Optical Manipulation of Arthropod Pests and Beneficials

Contributors

Antoine Abrieux, Department of Entomology and Nematology, University of California, One Shields Ave, Davis, CA 95616, USA. Email: aabrieux@ucdavis.edu

David Ben-Yakir, Department of Entomology, Agricultural Research Organization, Volcani Center, Rishon LeZiyyon 7505101, Israel. Email: benyak@volcani.agri.gov.il

Joanna C. Chiu, Department of Entomology and Nematology, University of California, One Shields Ave, Davis, CA 95616, USA. Email: jcchiu@ucdavis.edu

Joseph E. Funderburk, University of Florida, North Florida Research and Education Center, Quincy, FL 32351, USA. Email: jef@ufl.edu

Daphna Gottlieb, Department of Food Quality and Safety, Agricultural Research Organization, Volcani Center, Rishon LeZiyyon 7505101, Israel. Email: dafnag@volcani.agri.gov.il

Gábor Horváth, Environmental Optics Laboratory, Department of Biological Physics, ELTE Eötvös Loránd University, H-1117 Budapest, Hungary. Email: gh@arago.elte.hu

Simcha Lev-Yadun, Department of Biology and Environment, Faculty of Natural Sciences, University of Haifa-Oranim, Tivon, Israel 36006. Email: levyadun@research.haifa.ac.il

Un Taek Lim, Department of Plant Medicals, Andong National University, 36729 Andong, Republic of Korea. Email: utlim@andong.ac.kr

Xavier Martini, Department of Entomology and Nematology, Citrus Research and Education Center, University of Florida, Lake Alfred, FL 33850, USA. Email: xmartini@ufl.edu

Masami Shimoda, Institute of Agrobiological Sciences, NARO, Tsukuba, Ibaraki 305-0851, Japan. Email: shimoda1@affrc.go.jp

Robert W.H.M. van Tol, Wageningen University and Research, PO Box 69, 6700AB Wageningen, The Netherlands. Email: rob.vantol@wur.nl

Glossary

Light

Contrast: The difference in luminance or color that makes an object (or its representation in an image or display) distinguishable. In visual perception of the real world, contrast is determined by the difference in the color and/or brightness (or degree and angle of linear polarization, or circularity) of an object and other objects within the same field of view. The maximum contrast of an image is the contrast ratio or dynamic range.

Diffuse light (skylight): Diffuse light makes it difficult to delineate the image of an object from its background.

Direct light (sunlight): The portion of the electromagnetic radiation emitted by the Sun that reaches the Earth’s surface directly.

Emission: The radiation emitted by a light source measured at a certain location by a spectrophotometer as intensity in photon units at each wavelength.

Fluorescence: The phenomenon whereby short-wavelength radiation is absorbed by a material and re-emitted as longer-wavelength radiation. Fluorescence may enhance the intensity of a signal in a particular region of the spectrum. However, it usually reduces the energy of radiation due to conversion costs.

Fluorescent lamp: A cool white fluorescent lamp that is operated by alternating current and has a flickering rate that can be detected by insects.

Fluorescent yellow: A bright yellow-lime color with a peak wavelength at about 525 nm. Its RGB values are R: 204 (80%), G: 255 (100%) and B: 0 (0%).

High-power LEDs (HP-LEDs): LEDs that can be driven at currents of up to 1 ampere (1 A). The HP-LED power densities can reach up to 300 W/cm². HP-LEDs lamps must be cooled to function. One HP-LED can replace an incandescent bulb in a flashlight, or can be set in an array to form a powerful light source.

Hue: A color or the shade of a color (wavelength) in comparison with the major colors red, orange, yellow, green, blue and violet.

Interlights: Lamps that are placed inside the plant canopy to overcome shading. LEDs are most commonly used as interlights. Interlights often increase crop yield and quality in greenhouses.

Light: A form of electromagnetic radiation characterized by its intensity (radiance), wavelength (λ; ultraviolet: 100–400 nm, visible/optical: 400–750 nm, infrared: 750–1000 nm) and polarization (linear, circular or elliptic).

