Many basic and applied studies in insect ecology have considered responses of insect populations to their physical or chemical environment. For insects that live above ground, the mechanisms of behavioral responses to environmental factors often are directly observable. However, behavioral responses of soil-inhabiting insects are much more difficult to observe and quantify. Soil texture and structure can have a direct impact on arthropod behavior and adaptations. Field studies of soil insects often quantify the consequences of behavior, whereas the actual behaviors are only inferred. There have been studies of ecological and physiological adaptations of several soil arthropods that are not considered to be agricultural pests but have certain life history features that make them amenable to investigation. However, most insects that are agricultural pests as soil-inhabiting immature forms (e.g., wireworms or rootworms in corn, scarab grubs in turf grass) often have been studied in detail only in their more accessible, or observable, adult form.
This is in part because of the logistical challenge of observing the movements and other behaviors of the soil-bound larvae.
CHARACTERIZATION OF THE SOIL ENVIRONMENT
Soil Solids
Most soils have a complex structure, consisting of solids, liquids, and atmospheric gases. The solid components (e.g., sand or clay) constitute much of the soil matrix in bulk. Inorganic, or mineral, particles range in size from clays (<0.002mm in diameter) to silts (0.002-0.05 mm) to sands (0.05-2mm) to pieces of gravel (>2mm). The proportion of different sized particles, or soil texture, determines to a large extent the physical properties and appearance of a soil, as well as its ability to supply chemical nutrients to plants. The soil texture also has an impact on the soil arthropod population. For example, small soil arthropods sometimes find it difficult to move in heavy clay or tightly compacted soils.
Soil organic matter consists of an accumulation of partially disintegrated and decomposed plant and animal residues that have been broken down and resynthesized by microorganisms in the soil. Although organic matter usually does not constitute more than 6% by weight in topsoil (and even less in subsoils), it binds mineral particles into slightly larger granules that produce loose, crumbly soils that can hold more water than their mineral counterparts. Organic matter also is a primary source of energy for a variety of soil organisms, including many arthropods.
Pore Spaces
A typical loam soil will consist of roughly 50% soil solids (a combination of sand, silt, and clay) and 50% pore spaces and water. The size and distribution of pore spaces will depend on the size and shape of the mineral particles, as well as the activity of microorganisms. A predominantly clay soil will usually have very small pore spaces because the clay particles are very small and can pack together effectively. A sandy soil will tend to have much larger pore spaces because the sand grains are more irregular in shape and do not compact as readily. Atmospheric gases (most notably, oxygen and carbon dioxide) also occupy pore spaces and can move passively through the soil profile, depending on surface conditions.
Pore spaces are further characterized as micropores (<0.06mm) and macropores (>0.06mm). Macropores tend to allow movement of air and percolating water very readily, whereas micropores are the first to be filled with water in a moist field soil and do not permit much air movement into or out of the pores.
Convection can enhance the exchange of gases within a soil or between a soil and the atmosphere above. Aeration (movement of oxygen and other gases) near the surface of a soil occurs most readily in the presence of large, interconnected pore networks or channels. The rate of aeration is influenced by changes in barometric pressure, temperature gradients, and wind gusts. Temperature, relative humidity, surface texture, and continuity of soil pores affect the diffusion of gases into and out of soil.
Soil Water
Water (and dissolved minerals) accumulates in pore spaces and moves vertically through the soil profile if the surface input (e.g., rain or irrigation) exceeds the rate at which any vegetation absorbs the water. Water moves most readily through soils that have well-spaced,interconnecting macropores, but it also fills many of the micropores closest to the surface. Since water displaces air in the pore spaces, soils that are saturated with water cannot retain atmospheric gases that are critical to plant growth.
Soil moisture tension determines how much water remains in the soil at equilibrium and is a function of the sizes and volumes of pore spaces (matric potential), the presence of solutes in the soil (osmotic potential), and gravity. When the surface of a soil dries following an extended period of dry weather (further enhanced by low humidity or steady winds), water can also be drawn back toward the surface through capillary action.
The relative concentrations of oxygen, carbon dioxide, and water vapor often are considerably different in soil pore spaces (soil atmosphere) and in the open air. Oxygen concentrations tend to be lower and CO2 concentrations tend to be higher in the soil atmosphere as a result of plant and animal respiration and biochemical soil processes. Relative humidity tends to be relatively high, particularly in soils used to produce agricultural crops.
