ingredients [38]. Another complicating factor regarding effective management of spider mites is their high preference for lower (abaxial) leaf surfaces [39,40,41,42]. In an apple orchard, Osakabe [39] recorded ~99% of female individuals located on the abaxial side of leaves. Additionally, spider mites tend to be most prevalent in lower portions of crop canopies [43,44,45]. This non-random vertical distribution within crop canopies adversely affects the performance of contact-miticides, as it is challenging to obtain high and consistent spray coverage on the abaxial sides of leaves in lower portions of crop canopies [46,47,48]. Furthermore, as spider mites feed on individual leaf tissue cells (not vascular feeders), they have shown limited susceptibility to some systemic miticides, including neonicotenoids (acetamiprid, thiacloprid, imidacloprid) and diamides (chlorantraniliprole, cyantraniliprole, flubendiamide) [49].
Spider mites have shown positive phototactic responses to wavelengths of light between 375 and 575 nm with varying peaks of sensitivity [15]. In non-diapausing females, spider mites have been shown to be attracted to white, blue (466 nm), green (536 nm), and red (653 nm) light [17]. Regarding spider mites, light detection occurs through a pair of ocelli that are composed of external lenses with a biconvex anterior part and a simple convex part, each with five and twelve rhabdomeres, respectively, which make up the photoreceptors of the eye [50]. Naegele et al. [15] and Goto [51] have found that the photoreceptors in ocelli of spider mites show spectral sensitivity to wavelengths from 350 to 700 nm. These studies reported specific peak light sensitivity in the near UV (375 nm) and green light (525 nm) portions of the electromagnetic spectrum. Additionally, phototactic responses by spider mites to far red light (660 nm) has also been reported [52]. To complicate matters, it has been shown that exposure to far red light may alter phototactic responses by spider mites to near UV and green light [52]. Thus, there are potential interactions among light stimuli, and it seems possible that spider mites respond to light spectra, which are not being detected by photoreceptors in their eyes.
In laboratory experiments, spider mite individuals were manipulated from the abaxial to the adaxial sides of leaves when lower leaf surfaces were exposed to reflected UV light [39]. Under controlled experimental conditions, Suzuki et al. [53] demonstrated that sustained exposure of spider mites to UV-C (250 nm) triggered negative phototactic responses by non-diapausing females during a three day period. Furthermore, a similar negative phototactic response occurred sooner and was more pronounced when spider mites were exposed to sustained UV-A (350 nm), UV-B (300 nm), and UV-C (250 nm).
The following are the illustration of experiments included in this study (Figure 1): (1) video tracking of spider mite individuals in experimental arenas with/without the presence of a shelter and when exposed to one of several light sources [UV-C, UV-B, blue, red, white, near-infrared (NIR), and ambient (control)]. (2) Spider mites on individual lima bean (Phaseolus lunatus L.) leaves with either adaxial or abaxial leaf sides facing upwards and with combinations of light sources projected onto both leaf sides. (3) Whole soybean (Glycine max L.) plants experimentally infested with spider mites and subjected to one of three treatments: (1) Control (deionized water only), (2) Spray (miticide only), and (3) Light + Spray (deployment of blue and UV-B light sources for 10 min immediately prior to miticide application). Accordingly, experiments in this study were performed to examine the hypothesis that the deployment of specific light sources elicit positive or negative phototactic responses and can be used to enhance the performance of miticide applications. Results from this study provide strong support for claims that specific light sources elicit positive and negative phototactic response, similar to “push-pull trap cropping” [54]. Furthermore, results from this study support the notion of integrated pest management, in which specific light sources are used to boost performance of organically certified miticides.

2. Materials and Methods

2.1. Spider Mite Colony

Spider mites used in this study were obtained from a continuous colony reared on soybean plants inside insect cages (160 µm mesh, www.bugdorm.com, accessed on 24 July 2024) in controlled greenhouse facilities (25.2 ± 1 °C, 77 ± 10% RH, and a L:D 12:12 photoperiod) at the University of California, Davis, CA, USA. This colony has been maintained under ambient light conditions for more than five years on different bean species and strawberry varieties. Spider mites were not subjected to any forms of pest control (natural enemies and/or pesticides). When contaminations by other arthropods were detected, then adult spider mite females were carefully transferred to new/clean plants, so that the colony could be continued. The age and mating status of adult spider mite females in the experiments were unknown.

