Earthworms: Beneficials or Pests?
Earthworms are found in a wide range of habitats throughout the world, having adapted to many different soil types as well as to lakes and streams. Earthworms — often called night crawlers, garden worms, red worms or, simply, worms — are a valuable resource to many people. They provide bait for fishing, a source of protein for food and, most importantly, they play a unique and important role in conditioning the soil.
With the advent of chemical pest control, however, earthworms have become non-target recipients of many pesticides. Some of the most effective pesticides are broad spectrum in action, and they may inadvertently harm earthworms and other beneficial soil organisms. Harmful substances ingested by earthworms also may be concentrated up the food chain.
Earthworms belong to the phylum Annelida and the class Oligochaeta, which consists of over 7,000 species. Their bodies are long and tube-like, tapering on both ends and commonly ranging in length from 1 to 6 inches. Certain Australian earthworms are several feet long. Another characteristic of the phylum Annelida is a segmented body, including an enlargement of several segments to produce the clitellum, a glandular organ used for reproduction. Earthworms are hermaphroditic and homosexual, and thus they may function as either a male or a female during reproduction. Self-fertilization does not occur.
Although one acre of soil may hold up to eight million earthworms, most people pay little attention to these productive and beneficial animals. They mostly go unnoticed from day to day, unless a heavy rain forces them to the surface of the soil, an angler needs some bait or their casts disrupt a game of golf.
BUILDERS OF SOIL
Earthworms benefit the soil in many ways, primarily due to the physical and chemical effects of their casts and burrows. Earthworm casts, consisting of waste excreted after feeding, are composed mostly of soil mixed with digested plant residues. Casts modify soil structure by breaking larger structural units (plates and blocks) into finer, spherical granules. An exception to this has been reported from some Canadian clay soils in which, during wet weather, worms can convert a soil structure to a massive paste. As plant material and soil passes through an earthworm's digestive system, its gizzard breaks down the particles into smaller fragments. These fragments, once excreted, are further decomposed by other worms and microorganisms. Earthworm casts can contribute up to 50 percent of the soil aggregates in some soils.
Cast production is most abundant in moist spring and fall seasons when earthworms inhabit surface layers of the soil. During this time, 20 casts per square foot of soil surface are not uncommon, and as much as 40 pounds of casts per 1,000 square feet per year have been recorded. Under conditions of extreme temperatures or moisture stress during summer and winter, earthworms migrate downward into subsoil horizons and enter a resting state called aestivation. In irrigated areas, such as golf course greens, fairways and tees, this behavior may be altered and earthworms may not descend during the summer months. Thus, their activity may be regarded as a problem requiring management.
Many species of earthworms deposit their casts beneath the soil surface within their burrows, where casts contribute to pedogenesis. Species that excavate permanent, vertical burrows, however, deposit their casts on the soil surface, where they play a greater role in soil profile development. In addition to benefiting soil structure, casts also provide nitrogen in a usable form for other organisms that decompose organic matter on the soil surface. This interaction stimulates an accelerated decomposition rate, which helps reduce thatch buildup.
SOIL FERTILITY ENHANCED
Earthworms are also important to nutrient availability of the soil. As they feed, they deposit digested organic matter and associated minerals along their burrows in the form of casts, a rich source of nutrients is placed in close proximity to the plant roots that grow through the burrows.
Comparative analyses of casts and surrounding soil have shown that casts contain five times more nitrogen, seven times more phosphorus, 11 times more potassium, three times more exchangeable magnesium and one-and-one-half times more calcium. One explanation for this dramatic increase is that earthworms liberate nutrients from particles of both organic and mineral matter that would otherwise remain unavailable to plants. Lumbricus terrestris, the common nightcrawler, excretes pinhead-sized calcareous concretions that may raise the pH of the soil. Another factor is soil microbial activity within the casts, which promotes rapid transformation of soluble nitrogen into microbial proteins, thereby reducing the leaching of available nitrogen.
In soils populated by earthworms, accelerated decomposition of organic matter and an increase in available nitrogen results in greater numbers of nitrogen-fixing bacteria. Phosphorus availability also increases, due to earthworms' ingestion of phosphate rock particles and the consequent movement down burrows of phosphorus-containing casts. Furthermore, an abundance of earthworms means an abundance of decomposed organic matter — decomposition is limited only by the amount of material available, not by earthworms' capacity to ingest plant material.