Soil Temperature
Surface temperatures of soils often fluctuate at least as much as ambient air temperatures, but the difference between the daily maximum and minimum temperature decreases as depth in the soil increases. There is a delay of maximum and minimum soil temperatures compared with the overlying surface temperatures, correlated with depth. Seasonally the maximum and minimum temperatures occur in the warmest and coolest seasons, respectively, in the upper soil layers. In contrast, the highest temperatures occur in early winter and the lowest temperatures occur in midsummer, at 7 m depth. Soil insects and other arthropods often move vertically in direct response to soil temperature, moving downward in late autumn to avoid freezing temperatures on the surface and returning to the surface in the spring to resume feeding.
FORMS OF LIFE IN THE SOIL
A vertical cross section of a soil profile reveals several distinct layers. The lowest layer, or horizon, is the C horizon, which consists of unweathered rock. The B horizon contains weathered, rough mineral soil with small deposits of humus. The A horizon normally has fine mineral soil interspersed with organic matter. The O horizon is a layer of plant debris lying on the surface of the mineral soil. The thickness of this layer depends on the amount of vegetation that is deposited seasonally and annually, and on the amount of degradation that occurs as a result of soil organisms. Within the O horizon are several layers, including (from the top) leaf litter, a fermentation layer, and a humus layer. The humus layer often merges into humus-enriched topsoil.
Soils and the overlying organic layer are not homogeneous, but rather are stratified. Similarly, the arthropods that live in these regions are grouped into different life-forms that have adapted to the various conditions that exist in the soil.
Euedaphons
Euedaphic soil arthropods inhabit the lowest soil layers, generally moving within the soil pore system. These arthropods usually are small and are characterized by a round or wormlike body form. The body size corresponds to that of the pore system, and extremities are often reduced. Because they cannot escape predators, many euedaphons generate and release toxic or defensive substances. Most euedaphons are photophobic and either lack eyes or have eyes that have degenerated considerably. They tend to have well-developed mechano- or chemosensitive organs, which compensate for their poor or nonexistent vision. Arthropods occurring in the euedaphon include several species of proturans, diplurans, and symphylans, as well as a few oribatid mites.
Epedaphons
Epedaphic arthropods live on the soil surface and in leaf litter. They are not well adapted to the conditions found in the soil pore system (e.g., high relative humidity, restricted gas exchange, restricted mobility). They are represented by many different body forms, usually are strongly pigmented, and often are dorsoventrally flattened. They have well-developed sensory organs and are highly mobile. Arthropods occurring in the epedaphon include oribatid mites (Oribatei), springtails (Collembola), ectobiid cockroaches, several cricket species, and several predatory beetles, including rove beetles (Staphylinidae) and ground beetles (Carabidae).
Hemiedaphons
The hemiedaphon group represents a transitory form of life, enabling some epedaphic or atmobiotic arthropods to occupy burrows in the soil. Hemiedaphic arthropods have the ability to excavate through soil by means of modified mouthparts or fossorial legs, and often they can enlarge existing cracks and pores. Several insect taxa have adopted a hemiedaphic life for a variety of reasons: to dig channels and then wait for surface prey to fall into the pit, to burrow through the soil hunting for small epedaphic arthropods, to avoid temperature or moisture extremes on the surface, or to feed on roots of plants. Hemiedaphic arthropods include earwigs (Dermaptera), field crickets and mole crickets, tiger beetles (Cicindelidae), and white grubs (scarab larvae).
ADAPTIVE STRATEGIES OF SOIL ARTHROPODS
Response to Soil Texture
Organisms in the soil (and leaf litter) community play very different roles, based in part on their size. Organisms (e.g., protozoa, bacteria, and some nematodes) that exist in water films, often in soil micropores, have resource requirements and defense needs that differ from those of organisms able to move in and out of soil pores independently. Similarly, a soil macroarthropod, as it grows, will perceive the soil matrix differently (Fig. 1). A neonate exists functionally as a microarthropod, able to move only within existing pores in the
FIGURE 1 Schematic representation of the impact of soil particle size on movement of a soil insect. Japanese beetle larvae (neonate, late first instar, mid second instar, and mid third instar) shown in a square centimeter of typical loamy sand soil.
soil. Thus its ability to move is a function of the porosity of the soil (including the size of the pores and their continuity). As the arthropod grows, less of the pore space is available for free movement. At this point pore space is less important in impeding movement than gross soil structure (impacting insect movement among soil aggregates) and aggregate density (movement through the aggregates). Plant root activity, surface cover, traffic and other sources of compaction, and density of soil organisms all impact aggregate formation. As the insect grows, less of the soil pore space is available to the insect for free movement, but it may take advantage of preexisting soil channels created by soil macrofauna such as earthworms, other arthropods, or small vertebrates. Water-filled soil pores can inhibit movement.