2.2. Plant Materials

Lima bean (Phaseolus lunatus L.) (https://www.threshseed.com/) (accessed on 24 July 2024) and organic soybean (www.gorlion.com) (accessed on 24 July 2024) plants were grown in a different greenhouse from that hosting the spider mite colony but under the same environmental conditions. Bean seeds were planted in 1.0 L pots, which were filled to 80% capacity with a homogeneous mixture of pumice, sphagnum peat moss, sand, redwood sawdust, and dolomite at a ratio of 5.23 kg per m3 of soil mix autoclaved at 121 °C for 1 h. Pots were watered and fertilized four times a day (7 am, 10 am, 2 pm, and 5 pm) using an automated sprinkling irrigation system with a Dema Mix Rite injector (Model 2502) (https://ag.demaeng.com, accessed on 24 July 2024). Fertilizer element composition (values in ppm) was as follows: N = 150, P = 50, K = 200, Ca = 175, Mg = 55, S = 120, Fe = 2.5, Cu = 0.02, B = 0.5, Mn = 0.5, Mo = 0.01, and Zn = 0.05.

2.3. Light Sources

We included seven narrow-wavelength light sources with the following specifications: (1) ambient light (control), (2) white LED (λmax = 451 nm; irradiance at 5 in. = 1.24 mW/cm2), (3) blue LED (λmax = 462 nm; irradiance at 5 in. = 1.26 mW/cm2), (4) red LED (λmax = 667 nm; irradiance at 5 in. = 0.824 mW/cm2), (5) near-infrared (NIR) LED (λmax = 741 nm; irradiance at 5 in. = 0.902 mW/cm2), (6) UV-B lamp (λmax = 437 nm and 546 nm; irradiance at 5 in. = 1.30 mW/cm2), and (7) UV-C lamp (λmax = 254 nm, 437 nm, and 547 nm; irradiance at 5 in. = 1.75 mW/cm2). Emission spectra from experimental light sources were characterized and quantified with a fiber optics UV/vis spectrometer (Ocean Optics S2000). Irradiance values (mW/cm2) were obtained as a function of lamp distance with a handheld photometer (International Light Technologies, IL-1400) using either a Multi-Junction Thermopile (SED623) with Quartz Window (200–4200 nm) for the LEDs or a SiC detector (SED (SEL) 270/QT) with Teflon/quartz diffuser (200–380 nm) for the UV light sources. Measured irradiance values were corrected using the sensitivity factor of each detector. All light sources were mounted on a fixed structure, so that the distance between light sources and objects was constant.

