implications of silvicultural pesticides on forest soil animals, insects, fungi, and other organisms...

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This article was downloaded by: [UQ Library] On: 11 October 2014, At: 10:03 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Communications in Soil Science and Plant Analysis Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/lcss20 Implications of silvicultural pesticides on forest soil animals, insects, fungi, and other organisms and ramifications on soil fertility and health Felix Ponder Jr. a a USDA Forest Service , North Central Research Station , Lincoln University , 208 Foster Hall, Jefferson City, MO, 65102, U.S.A. Published online: 05 Feb 2007. To cite this article: Felix Ponder Jr. (2002) Implications of silvicultural pesticides on forest soil animals, insects, fungi, and other organisms and ramifications on soil fertility and health, Communications in Soil Science and Plant Analysis, 33:11-12, 1927-1940, DOI: 10.1081/CSS-120004833 To link to this article: http://dx.doi.org/10.1081/CSS-120004833 PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions

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This article was downloaded by: [UQ Library]On: 11 October 2014, At: 10:03Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House,37-41 Mortimer Street, London W1T 3JH, UK

Communications in Soil Science and Plant AnalysisPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/lcss20

Implications of silvicultural pesticides on forest soilanimals, insects, fungi, and other organisms andramifications on soil fertility and healthFelix Ponder Jr. aa USDA Forest Service , North Central Research Station , Lincoln University , 208 Foster Hall,Jefferson City, MO, 65102, U.S.A.Published online: 05 Feb 2007.

To cite this article: Felix Ponder Jr. (2002) Implications of silvicultural pesticides on forest soil animals, insects, fungi, andother organisms and ramifications on soil fertility and health, Communications in Soil Science and Plant Analysis, 33:11-12,1927-1940, DOI: 10.1081/CSS-120004833

To link to this article: http://dx.doi.org/10.1081/CSS-120004833

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) containedin the publications on our platform. However, Taylor & Francis, our agents, and our licensors make norepresentations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of theContent. Any opinions and views expressed in this publication are the opinions and views of the authors, andare not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon andshould be independently verified with primary sources of information. Taylor and Francis shall not be liable forany losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoeveror howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use ofthe Content.

This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in anyform to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions

IMPLICATIONS OF SILVICULTURALPESTICIDES ON FOREST SOIL ANIMALS,

INSECTS, FUNGI, AND OTHERORGANISMS AND RAMIFICATIONS ON

SOIL FERTILITY AND HEALTH

Felix Ponder, Jr.*

USDA Forest Service, North Central Research Station,

208 Foster Hall, Lincoln University, Jefferson City,

MO 65102

ABSTRACT

Sufficient information is available to show that pesticides can be

properly applied and used safely in forest management. However,

much of the information on the effects of pesticides on soil

organisms is often based on methodologies involving soil

processes (i.e., toxicology studies) rather than on individual

groups of organisms. Because more than one group of soil

organisms may carry out the same function, the effects of

pesticides on a particular group can be missed. On the other hand,

while laboratory test may show pesticide effects on one group

under an array of controlled conditions, the same organism may

respond differently in a field setting. Not much information is

available on soil organisms resulting from combining various

silvicultural herbicides or pesticides. Information is presented to

show that with few exceptions, pesticides can affect soil organism

1927

Copyright q 2002 by Marcel Dekker, Inc. www.dekker.com

*E-mail: [email protected]

COMMUN. SOIL SCI. PLANT ANAL., 33(11&12), 1927–1940 (2002)

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populations, but the effects may be short-term with little

noticeable long-term affect on soil health and quality.

INTRODUCTION

Because of the unrelenting aggression of early succession plant species,

herbicides are likely to be a part of any cost effective approach to regenerating

old-fields to the production of fine quality hardwoods such as black walnut, red

oak, or white ash. Also, it is likely that pesticide usage is part of the history of

most old fields, those being converted to tree plantations. During the process of

selecting sites to plant trees, the decision on site quality is frequently based on

numerous physical and chemical factors. These factors may or may not be

manipulated to enhance soil quality and health; thus affecting the vigor and

health of the tree stand. Seldom, if ever, is it realized that pesticide applications to

control weeds or other pests could affect the site’s soil health and quality either

directly or through impacts on soil litter or its inhabitants. The effect of

silvicultural herbicides on soil organisms is poorly understood (1) and a

considerable amount of the data used to assess impacts are from laboratory work

rather than field trials.