Response to Temperature
Several soil insect species demonstrate a seasonal pattern of vertical movement associated with soil temperature. In temperate climates, many soil macroarthropods move downward in late autumn to avoid freezing and return to the upper soil layers in spring. Some species move away from the soil surface in the middle of summer, in part to avoid high soil temperatures. Species-specific responses to soil temperatures influence periods of feeding activity and may enable similar species to occupy slightly different niches (e.g., wireworms, scarab grubs).
Response to Moisture
Some hemiedaphic arthropods have developmental stages that cannot tolerate extremes in moisture, and many of those stages are very sensitive to soil moisture levels. For example, grubs of several scarab species that had been held in dry soils moved upward almost immediately after moisture was applied to the surface. Several macroarthro-pods, including some wireworm species, alter the soil environment by creating semipermanent earthen cells. These temporary cavities enable the insects to create nearly saturated chambers in the soil, greatly reducing moisture loss from evaporation. Numerous desert arthropods create earthen cells in which they can aestivate when soil moisture is extremely low (or temperature is extremely high).
Usually, eggs and pupae of insects are most resistant to moisture loss and least able to escape undesirable conditions. Larvae and adults are often mobile stages and may be able to move away or alter their behavior to minimize the impact of adverse moisture extremes. For example, scarab larvae can move downward in the soil profile to seek moister (and cooler) conditions during periods of heat or drought stress. Heavily sclerotized soil arthropods may be less vulnerable to cuticular moisture loss than are less sclerotized forms, such as grubs or maggots.
Locomotion
Edaphic arthropods move through soil to locate food, to escape predators, or to escape unfavorable abiotic conditions. Adaptations for movement in soil depend on soil type, particle size, pore size, and soil density, among other things. Although many epedaphic species use their bodies as wedges, euedaphic species tend to dig through soil, using their legs and mandibles as shovels. Legs of edaphic insects often are highly modified to facilitate digging or burrowing through soil. At least one leg segment is likely to be enlarged, specially shaped, and edged with spines or lobes to create functional spades. Expanded tibiae or femora provide increased surface area, providing improved leverage when the insect is moving soil. For example, mole crickets (Orthoptera: Gryllotalpidae) use their greatly enhanced fossorial forelegs to burrow through soils very rapidly.
Many euedaphic arthropods lack obvious modifications for digging, but are able to move through soil by fitting between particles or by moving in existing burrows or crevices. Body shapes may be flattened or cylindrical, but in general antennae and legs tend to be reduced or absent. Millipedes serve as an example of the variety of adaptations that have arisen over time. Some species act as bulldozers with long bodies, many legs (for purchase against soil particles), and broad heads; other species have shorter bodies, fewer but longer legs, and tapered heads that allow the millipedes to wedge through small spaces in the leaf litter or upper layers of soil. Still other species of millipedes have very tapered anteriors and compressible bodies that can be used to widen crevices. The heavily sclerotized elytra and terga on adult beetles can provide a very effective protective shield when an insect is pushing aside soil particles or layers of leaf litter.
Host Finding
Much of the behavioral research that has been conducted over the past 50 years has centered on atmobiotic insects, in part because until recently it was virtually impossible to observe soil insects in situ without disturbing them. Destructive sampling techniques enabled researchers to make quantitative assessments but revealed very little information about how or why soil insects exhibited certain behaviors.
For many hemiedaphic insects, host finding begins with choices made by the mobile adult female as she seeks oviposition sites. For example, a female corn rootworm beetle (Diabrotica) may oviposit in a field where corn is growing, but if the field is planted to a different (nonhost) crop the following growing season, the neonates that emerge in the spring may have to move relatively large distances to reach a suitable host. Similarly, emerging scarab larvae must locate suitable roots and begin feeding within 24-48 h of eclosion, and overwintering grubs must relocate to suitable host plants when returning to the upper soil layers in the spring.