2.4. Video Tracking and Analytical Approach

Movement of individual spider mites was recorded during 3 min at a rate of 15 observations per second, with a video camera (Computar Mega-Pixel Vari Focal, H2Z0414C) and accompanying tracking software (EthoVision XT® software (Version 11.5, Noldus Information Technology Inc., Leesburg, VA, USA). Individual spider mites were placed inside an experimental arena consisting of 9 cm diameter filter papers with adhesive tape with sticky side facing upwards as outer boundary. Experimental light sources were mounted as two parallel light sources 20 cm above a light table with experimental arenas. Due to the light table, spider mite individuals appeared dark and were easily detectable with video tracking software. The order of bioassays with different experimental light sources was randomized. Proper personal protection equipment (long sleeves, gloves, UV protective goggles) was worn to protect against harmful UV light during those respective bioassays. In an additional experiment, a shelter was added to the arena center. Shelters consisted of a 2.5 cm by 2.5 cm box with open sides, so that spider mite individuals could move freely in and out of shelter. Shelters were made of overhead transparencies to allow video tracking but protecting spider mites from UV radiation. Overhead transparencies are made from polyester film (PET or polyethylene terephthalate). PET possesses a chromophore group that absorbs UV radiation in wavelengths from 250 to 310 nm, and also considerable absorption in wavelengths from 310 to 370 nm [55]. Thus, overhead projectors were considered highly suitable as material to protect from high intensity wavelengths and simultaneously allow for video tracking. Without shelter, a total of 15 replicated bioassays were performed for each of the 7 experimental light sources. With shelter, a total of 20 replicated bioassays were performed for each of the 7 experimental light sources. For each combination of light source and presence/absence of shelter, different spider mites were used in bioassays (individual spider mites were only bioassayed once).
Under experimental settings, average behavioral responses by spider mites, and other animals, are often associated with considerable stochastic variation [17,56,57], which adversely influences abilities to demonstrate significant treatment effects. One possible explanation for such outcomes is that it is assumed that only high or low bio-responses are assumed to occur in response to a given treatment. That is, it may be assumed that only increased movement is a likely response to exposure to unsuitable conditions as an attempt to avoid danger and escape. However, there may be experimental scenarios in which both low and high bio-responses may be likely outcomes. As an example with relevance to this study, spider mite individuals exposed to a non-suitable light source may be expected to either have significantly increased movement (attempt to avoid) or significantly less movement (avoid exposure by protecting their body in an immobile posture). If so, and as discussed in a recent study [58], behavioral responses, such as movement, may be analyzed statistically based on alignment of individual observations in ascending order and subsequently examine regression coefficients (intercept and slope) as indicators of bio-response. This analytical approach is illustrated in Figure 2. Moreover, total movement results from 15 replications under ambient light (control) were ranked in ascending order and ranged from 2.81 to 26.98 cm (average = 12.47 ± 2.08 s.e.). Due to this considerable range, traditional means comparisons will often fail to show significant treatment effects.
In the example presented in Figure 2, movement results obtained under ambient light produced a highly significant linear regression with slope = 1.69 and intercept = 1.02. Regression coefficients were generated for each of the seven light sources, and statistical analyses of regression coefficients were used to examine treatment effects. Based on this analytical approach, a low (possibly negative) intercept is an considered indicator of generally low bio-response to the given treatment. A shallow slope is also considered an indicator of a generally low bio-response to the given treatment.

2.5. Phototactice Responses on Leaves

This experiment represented a logic continuation of video tracking on filter paper, as it provided quantitative insight into phototactic responses when spider mites were on actual crop leaves. Moreover, phototactic bio-response by spider mites to experimental light sources projected onto both abaxial and adaxial surfaces were characterized using individual leaves from lima bean plants. Bioassays were conducted in a darkened greenhouse at consistent conditions of 20–22 °C and 75 ± 10% RH. Leaves with petiole in cotton wool inserted into microcentrifuge tubes with water were placed on two lines of string and infested with five spider mite individuals. After 10 min acclimation, experimental light sources were applied for 10 min. We included four light sources: no light (control as experiment was conducted in a dark greenhouse), UV-B, blue, and near-infrared (NIR). Specifications on light treatments are described above. These light sources were either projected downwards or upwards onto leaf sides in a total of 11 light source configurations. All 11 light source configurations were tested with bean leaves placed with adaxial leaf sides facing either upwards or downwards. After 10 min, the numbers of spider mites settled on adaxial and abaxial sides of each leaf were counted. Spider mite bio-responses to all combinations of light source configurations and adaxial leaf side upwards or downwards were repeated 30 times.

2.6. Validation of Light Source Combination with Miticide Application

Key results from experimental exposures to light sources were integrated into a miticide application with the purpose of determining whether a 10 min light source would enhance the performance of miticide application. More specifically, we included a light source combination that elicited positive (blue light) and negative (UV-B) phototactic responses to manipulate spider mite individuals towards upper canopy portions immediately prior to miticide application. As miticide, we used a commercial combination of pyrethrins and Beauveria bassiana (BotaniGard Maxx®, Certis, L.L.C., Columbia, SC, USA). Thirty 30-day-old soybean plants were maintained in individual insect cages (160 µm mesh, www.bugdorm.com) inside controlled greenhouse facilities (25.2 ± 1 °C, 77 ± 10% RH, and a L:D 12:12 photoperiod). Each soybean plant was trimmed to two leaves and subsequently infested with 60 adult spider mite females. After infestation, soybean plants were randomly separated into three treatment groups: deionized water (negative control), miticide only (positive control), and light source exposure (UV-B light projected upwards onto soybean plants and blue light projected downwards onto soybean plants for 10 min immediately prior to miticide application) and miticide. Plants were sprayed with a backpack sprayer (Dramm BP-4 backpack sprayer, www.dramm.com) after being taken out of insect cages and placed in separated treatment groups. One day after infestation, miticide and deionized water were applied using a back sprayer until runoff stage. Five days after applications, all leaves of each plant were collected to count spider mite mobiles (larvae, nymphs—pooling protonymphs and deutonymphs—and adults) and eggs under a stereomicroscope.