Fig. G1. Subdivisions of the sunlight spectrum. (Modified from www.quora.com/Whats-the-range-of-wavelengths-of-visible-light-from-red-to-violet; accessed 17 December 2019).

Light-emitting diode (LED): A semiconductor light source that emits light when electric current flows through it. Standard LEDs are driven at currents up to tens of milliamps (mA). The light emitted from each type of LED has a narrow spectral range and therefore is considered monochromatic in practical terms. LEDs have several advantages over incandescent light sources, including lower energy consumption, a longer lifetime, a smaller size and less heat loss/emission.

Light intensity (radiance or brightness): The radiometric quantity. This can be measured as energy (W/m²) or as illuminance (lux: lumens/m²). In plant science, it is often measured as photosynthetic photon flux density (μmol photons/m²/s). It may also be expressed as a subjective perception elicited by the luminance of a source.

Light pollution: The harmful effects of unpolarized emission of artificial light sources on organisms. Light pollution interferes with visual perception and the natural behavior of arthropods due to the abundance of artificial lights during the night in the agricultural environment and in human dwellings.

Linear polarization: Light becomes linearly polarized when it is reflected from a non-metallic surface or is scattered from molecules of gases, liquids or solids. The degree of linear polarization depends on the angle at which the light hits the surface and the type of reflective material. Unpolarized sunlight becomes partially linearly polarized due to scattering in the Earth’s atmosphere. Dark water surfaces and dark grey asphalt roads, for example, reflect sunlight with a high degree of linear polarization. Linearly polarized light is commonly characterized by its degree of linear polarization (designated p) and angle of polarization (designated a) measured from a reference direction.

Monochromatic light: Light with a given wavelength (one pure color).

Photosynthetically active radiation (PAR): The spectral range of solar radiation from 400 to 700 nm that photosynthetic organisms use in the process of photosynthesis.

Polarized light pollution: In general terms, this refers to the harmful influences of polarized light reflected from artificial surfaces on polarization-sensitive animals. More specifically, it is the harmful effects of highly and horizontally polarized light reflected from smooth and dark artificial surfaces on positively polarotactic aquatic insects or insects associated with water.

Reflection: Sunlight, skylight or artificial light reflected by an object or a colored surface. It is either mirror-like (specular) or diffuse, depending on the nature (roughness/smoothness) of the reflecting surface. It is measured by a spectrophotometer as intensity in photon units at each wavelength and presented as a fraction (%) of the incident irradiance. Sunlight reflection of the Earth is termed surface albedo.

Spectrometer: An instrument for measuring the spectra of radiation. Spectrometers can be used as spectroradiometers or as spectrophotometers. A spectroradiograph is a graphical representation of the radiation measured by a spectrometer.

Transmittance: Radiation that is transmitted by an object, presented as a fraction of the incident irradiance.

Ultraviolet (UV) light: The portion of the solar radiation with wavelengths between 100 and 400 nm, which comprises 7–9% of the total solar radiation reaching the Earth’s surface. The UV spectrum is subdivided into UVA (315– 400 nm), UVB (280–315 nm) and UVC (100–280 nm). While 95% of UVA emitted by the Sun reaches the Earth’s surface, over 90% of UVB and all UVC are blocked by the stratospheric ozone layer. Although UV light is only a small fraction of the solar radiation reaching the Earth, it is a highly energetic and very penetrating radiation.

The eye

Apposition compound eyes: Each ommatidium receives light exclusively from its own facet or lens.

Broadband photoreceptors: Respond to a wide range of light spectrum. For example, in the ommatidium of Drosophila, the outer photoreceptors have a broadband spectral sensitivity that is thought to mediate achromatic vision exclusively.

Compound eyes: These are composed of densely packed visual units called ommatidia.

Dichoptic eyes: These are eyes that are situated on the head separately.

Holoptic eyes: These are eyes that meet along the median dorsal line of the head.

Iris cells (pigment cells): These cells surround each ommatidium and prevent the entrance of light from neighbouring ommatidia through the sides.