AERATION AND DRAINAGE
Earthworm burrows, too, exert both physical and chemical effects on soil. Burrows are of two types. Temporary burrows are made by earthworms moving from one feeding site to another. Permanent burrows are homes to individual worms, are usually more extensive and are open to the surface, allowing the resident earthworm to select the most favorable microenvironment for feeding. Permanent burrows are fastidiously rebored by earthworms removing casts, organic matter and soil that have washed in.
As they burrow, earthworms excavate networks of passageways throughout the soil, which improves the soil's porosity. Up to two-thirds of all pore space in some soils are estimated to be the result of earthworm burrows, which can increase a soil's moisture-holding capacity — in some cases by as much as 400 percent. Because of the large diameter and low surface-tension of most burrows, they also serve as drainage systems during irrigation and heavy rainfall. This may account for better mixing of soluble nutrients throughout the soil profile.
Earthworms also act as effective agents of soil aeration. As they penetrate the topsoil and proceed downward into the subsoil, they may increase the soil-to-air ratio by eight to 30 percent.
With so many benefits to the soil accrued from the activity of earthworms, why are they given so little consideration when pesticides are selected — pesticides that ultimately bring them harm?
Pesticide registration guidelines initially gave little consideration to the potential impact of pesticides on non-target species. This has changed dramatically in recent years, and the Environmental Protection Agency (EPA) now gives considerable attention to the impact of pesticides on earthworms and other non-target species during the registration process. Use patterns that negatively impact non-target species are unlikely to obtain registration; in fact, at present there are no pesticides registered by the EPA specifically for earthworm control. In addition, the passing of the Food Quality Protection Act in 1996 had lead to the reevaluation of currently-registered pesticides to determine their relative safety to humans, non-target species and the environment. As a result, many pesticide uses have been discontinued by the product manufacturer. This is especially noticeable in the turf and landscape arena.
Additionally, the applicator is often unaware of the detrimental effects that various pesticides have on earthworms. To be sure, the acute effects of various pesticides on earthworm distribution and abundance have been the topic of very little research in this country. Even less is known about pesticides' chronic effects on earthworms.
Another explanation may be linked to the game of golf increasing in popularity during recent years. To meet the demands of greater use, more sophisticated means of pest control — and more advanced chemicals — are needed to maintain tees, fairways and greens under heavy use . Finally, early chemicals with broad-spectrum pesticidal activity and long-term residual effects, such as chlordane, resulted in the chronic reduction of earthworm activity. A single treatment could hold earthworm numbers in check for multiple seasons, depending on soil type and climatic conditions. By comparison, pesticides in use today are generally less toxic to earthworms; consequently, earthworm activity is more noticeable.
PESTICIDES AND EARTHWORMS
Toxicity to earthworms varies widely among types of pesticides classified by use — insecticides and related compounds, fungicides, herbicides, fumigants and vermicides. Two groups of pesticides are extremely toxic to earthworms and most other soil organisms:
Vermicides (designed intentionally to kill worms), most of which are no longer registered for use.
Herbicides, at the other extreme, pose relatively little threat of earthworm toxicity. Their modes of action are directed toward plant regulation, and physiological processes of plants differ significantly from those of animals. This leaves fungicides and insecticides responsible for the most extensive pesticide impact on earthworms.
Insects, like earthworms, may be beneficial inhabitants of the soil in that they decompose organic matter; they may also act as predators or parasites to harmful insects. However, they can also be serious pests and must be maintained below damaging levels. Root- and shoot-feeding insects, which pose the greatest threat to golf course turf, are presently managed with organophosphate and carbamate insecticides to reduce their populations to non-injurious levels. However, a determination of non-injurious population densities is purely arbitrary.
Earthworms are generally susceptible to carbamate compounds, which will significantly reduce their populations. Carbaryl, a carbamate pesticide often used for insect control, acts as a cholinesterase inhibitor, thereby producing long-lasting immobility and rigidity. Bendiocarb (Turcam) and propoxure (Baygon) are two other carbamate insecticides that cause paralysis in earthworms at normal dose rates. Carbofuran, another carbamate, is also very toxic to earthworms. Moreover, a sublethal response, characterized by weight loss, delayed clitellum development, and absence of cocoon production, has also been observed at recommended rates of carbofuran application.