2.7. Statistical Analyses

Data processing and statistical analyses were performed using R v3.6.1 (The R Foundation for Statistical Computing, Vienna, Austria). For the results from movement experiments with/without presence of shelter inside arenas, we used a z-test [library BSDA, Equation (1)] to perform pairwise statistical comparisons of regression coefficients as follows:
z = x 1 − x 2 s q r t S E x 1 2 + S E x 2 2  
in which “x1” and “x2” represent two linear regression coefficients to be compared (slope or intercept), and “SEx1” and “SEx2” represent standard errors associated with the two linear regression coefficients, respectively. Z-table values are available online, and critical z-values were approximately as follows: z = 1.6 (p < 0.05); z = 2.4 (p < 0.01); and z = 3.1 (p < 0.001). Results from ambient light source were compared with results from the other six light sources [UV-C, UV-B, blue, red, white, near-infrared (NIR)].
Wilcoxon signed-rank test (library MASS) was used to compare percentages of adult spider mites on leaf sides exposed to light source configurations. Analysis of variance (library multcomp) was used to compare means of mobiles and eggs per plants five days after infestation and after being subjected to either deionized water, miticide only, or light source exposure combined with miticide application.

3. Results

3.1. Phototactic Response in Experimental Arena Without and With Shelter

In experimental research, it is important to develop highly repeatable, quantitative, and cost-effective methods and experimental designs. Furthermore, when responses to a large number of treatments are examined, and when high numbers of replications are conducted, it becomes a priority to develop a methodology that is executable in a timely manner. It was within this context that the phototactic bio-responses by spider mite individuals were recorded inside filter paper arenas with/without the presence of a shelter.
Figure 3 shows linear regressions and Table 1 includes basic metrics from the movement experiment to characterize bio-responses to light sources in arenas without a shelter. Across all light sources, minimum and maximum movement by individual spider mites varied between 0.40 and 33.00 cm, which is about 82-fold. The average movement per light sources varied from 11 to 17 cm, and averages were associated with considerable standard errors. Thus, conventional means comparison (analysis of variance) could not detect significant treatment effects (p-values > 0.05). After ascended ranking of observations obtained with each light source, highly significant linear regression fits were obtained with adjusted R2-values ranging from 0.77 to 0.96.
As seen in Figure 3, linear regression fit to bio-response to UV-B was characterized by a comparatively low (highly negative) intercept and steep slope. Accordingly, both regression coefficients were significantly different from those derived from linear regression fit to ambient light. Pairwise comparisons of regression coefficients also revealed significant bio-responses (compared to ambient light) to red and near-infrared light sources. It was considered noteworthy that the lowest coefficients of determination (adjusted R2-values) were observed for white and ambient light sources (Table 1). This could be interpreted as these light sources having the least effect on spider mite movement.
In the experiment with a shelter present in the arena center, we performed a similar analysis to that of movement bio-response, but we instead ranked percentage of time spent inside shelter (Figure 4 and Table 2). Across all light sources, minimum and maximum percentage of time spent in shelter by individual spider mites varied between 0.00 and 100.00%, and treatment averages varied from 33 to 66%. After ascended ranking of observations obtained with each light source, highly significant linear regression fits were obtained with adjusted R2-values ranging from 0.92 to 0.97.
Figure 4 shows that most of the seven light sources generated intercepts <0 and highest percentages near 80%. These results suggest that spider mite individuals spent little time under shelters. However, Figure 4 also showed that UV-B and UV-C were both associated with intercepts near 20% and highest percentages near 100%. Thus, UV-B and UV-C light sources elicited bio-responses that suggested avoidance by spider mites spending more time inside shelter. Accordingly, regression intercepts for UV-B and UV-C were significantly different from that of the ambient light source. The regression intercept for NIR was also significantly different from that of the ambient light source. Regarding regression slopes with the presence of a shelter, significant effects (difference from ambient light source) were observed for NIR and UV-B light sources. Although not statistically significant, bio-response to blue light was noticeable, as both regression fits were numerically lower than those derived from the ambient light source. This result was interpreted as spider mite individuals potentially showing a positive phototactic response (attraction) to blue light.