There are many plant-derived chemicals that elicit responses in insects in general, including host plant extracts that initiate host-searching behaviors or avoidance mechanisms. Many of the most intensively studied phytochemicals are produced in leaves or stems, but soil insects are more likely to respond to chemicals produced in the root zone. Some of these compounds are quite specific and elicit responses (e.g., host seeking) from limited taxa. Others, like carbon dioxide, are not species-specific and influence a wide range of soil insects. Chemicals produced in the soil (typically as root extracts) may diffuse over relatively large distances, but the diffusion rate depends on soil moisture, texture, and compaction.
Defensive Adaptations
Edaphic arthropods produce a variety of compounds that can function as contact toxins, repellents, or irritants. Many different taxa use similar biosynthetic pathways to produce closely related compounds. For example, several soil arthropod groups, including some millipedes and centipedes, as well as some chrysomelid larvae, produce hydrogen cyanide. The glands that produce this nonselective toxin apparently are not homologous, suggesting that the capability has evolved more than once.
Some edaphic arthropods have developed chemical defenses against deep-soil predators that use mechanoreceptors and chemore-ceptors to provide cues to locate their prey. Others evade predators by running or jumping. Epedaphic Collembola (springtails) that live in leaf litter are cryptically colored and have a highly evolved mechanism that enables the insect to jump away from a disturbance virtually instantaneously. In contrast, Collembola that live wholly within the soil (and thus are constrained by soil particles) tend to be smaller and paler, and to have less well-developed jumping mechanisms than epedaphic species. Instead, the euedaphic springtails secrete noxious fluids that protect them against many predators.
Interactions of Soil Insects with Chemical Control Agents
Edaphic insects that are considered to be pests in production agriculture or the green industry are often much more difficult to “control” than their atmobiotic counterparts. One of the greatest challenges is achieving adequate contact of an insecticide with the target insect. Many insecticides dissipate or degrade relatively quickly (before they reach the soil) or are adsorbed to soil particles. Most soil insecticides (and other pesticides) remain in the top 5-10 cm of the soil, where they are subject to microbial degradation. Soil factors such as pH, organic matter, moisture, temperature, and microbial community diversity will have a direct impact on the mobility and persistence of a soil insecticide. Insecticides that are highly mobile in soil may be ineffective because they move beyond the target zone too rapidly.
Many soil insects can detect the presence of insecticides and other chemicals and will initiate avoidance behavior (e.g., moving away from the soil zone in which the chemical is detected). Abiotic factors, such as soil moisture or temperature, that induce a target insect to move as little as 1 cm further into the soil profile may place target insects beyond the effective “range” of some chemical control agents. Often the manipulation of irrigation apparatus or the use of application equipment that incorporates a control agent directly into the soil at the desired depth can enhance the efficacy of a soil insecticide.
IMPACT OF SOIL ON PATHOGENS, PREDATORS, AND PARASITOIDS
Pathogens
The upper layers of most soils, as well as leaf litter, support active microbial communities. Many of these organisms are natural decomposers, breaking down plant and animal tissues that ultimately become part of the organic matter in the underlying soil. Interestingly, many edaphic arthropod populations are nearly free of disease. Several studies have demonstrated that secretions from many different edaphic arthropods inhibit vegetative growth or suppress the germination of pathogenic organisms.
Edaphic arthropods that are highly susceptible to pathogenic organisms in laboratory tests are rarely infected in the field, suggesting that there may be a critical behavioral component. For example, several soil insects, including earwigs (Dermaptera), mole crickets, and ants, tend and lick eggs. This behavior may remove fungal spores or bacteria or inhibit their germination. In addition, some laboratory studies utilize artificially dense populations of the target arthropod, which may enhance the spread of pathogens from one organism to another.
Nevertheless, several insect pathogens occur naturally in soils. For these pathogens to induce an epizootic, three conditions must be met. A susceptible host must be present, with host susceptibility being governed by population density, species composition, presence or absence of other stress factors, and behavioral responses to the pathogen. A pathogen must be present, with a suitable level of virulence and persistence. Finally, the environment must support both the host and the pathogen. Soil conditions, such as low temperature or high moisture levels, may stress the target insect population, predisposing individuals to infection and ultimately leading to population declines.