Narrow-band photoreceptors: Respond to a small portion of light spectrum. For example, in the ommatidium of Drosophila, there are four types of socalled inner photoreceptors expressing different narrow-band opsins.

Photopic eye: The eye of a day active insects that have color perception, high visual acuity and temporal resolution.

Scotopic eyes: The eyes of night-active insects that have poor color perception, low visual acuity and low temporal resolution.

Simple eyes: These are eyes that cannot focus and function mainly as detectors of the horizon and light intensity. They are usually present in arachnids (mites and spiders) and larvae of holometabolous insects, and as dorsal ocelli in most winged adult insects.

Superposition compound eyes: Each photoreceptor in an ommatidium receives light from its own facet or lens and several neighbouring ommatidia.

Vision

Achromatic vision: Vision characterized by a lack of color vision. It elicits a light intensity-dependent type of attraction.

Blue content: Defined as the solid angle or area of a target spectral emission per unit area in photon units of spectral sensitivity of the blue receptor, as seen by the eye. It is a measure of the response. The blue content depends on the display pattern as well as the color. For practical purposes, it is sufficient to calculate the blue content relative to a white paper in sunlight for each target.

Blue or green modulation: A measure of the response in the nervous system. The stimulus includes the total length of edges detected, besides the spectrum of sunlight, the contrast and the spectral sensitivity of photoreceptors. Estimates of modulation can be made relative to black/white edges or by measurement of signals in the optic lobe neurons.

Color constancy: A mechanism that enables the brain to recognize an object as having the same color under various lighting conditions.

Color-opponent mechanism: A model of opponent processing that includes the opsin of the outer photoreceptors scored to the best fit to wavelength discrimination data.

Contrast sensitivity: A measure of the ability to discern between luminances of different levels in a static image. Parallel bars of varying width and contrast, known as sine-wave gratings, are often used to assess contrast sensitivity. The width of the bars and their distance apart represent angular frequency, measured in cycles per degree. The contrast sensitivity is equal to 1/contrast threshold.

Electroretinography: A measure of the electrical responses to light of various cell types in the retina, including the photoreceptors, inner retinal cells and ganglion cells.

Green contrast: A measure of the stimulus detected by green receptors as they scan each boundary or edge.

Red, green and blue (RGB) color analysis: A method to identify a color by its red, green and blue components. Each component color is defined as a value on a scale between 0 (black) and 255 (white).

Spatial resolving power: This is linked to interommatidial angles determined by the number of ommatidia in each eye and their spatial arrangement. It is also affected by the rhabdom acceptance angle, which is determined by the diameter of the rhabdom. The smaller these two angles are, the greater the spatial resolving power of the eye.

Stereoscopic (or binocular) vision: This is enabled by partial overlapping of visual fields of the (compound) eyes.

Temporal resolving power: This is determined by the frequency with which images are sent from the eyes to the brain for processing. This frequency is often defined as the critical flicker-fusion frequency (CFF), a threshold at which an animal ceases to perceive a flickering light source as a series of flashes and instead sees it as a continuous stream of light. The higher the CFF, the better the temporal resolving power.

Visual acuity: This is determined by both spatial and temporal resolving powers. It is expressed by the angle with which one can resolve two points as being separate (when the image is shown with 100% contrast).

Behavioral responses

Aposematic coloration: A color design of organisms used to warn off predators.

Optomotor response: An innate behavior in insects and other animals (and humans) comprising a reflex turning of the eyes or head in response to movements of environmental objects. It serves for course stabilization during free locomotion through an involuntary displacement from a straight course. The purpose of this behavior is to regain the desired course of locomotion.

Phototaxis: Movement of animals towards (positive) or away from (negative) unpolarized light.

Polarotaxis: Movement of animals towards (positive) or away (negative) from polarized light.

Natural enemies of arthropod pests

Banker plants: Good host plants for natural enemies that are used for the initial establishment and maintenance of natural enemies in a greenhouse.

Insectary plants: Plants that are good hosts for natural enemies.