3.2. Phototactice Responses on Leaves

Based on the results from movement experiments with/without the presence of shelter in the arenas (Figure 3 and Figure 4, and Table 1 and Table 2), we selected four of the seven light sources [no light (control), blue, NIR, and UV-B] for further investigation in an experiment with soybean leaves, placed with adaxial leaf side facing either upwards (Figure 5a) or downwards (Figure 5b). While the adaxial leaf side facing downwards has no relevance to commercial settings, it served as an important reference in the assessments of relative ability of light sources to elicit positive or negative phototactic bio-responses. With the adaxial leaf sides facing upwards (natural position), 7 of the 11 light source configurations did not elicit significant treatment effects (p > 0.05). However, there was a numerical preference for abaxial leaf sides under most of the examined light configuration sources. This result supports the generally accepted notion of spider mites showing preference for abaxial leaf sides [39,40,41,42]. Among the four light source configurations eliciting significant treatment effects, there were noticeable trends with blue light eliciting positive and UV-B eliciting negative phototactic bio-responses, respectively. In the experiment with the adaxial leaf side facing downwards, we observed a significant preference for top side (abaxial leaf side) in 5 of the 11 light source configurations (Figure 5b), which supports the claim of spider mites preferring abaxial leaf sides. However, it was noticeable that light configurations with NIR and blue light elicited the same phototactic bio-response, irrespectively of whether the adaxial lead side was facing upwards or downwards. Meaning, this light configuration was considered highly “robust” and able to significantly manipulate spider mite distribution in crop canopies. Similarly, but more pronounced, the light source combination of blue light from the top and UV-B light from the bottom manipulated about 80% of adult spider mites to leaf sides facing towards blue light, irrespectively of whether the adaxial leaf side was facing upwards or downwards.

3.3. Validation of Light Source with Miticide Application

Due to the significant and highly robust manipulation of adult spider mites on soybean leaves (Figure 5), we performed a validation experiment in which a miticide was applied after 10 min exposure to the light configuration of blue light from the top and UV-B light from the bottom. Both the numbers of live mobile spider mites and live spider mite eggs were significantly reduced (Figure 6). Moreover, the addition of the proposed light source caused a two-fold performance increase to suppression of spider mite mobiles.

4. Discussion

In this study, we examined the hypothesis that light sources elicit positive or negative phototactic responses and can be used to enhance performance of miticide applications. The analyses of movement responses were based on an approach, in which regression coefficients derived from light sources were used as indicators and compared statistically with those derived from control conditions (ambient light). Moreover, a low (possibly negative) intercept and shallow slope were considered indicators of low bio-response to the given treatment. In the experiments both with and without the presence of a shelter, we demonstrated significant movement bio-responses to UV-B and NIR light sources, and results were interpreted as denoting negative phototactic responses. Although not statistically significantly, we also observed a numerically positive response to blue light. Thus, these light sources were selected for further analyses. Using soybean leaves placed with the adaxial leaf side facing either upwards or downwards, highlighted significant positive and negative phototactic responses to blue and UV-B light sources, respectively. These findings supported our study hypothesis that the deployment of specific light sources elicits positive or negative phototactic responses and can be used to enhance the performance of miticide applications. Moreover, the experimental results with spider mites on individual leaves were validated based on an experiment with whole bean plants and application of miticide either alone or in combination with pre-exposure to a light configuration of blue light projected downwards and UV-B light projected upwards immediately before miticide application. This validation experiment confirmed that the performance of miticides may be significantly improved by being integrated with the use of blue and UV-B light to manipulate spider mites upwards into crop canopies.