The definition of soil quality and health is linked to the soil’s ability to

perform vital functions including to 1) sustain biological productivity, activity,

and diversity, 2) store and cycle nutrients and other materials, 3) partition water,

energy and solute flow, 4) filter, buffer, immobilize, and detoxify organic and

inorganic materials, and 5) support structures and protect archeological treasures

(2). Soil quality generally can be judged by soil properties that regulate their

ability to store and cycle nutrients and carbon, store and release water, and

provide favorable gas and heat exchange for specific functions. Soil

microorganisms play some role in all these soil processes, but they are

particularly important for nutrient and carbon cycling, energy flow, and nitrogen

fixation. Mycorrhizae are specialized soil fungi that penetrate secondary roots

during periods of root growth with structures called hyphae, thus becoming

extensions to roots to facilitate water and nutrient movement from soil to plant

(3–5). Alterations of physical and chemical conditions can alter the incidence of

soil borne microbes and diseases, which in turn, may affect the health of the

ecosystem and its inhabitants.

For example, habitat for small mammals that are important in distributing

fungal spores of several belowground mycorrhizal fungi (6) can be lost. Thus,

numbers, diversity, and activity of beneficial soil organisms can be reduced by

repeated removal of organic matter from a site. An examination of small mammal

digestive tracts revealed mycorrhizal fruiting bodies among the contents. Small

mammals included screws, mountain cottontails, chipmunks, ground squirrels,

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pocket gophers, mice, and voles. Ponder (7) concluded that rabbits and

grasshoppers are vectors of mycorrhizal fungi.

Further, the destruction of soil organic matter and associated degradation of

soil structure may lead to soil compaction and increased mechanical resistance to

root development (8). Another main consequence of soil organic matter loss is

the mineralization of carbon and nitrogen. Losses of carbon and nitrogen can be

substantial, as noted by Tiessen and Stewart (9), who observed net losses of 34%

carbon and 29% nitrogen over 60 years in a small grain-fallow rotation. When

cultivated soil was returned to zero tillage (no tillage) bulk density of soil in the 0

to 20 cm depth of the Ap horizon increased without substantial reduction in root

growth (10). It was suggested that roots utilized the biopores (earthworm burrows

and decayed root channels) of no tilled soil; and, hence, root growth was not

reduced. It is conceivable that young tree roots also initially utilize existing

openings in the soil during early years of growth during the conversion of

cropland and old-fields to forestland. Subsequently, during the conversion

process, soil organic matter increases. Further, soils lacking organic matter, as

well as numerous trace minerals and carbon, have very poor moisture retention.

Undoubtedly, loss of organic matter influences both soil quality and health.

Soils vary widely in their quality and capacity to perform vital functions.

Management activities affect long-term productivity and sustainability of soil by

altering soil conditions and processes. Where soil health is maintained or

improved, productivity will be maintained or improved. When soil functions are

imbalanced and soil health is degraded, plant vigor and productivity is reduced

(11). For example, long-term cultivation of croplands resulted in a reduction of

total soil organic matter (12). The purpose of this report is to discuss the

importance of soil organisms and how silvicultural management using pesticides

may affect them.

Role of Herbicides in Plantation Management

Environmentally safe, selective herbicide treatments include tree injection,

cut-stump sprays or wipes, basal sprays or wipes, directed foliar sprays, and soil-

spot and strip sprays. These treatments have the potential to control or suppress

the full range of unwanted plants when appropriate individual herbicides or tank

mixtures are used (13). Selective control can also be achieved using broadcast

applications of selective herbicides with aerial and ground systems. Changing

application rate, timing, additives, and herbicide formulation can often enhance

selectivity.