Recruiting: Encouraging natural enemies to migrate to and establish on crop plants.

Chronobiology

Chronotoxicity: Variations in susceptibility of arthropods to pesticides or to biocontrol agents during the circadian cycle.

Circadian: Activities that are repeated roughly every 24 h.

Diapause: A physiological state of dormancy used by arthropods to overcome periods of unfavourable environmental conditions. Possible mechanisms of diapause induction are: (i) internal coincidence, whereby a timer measures time differences in the onset and termination of day or night, and diapause will be induced when day length decreases below or night length increases above a defined threshold; and (ii) external coincidence, whereby an endogenous photoperiodic factor F is activated only when day length is over a defined threshold; diapause will be induced when F is not activated.

Phase shift: An advance or a delay in the bioclock of an organism often caused by a light or dark pulse given in a specific phase of its circadian cycle.

Photoperiod: Daily changes in light intensities, and in the duration of light and dark periods. Photophase is the daily period of light, and scotophase is the daily period of darkness.

Zeitgeber: An environmental cue that entrains or synchronizes biological clocks.

1Introduction and Summaries of Chapters

DAVID BEN-YAKIR*

Department of Entomology, Agricultural Research Organization, Volcani Center, Rishon LZiyyon 7505101, Israel

*benyak@volcani.agri.gov.il

1.1 Introduction

The phylum Arthropoda contains about 84% of all known species in the animal kingdom (Minelli et al., 2013). Arthropods live in most habitats on Earth, and they are usually well adapted to their environment. In this book, we focus on arthropods in the class Insecta (insects) and the subclass Acarina (mites). Arthropod pests are a major cause of reduction in quantity and quality of agricultural products (Oerke, 2005). Some arthropod pests are important vectors of microbial diseases that they transmit to humans, animals and plants (Eigenbrode et al., 2018; Mullen and Durden, 2018). Thus, arthropod pests cause significant harm to human health, food, wood and other resources. However, beneficial arthropods are important pollinators of many cultivated plants and serve as natural enemies that control many pests (Alford, 2019).

Toxic chemicals are currently the main means of protecting human interests against arthropod pests. Frequent applications of pesticides create health hazards for humans and their environment. Moreover, continuous use of pesticides often induces resistance in pest populations and harms beneficial arthropods. Therefore, alternative methods for protecting against arthropod pests are needed. In this book, we present several possibilities for using optical manipulation as a method for pest management.

Light is one of the most powerful environmental cues that influence organismal biology (Björn, 2008). Arthropods use the information encoded in light to reach their destinations and to adapt to changes in their environment (Cronin and Douglas, 2014). Much knowledge has been accumulated on the vision of arthropods (Warrant and Nilsson, 2006; Land, 2009; Land and Nilsson, 2012) and on their neural and behavioral responses to optical cues (Song and Lee, 2018; Cronin et al., 2014). This book deals mainly with optical cues perceived by arthropods from their hosts and their environment. It excludes optical cues given by the arthropods themselves to other organisms. It mainly covers arthropods that affect agricultural production and a few that affect the health of humans and their domesticated animals.

Because light is the main energy source for plant growth, most manipulations of light in the agricultural environment are aimed at improving the quantity and quality of plant products (Rajapakse and Shahak, 2007; Ilić and Fallik, 2017). Some manipulations of light are done to improve the production of domesticated animals (e.g. Bédécarrats and Hanlon, 2017). Optical manipulation of arthropod pests as a method of protecting agricultural crops was introduced by Antignus (2000) and was followed by studies by Ben-Yakir et al. (2012), Shimoda and Honda (2013), and Tazawa (2014). However, so far, the use of light manipulations for protecting against arthropod pests, or for enhancing the activity of beneficial arthropods, has been limited. The potential for using optical manipulation of arthropods is particularly high in protected crops (Vänninen et al., 2010; Johansen et al., 2011; Ben-Yakir et al., 2012).