4.1. Movement and Phototactic Responses

Non-random phototactic responses are not surprising, as animals, including spider mites, rely on specific light cues to optimize orientation and successful identification of food, mates, oviposition sites, refuges, and suitable habitats [26,59]. Negative phototactic responses to UV-C is likely explained by such light sources being harmful to many organisms and leading to avoidance behavior [53,60]. For instance, UV-C elicited a significant decrease in spider mite egg hatch on strawberry (Fragaria × ananassa) cultivars [61] and common bean plants [62]. Naegele et al. [15] and Goto [51] reported peak light sensitivity by spider mites to UV-A (375 nm) and green light (525 nm). Of particular importance to the current study, Suzuki, Kojima [17] reported consistent negative phototactic responses by spider mites to UV-B (peak at 307 nm) and UV-A (peak at 370 nm) radiation in both non-diapausing and diapausing spider mite individuals. Additionally, other studies suggest that UV-B light sources may effectively suppress spider mite eggs, larvae, and nymphs [63].

4.2. Phototactice Responses by Spider Mites on Crop Leaves

Wavelength-specific behaviors are driven by photoreceptors with varying sensitivities, which can independently trigger and/or inhibit specific phototactic responses [64]. Romero and Benson [65] reported that spider mites tend to predominantly inhabit the abaxial sides of leaves due to a favorable microenvironment characterized by higher humidity, cooler temperatures, and protection from desiccation and predators. Similarly, Suzuki, Kojima [17] explored the effects of light direction on spider mite distribution and found that spider mite preference for the abaxial leaf sides under natural conditions is a strategy to avoid harmful effects of UV-B radiation from the adaxial surface. Furthermore, Tsolakis, Ragusa [66] found that leaf side preference by spider mites is influenced more by leaf morphology than by light wavelengths. This indicates that the abaxial surface, with its unique structural characteristics, is inherently more attractive to spider mites. However, ambient light under controlled conditions may have lower levels of UV-B radiation, which typically drives spider mites to avoid the adaxial surface in favor of the abaxial surface. This could explain the non-preference for either the abaxial or adaxial surface when abaxial leaf sides faced downwards.
Under experimental greenhouse settings, Stukenberg, Pietruska [60] found that a trichromatic photoreceptor setup involving blue, green, and UV-B lights significantly reduced positive phototactic responses by western flower thrips (Frankliniella occidentalis), which was initially observed under single-wavelength exposures. Athanasiadou and Meyhöfer [67] reported that a combination of blue and UV-B caused a significant avoidance by greenhouse whiteflies (Trialeurodes vaporariorum) of tomato plants compared to the use of monochromatic blue or UV-B. Results from this study provide additional insights into the complementary and highly synergistic benefits of combining light treatments with negative and positive phototactic responses. Moreover, we demonstrated that a configuration of blue light projected downwards onto leaves and UV-B light projected upwards onto leaves caused about 80% of adult spider mites to aggregate on the leaf side facing blue light. And this trend was observed irrespectively of the leaf side facing upwards. To further validate results from experimental settings, we experimentally infested bean plants and demonstrated that 10 min exposure to the light configuration of blue from the top and UV-B light from the bottom immediately before miticide application significantly improved the performance of miticide applications. We observed significant reductions in the numbers of both spider mite mobiles and eggs laid. A significant reduction in oviposition is likely attributed to a lower number of adults, as a large proportion of the initial population was likely killed by the miticide after being manipulated upwards into the crop canopy. Thus, results supported the study hypothesis that light sources elicit positive or negative phototactic responses and can be used to enhance the performance of miticide applications.

5. Conclusions

This study was composed of three main experiments, of which the following two were highly experimental: (1) the recording of movement by individual spider mites in the arenas with/without the presence of a shelter and (2) settlement on leaves exposed to different light source configurations and with the adaxial side facing either upwards or downwards. Results from these experimental studies informed a validation experiment with experimentally infested plants. Thus, it exemplifies how a research hypothesis can be comprehensively explored based on an experimental design with a progressively higher degree of complexity and applied relevance. Moreover, starting with seven light sources, we identified blue and UV-B lights as eliciting positive and negative phototactic responses, respectively. Despite a considerable consistency of results from this study with the existing body of literature, it is important to highlight that behavioral results obtained under highly experimental conditions should be interpreted with caution, unless combined with validation experiments which at least partially simulate real-world commercial crop production. Thus, in a whole-plant experiment, we demonstrated that integration of this combination of light sources caused about a two-fold increase in miticide suppression of mobile spider mites and a statistically significant reduction in egg counts. Thus, we have provided a thoroughly examined basis for commercial crop producers to consider this integrated approach to spider mite management. The integration of blue light (to elicit positive phototactic response) and UV-B (to elicit negative phototactic response) is believed to be of particular relevance to organic crop producers and/or to producers of crops for which few miticides are registered. That is, we demonstrated that the spray application of an organically certified miticide (BotaniGard Maxx) was significantly improved when combined with the integration of a customized light source combination.