Organophosphates are the most widely used class of turf insecticides. They have been successful in controlling white grubs, mole crickets, chinch bugs and sod webworms, to name a few. Of the organophosphates, ethoprop is the most toxic to earthworms. In contrast, chlorpyrifos, isofenphos and trichlorfon are considered non-toxic to earthworms when applied at normal dose rates.
Understanding how particular classes of biocides act upon target species may yield insights as to their effects on other living organisms. Organophosphates, as well as carbamates, mimic the structure of the acetylcholine molecule, an important component in the transmission of nerve impulses across synaptic gaps in many animals. Cholinesterase, an important enzyme in the nervous system, is responsible for the destruction of acetylcholine once a nerve impulse has crossed the synapse, thus preparing the synapse for another impulse. The presence of organophosphates or carbamates results in the phosphorylation of cholinesterase, thereby suppressing the destruction of acetylcholine. This results in a continuous firing of nerve impulses across the synapse, which is manifested as tetany. Because the axillary neuromuscular junctions of insects and other lower animals do not contain acetylcholine or cholinesterase, organophosphate and carbamate insecticides act instead on the central nervous system. The result is hyperexcitability, tremors, convulsions, paralysis and, eventually, death. Experimental evidence shows that long-term disruptions of the nervous system, such as excision of the brain, indicates that respiration in earthworms is not dependent on muscular contraction as in insects. Rather, it is the circulation of blood by rhythmic peristaltic muscle contractions that is affected. Thus, organophosphate and carbamate insecticides are believed to cause death by anoxia, not as a function of respiration but as a function of reduced blood circulation.
Of the numerous fungicides registered for use on turf, only those in the benzimidazole class have demonstrated any remarkable toxicity to earthworms. This class includes benomyl, thiabendazole, thiophonate-methyl and carbendazim, which is a metabolite of benomyl, and thiophonate-methyl. These compounds are used as broad-spectrum protectants. Their mode of action is primarily systemic; the ester metabolites of these compounds interfere with DNA synthesis by disrupting microtubule formation, which results in delayed mitosis. In addition to the acute toxicity of the benzimidazoles, other sublethal effects, have been noted in treated worms, including reduced feeding, retarded growth rates, reduced cocoon production and reduced nerve conduction velocity.
Carbamate fungicides will exert the same toxic effect on earthworms as do their insecticide counterparts, though their mode of action on the target pathogen may be entirely different. The thiocarbamates most often applied include various thiram products.
Although the abundance of earthworms may be affected by relatively few turf pesticides, earthworm distribution and behavior may be altered to a greater degree. Litter and surface soils treated with certain pesticides have a repellent effect on earthworms, and this reduces the breakdown and incorporation of organic matter into the subsurface horizons. Benomyl and carbendazim are particularly lethal to earthworms and also exhibit this repellent effect, which results in the avoidance of feeding in treated soils. Consequences include reduction in the amount of available nutrients in the root zone, decreased porosity and aeration of the soil, decreased water-holding capacity, and poor drainage.
Earthworms, though often regarded as an annoyance by golfers and golf course superintendents, also provide several benefits to turf. Reduction in the number of earthworms, whether intentional or not, can have a detrimental effect on both the physical and the chemical properties of the soil. Therefore, to maintain good soil structure capable of sustaining optimum plant growth, it would appear that attempts should be made to reduce the application of biocides known to adversely affect earthworm populations.
Clearly, the earthworm and its presence on the golf course raises many more questions than there are answers. Earthworms are generally thought to be beneficial; however, as with any other species, populations that are too high or out of place may warrant control actions. Currently there is insufficient data to determine at what levels earthworms become pests. In addition, a scientifically-based benefit: pest ratio has yet to be determined. Alternative management options need to be devised and the feasibility of such options evaluated. Chemical compounds can be developed specifically for earthworm control, but they may have a greater adverse effect on non-target organisms than pesticides registered for insect or pathogen control. All of these issues should be addressed and research carried out to answer the many questions that have arisen over the understanding of earthworm ecology.
Karen Delahaut is a vegetable outreach specialist in the Department of Horticulture and C.F. Koval is professor emeritus in the Department of Entomology, both at the University of Wisconsin-Madison.
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