In this book, we present the current knowledge on arthropod vision and the results of successful manipulations of arthropods. We also suggest new methods for using optical manipulation to protect against arthropod pests and to improve the performance of beneficial arthropods. Developing new methods for optical manipulation should be based on knowledge about light (both natural and artificial, and unpolarized and polarized), and on arthropod vison and behavior. Therefore, developing new methods requires the multi-disciplinary collaboration of basic and applied researchers. We hope that this book will enhance the use of optical manipulation as a component of integrated pest management.

This book was written mainly by applied scientists and is addressed to plant protection professionals. Due to the applied nature of this book, only brief overviews of the knowledge about light, vision and behavior are included (Chapters 2 and 3). The main applied information is presented in Chapters 6–9. The information in Chapters 3 and 7 is classified by the orders and families of the arthropods. The references included in this book are only a fraction of the published knowledge in the various topics. An emphasis has been put on recent publications, reviews and books that the readers can use for obtaining further knowledge.

1.2 Chapter 2: Light in the Agricultural Environment

Light is a transversal electromagnetic radiation characterized by its intensity (or radiance), wavelength and polarization. In the agricultural environment, light is usually a mixture of electromagnetic waves with wavelength-dependent intensity and polarization. The electromagnetic radiation of the Sun that reaches the Earth’s surface is the major source of energy and light for most biological processes. Unobstructed radiation from the Sun reaches the surface as direct light (sunlight), but if it is scattered or reflected, it reaches the surface as diffuse light (skylight). About half of the electromagnetic radiation of the Sun reaching the Earth’s surface ranges from ultraviolet (UV) to the end of the visible spectrum (100–780 nm). The visual systems of most animals have specific receptors for light within this range. The pattern of the angle of polarization of skylight is very important for the navigation of many arthropod species. The reflecting object determines the characteristics of the reflected light. The fraction of solar radiation that is reflected (surface albedo) by wet soil, forest, meadow and crop plants ranges from 5% to 25%. Water surfaces, shiny black horizontal plastic sheets used in agriculture and dark grey asphalt roads reflect sunlight with high degrees of horizontal polarization. The sunlight that reaches crop plants may be augmented by reflective surfaces below the plants or reduced by shading materials above the plants. In recent years, colored shading nets and optically active cladding sheets and nets are used for improving crop production. Artificial light sources are used as supplemental light for protected crops to increase the growth and yield of the plants. These include fluorescent, high-pressure sodium, metal halide, incandescent and light-emitting diode (LED) lights. Artificial lights, especially monochromatic LEDs, have high potential as tools for optically manipulating arthropods. Artificial light sources during the night interfere with the visual perception and natural behavior of both nocturnal and diurnal insects. Direct exposure of insects to light can have deleterious effects on them. Blue light (400–500 nm) can have lethal effects on various insects and may be used for pest control. In addition, direct exposure of plants to certain lights can indirectly have deleterious effects on insects.

1.3 Chapter 3: Arthropod Vision

Animal vision starts by detecting chromatic inputs using photoreceptors in the eye and continues by extraction and integration of the chromatic information in the brain. Arthropods have both simple and compound eyes. Simple eyes cannot focus, and function mainly as detectors of the horizon and light intensity. Compound eyes are composed of densely packed units called ommatidia. The iris cells surround each ommatidium and prevent the entrance of light from neighbouring ommatidia through the sides. Most day-active insects have apposition eyes, in which each ommatidium receives light exclusively from its own facet lens. Most nocturnal insects have refracting superposition eyes, in which light entering from several neighbouring ommatidia is focused on to a single photoreceptor. The partial overlapping of visual fields of the two compound eyes enables the insect to have stereoscopic vision. The visual acuity of the compound eye is determined by both spatial and temporal resolving powers. The number of ommatidia in each eye, and their spatial arrangement, determines the spatial resolving power of an arthropod. Visual cues must be large enough to be detected by at least one ommatidium to be resolved. Compared with vertebrates, the spatial resolution of arthropod eyes is lower and the temporal resolution is higher. Therefore, arthropods cannot see well-focused objects, but they can detect their motion very well. Under natural