Author Contributions

Conceptualization, T.W. and C.N.; formal analysis, P.J.S. and C.N.; investigation, T.W., J.H.L., C.N., A.V.M. and H.K.; methodology, T.W., J.H.L., A.V.M. and H.K.; supervision, C.N.; writing—original draft, C.N., T.W. and P.J.S.; writing—review and editing, C.N., P.J.S. and T.W. All authors have read and agreed to the published version of the manuscript.

Funding

This research was partially funded by the USDA/ARS Floriculture, Nursery Research Initiative, the American Floral Endowment, the USDA/Specialty Crop Multi-State Program (grant# 21-0732-001-SF), and the NIFA/Organic Agriculture Program (grant# 2023-04746).

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. A visual abstract of the experiments included in this study. This study was composed of three separate experiments to examine the potential of using light sources as part of spider mite pest management in controlled environment crop production systems.
Figure 1. A visual abstract of the experiments included in this study. This study was composed of three separate experiments to examine the potential of using light sources as part of spider mite pest management in controlled environment crop production systems.
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Figure 2. An illustration of the analytical approach applied to arena experiments. Observations for each treatment in movement experiments were ranked in ascending order, and a linear regression was generated. The regression coefficients (slope and intercept) are compared statistically among treatments.
Figure 2. An illustration of the analytical approach applied to arena experiments. Observations for each treatment in movement experiments were ranked in ascending order, and a linear regression was generated. The regression coefficients (slope and intercept) are compared statistically among treatments.
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Figure 3. Linear regression lines of spider mite bio-responses without presence of shelter. Linear regression lines of movement based on ascended ranking of observations.
Figure 3. Linear regression lines of spider mite bio-responses without presence of shelter. Linear regression lines of movement based on ascended ranking of observations.
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Figure 4. Linear regression lines of spider mite bio-responses with presence of shelter. Linear regression lines of percentage of time spent inside shelter based on ascended ranking of observations.
Figure 4. Linear regression lines of spider mite bio-responses with presence of shelter. Linear regression lines of percentage of time spent inside shelter based on ascended ranking of observations.
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Figure 5. The settlement of adult female spider mites on the leaves exposed to light source configurations. The different light source configurations [combinations of ambient (control), blue, near-infrared (NIR), and UV-B] were projected onto the top and bottom sides of soybean leaves. The same light source configurations were applied to soybean leaves placed with the adaxial leaf sides facing upwards (a) and downwards (b). The average bars (±s.e.) show percentages of adult spider mite adults on either leaf side. “n.s.” denotes non-significant, while “*” denotes significant preference at the 0.05-level.
Figure 5. The settlement of adult female spider mites on the leaves exposed to light source configurations. The different light source configurations [combinations of ambient (control), blue, near-infrared (NIR), and UV-B] were projected onto the top and bottom sides of soybean leaves. The same light source configurations were applied to soybean leaves placed with the adaxial leaf sides facing upwards (a) and downwards (b). The average bars (±s.e.) show percentages of adult spider mite adults on either leaf side. “n.s.” denotes non-significant, while “*” denotes significant preference at the 0.05-level.
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Figure 6. The performance of miticide application when integrated with light source combination. The average number (±SE) of mobile (live larvae, nymphs, and adults) (A) and live eggs (B) in response to the following treatments: Control (deionized water only), Spray (miticide spraying only), and Light + Spray (10 min exposure to a light configuration of blue light projected downwards and UV-B light projected upwards immediately before miticide application). The letters denote significant difference at the 0.05-level.