Several microbial insecticides were identified and developed during the last half of the 20th century. All were found in naturally occurring epizootics in the soil and were subsequently commercialized. Microbial insecticides are passively mobile because an insect that comes in contact with the microbial product may move some distance from the initial point of contact before it dies. The behavior of the target insect can be important to the spread of the pathogen, particularly when normal (or pathogen-induced) behaviors result in movement of individuals beyond their normal range. Most microbial insecticides are able to replicate within the host.
In some instances, edaphic arthropods are able to detect and avoid fungal pathogens in soil. In 1994 Villani et al. conducted a series of microcosm studies proving that when incorporated into soil, mycelial formulations of Metarhizium anisopliae, a naturally occurring soil fungus, repell third-instar Japanese beetle (Popillia japonica) grubs for as long as 3 weeks. Similar responses have been observed with tawny mole crickets and subterranean termites.
Examples of microbial insect pathogens include bacteria (e.g., Bacillus popilliae, B. thuringiensis, Serratia marcescens, S. entomophi-las), fungi (e.g., M. anisopliae, Beauveria bassiana, Fusarium spp., Penicillium spp., and Aspergillus spp.), protozoa (e.g., Ovavesiculapop-illiae), and various rickettsia (bacteria-like) organisms. Many of these have been developed commercially, with varying degrees of success.
External factors relating to soil condition may modify arthropod behavior. Localized flooding may force edaphic insects to move to unsaturated soils, whereas after several weeks without rain these insects may seek moister (usually lower) ground. These localized migrations may result in contacts between populations of edaphic insects and pockets of pathogen activity that otherwise might not have occurred. Disruptions in social behavior may increase or decrease infection rates. For example, studies have demonstrated that applications of sublethal rates of certain soil insecticides, such as imidaclo-prid, greatly increase the pathogenicity of some pathogens, including B. bassiana and some entomopathogenic nematodes (see next section). Apparently the sublethal exposure of the insecticide disrupts normal social behavior in the termite colony, including grooming, trophallaxis (food exchange), and construction of tunnels.
Predators and Parasitoids
Insect predators are mobile and self-replicating. Their effectiveness depends on the interaction of the soil environment with both the agent and the host. The initial contact and subsequent spread through the population depend on temporal and spatial overlap. The predator must be well adapted to the soil conditions. In particular, the predator must be able to move through the soil and to respond to host cues. Some predators are edaphic arthropods, such as predatory beetles or spiders.
Entomopathogenic nematodes can also be considered to be predators, since they move through the soil in search of host insects. Some species move actively, whereas others are more passive, ambushing prey as it moves nearby. Entomopathogenic nema-todes enter the host through natural openings, such as the mouth, spiracles, or anus. Nematodes in the genera Heterorhabditis and Steinernema carry a pathogenic bacterium, which is released in the body cavity of the host. The bacteria multiply within the host and produce toxins that kill the host rapidly. Although several nematodes species are available commercially, their efficacy in field conditions has been inconsistent, in part because the nematodes are extremely sensitive to temperature and soil moisture levels.
Several insects have evolved as parasitoids of edaphic arthropods. Host finding is presumed to be much more complex than for atmobiotic hosts because any host volatiles must move through the soil matrix. The parasitoid also must be able to move through the soil structure to reach the host. Studies attempting to evaluate the specific host-finding behaviors of these parasitoids must include consideration of soil texture, moisture, and temperature, as well as root zone exudates and sensitivity to movement-induced vibrations.
SAMPLING TECHNIQUES FOR SOIL INSECTS
One of the greatest challenges facing soil insect ecologists is the need to develop techniques of following insect movement and feeding behavior in situ while minimizing disturbance of the soil system. Until recently, researchers relied on the “snapshot” approach of collecting soil samples and sampling destructively, to determine how many soil insects might be present in the sample. This approach provided limited quantitative assessments but could not provide information over an extended period of time.
One technique that seems to be ideally suited to observing soil insect behavior is radiography, which has been used to trace the movement of scarab grubs and mole crickets in turfgrass, wireworms in corn, and onion maggots in onions, among other arenas. Plastic boxes of varying dimensions are filled with soil, and virtually any edaphic arthropod can be introduced to the microcosm and observed without disturbance. The technique has been expanded since Villani and Wright first described some of the applications in 1988. It has been used to investigate the response of soil insects to the presence of pathogens, to study the movement of two different species in a confined space, and to conduct preliminary basic observations of species behavior in soil. Understanding of insect movement in soil has expanded tremendously as a result of radiographic observations.