Figure 6. The performance of miticide application when integrated with light source combination. The average number (±SE) of mobile (live larvae, nymphs, and adults) (A) and live eggs (B) in response to the following treatments: Control (deionized water only), Spray (miticide spraying only), and Light + Spray (10 min exposure to a light configuration of blue light projected downwards and UV-B light projected upwards immediately before miticide application). The letters denote significant difference at the 0.05-level.
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Table 1. Observation metrics and regression results for experiments without presence of shelter.
Table 1. Observation metrics and regression results for experiments without presence of shelter.
VariableAmbientUV-CUV-BBlueRedWhiteNIR
Min2.810.430.432.216.394.630.50
Max26.9830.7432.7225.1332.1133.6926.44
Average (s.e.)12.47 ± 2.0817.01 ± 2.3513.14 ± 3.2413.65 ± 1.7216.43 ± 2.0313.29 ± 2.0511.27 ± 2.48
Adj R2-value0.860.960.90.940.940.770.93
Intercept (Int)−1.021.02−8.362.072.610.65−5.38
Slope (Slo)1.692.003.071.452.301.692.08
Z-value (Int) −1.102.61 **−1.69 *−1.79 *−0.632.07 *
Z-value (Slo) −1.52−4.08 ***1.19−2.43 **0.00−1.71
The movement experiments with individual spider mites in the arenas without shelter. Z-test pairwise comparisons of regression coefficients (intercept and slope) from ambient light source with those from the six other light sources in experiments with and without a shelter. Z-table values are available online, and critical z-values were approximately as follows: z = 1.6 (p < 0.05); z = 2.4 (p < 0.01); and z = 3.1 (p < 0.001). Accordingly, “*” denotes significant effect at 0.05-level, “**” denotes significant effect at 0.01-level, and “***” denotes significant effect at 0.001-level.
Table 2. Observation metrics and regression results for experiments with presence of shelter.
Table 2. Observation metrics and regression results for experiments with presence of shelter.
VariableAmbientUVCUVBBlueRedWhiteNIR
Min0.000.003.650.000.000.000.00
Max96.1499.5284.2886.8198.9692.41100.00
Average (s.e.)37.38 ± 6.8364.30 ± 6.4650.83 ± 5.2933.47 ± 6.4639.51 ± 6.6838.77 ± 7.0755.08 ± 7.58
Adj R2-value0.930.920.930.950.950.970.97
Intercept (Int)−15.0414.8710.25−16.56−12.23−16.64−4.17
Slope (Slo)4.994.944.064.764.935.545.64
Z-value (Int) −5.58 ***−5.26 ***0.31−0.570.35−2.31 **
Z-value (Slo) 0.112.28 **0.560.16−1.43−1.66 *
The movement experiments with individual spider mites in the arenas with the presence of a shelter. Z-test pairwise comparisons of regression coefficients (intercept and slope) from ambient light source with those from the six other light sources in the experiments with and without a shelter. Z-table values are available online, and critical z-values were approximately as follows: z = 1.6 (p < 0.05); z = 2.4 (p < 0.01); and z = 3.1 (p < 0.001). Accordingly, “*” denotes significant effect at 0.05-level, “**” denotes significant effect at 0.01-level, and “***” denotes significant effect at 0.001-level.
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Nansen, C.; Savi, P.J.; Ward, T.; Khodaverdi, H.; Lieth, J.H.; Mantri, A.V. Manipulation of Phototactic Responses by Two-Spotted Spider Mites to Improve Performance of Miticides. Crops 2024, 4, 568-583. https://doi.org/10.3390/crops4040040

AMA Style

Nansen C, Savi PJ, Ward T, Khodaverdi H, Lieth JH, Mantri AV. Manipulation of Phototactic Responses by Two-Spotted Spider Mites to Improve Performance of Miticides. Crops. 2024; 4(4):568-583. https://doi.org/10.3390/crops4040040

Chicago/Turabian Style

Nansen, Christian, Patrice Jacob Savi, Tora Ward, Haleh Khodaverdi, Johann Heinrich Lieth, and Anil V. Mantri. 2024. "Manipulation of Phototactic Responses by Two-Spotted Spider Mites to Improve Performance of Miticides" Crops 4, no. 4: 568-583. https://doi.org/10.3390/crops4040040

APA Style

Nansen, C., Savi, P. J., Ward, T., Khodaverdi, H., Lieth, J. H., & Mantri, A. V. (2024). Manipulation of Phototactic Responses by Two-Spotted Spider Mites to Improve Performance of Miticides. Crops, 4(4), 568-583. https://doi.org/10.3390/crops4040040

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