Among pesticides, chemical herbicides used in modern forestry are

vigorously tested and must meet strict standards of environmental safety and

human health protection before they are registered for use. The newer forestry

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herbicides act on biochemical processes such as photosynthesis, amino acid

pathways, and growth regulation (13). Most forestry herbicides used today

dissipate quickly by photodegradation, soil microbial biodegradation, and plant

enzyme degradation (14).

Importance of Soil Microorganisms

Soil microorganisms are increasingly the subject for study for their effect

on soil fertility and soil health, especially in the conversion of croplands into

forestlands. Soil organisms play a critical role in soil processes that regulate the

availability of nutrients and moisture in the soil for plant uptake. Their diversity

and abundance are affected by soil nutrient status, moisture, temperature, pH,

organic matter content, litter inputs, and vegetation type (15). Some soil

microorganisms have been reported to produce antibiotics or other metabolic

products, which inhibit various root pathogens (16). These organisms, their

genes, enzymes or metabolic by-products have the potential to benefit society in

the mitigation of polluted soil and for antibiotic production (17).

Another significant role of soil microorganisms is their ability to detoxify,

buffer or immobilize compounds in the soil. As integral components of the soil

foodweb, soil organisms are important food sources for many organisms at

different trophic levels.

REASONS FOR CONCERN ABOUT PESTICIDE EFFECTS ONSOIL ORGANISMS

The soil microbial community and larger inhabitants in the rhizosphere

(whole soil mass occupied by roots) are inevitably impacted on disturbed sites.

Compared to forested sites, the soil flora and fauna components beneath old-

cultivated fields are very likely to be different in both diversity and numbers.

Earthworm populations in no-till farming systems tended to be significantly

higher compared to till farming systems (18). It is important during the time of

old-field conversion to forest that management activities do not hinder the

development of these changing ecosystems. Although there is no “magic bullet”

for enhancing the restoration, there is great opportunity to use soil organisms as

“tools” (19). Also, research is now underway to identify organisms best adapted

to specific environmental and biotic conditions and to assess the potential for

managing these soil organisms. By understanding soil organisms and putting

them to wise use, land managers can better not only maintain populations of

beneficial organisms on site but also achieve greater likelihood of plantation

success. While presumed environmentally safe, selective herbicide treatments

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can be adapted to manage aboveground habitats and direct plant species

succession towards desired tree stands; there is concern that these chemicals may

affect the soil inhabitants and their functions.

Nutrient Cycling

Fine roots of developing vegetation move through the soil exuding

carbohydrates, amino acids, and other compounds that stimulate the growth of

microflora such as bacteria, antinomycetes, and fungi, which in turn produce their

own compounds that either stimulate or repel other soil organisms. Microflora are

the prime food for “grazer” herbivores such as mites, nematodes, and springtails,

which themselves fall prey to carnivores such as centipedes and spiders.

Saprophytic organisms feed on the dead remains of microbes and roots

accumulating in the rhizosphere that results in the decomposition of complex

organic molecules into basic components. Nutrients released through the

decomposition of organic matter, as well as water, may be captured and

transported to host plants by mycorrhizae (20). Mycorrhizae enhance water and

nutrient uptake not only by increasing the absorbing surface area of roots but also

through active physiological mechanisms. Ectomycorrhizal fungi (colonizes

primarily the root surface with hyphae extending into the soil) are associated with

woody species including oaks and conifers, and endomycorrhizae (colonizes the

inside of root cells with hyphae extending into the soil), which are commonly on

herbaceous species and a few woody species such as black walnut. Both groups

release enzymes that increase the availability of phosphorus to higher plants and

subsequently, its uptake (21–23). Mycorrhizae have been shown to increase

aggregation of soil particles (24).

Few nutrients leach from the soil when populations of soil organisms are

healthy and active (19). This is particularly significant for soluble forms of N

such as nitrate, which is highly soluble and mobile in the soil. As N and other

nutrients become available in the soil through decomposition of organic mater or

symbiotic and asymbiotic fixation, various soil organisms form an intricate

association to capture and assimilate N and other products into complex organic

compounds, and then slowly release them back into the soil.

Earthworms mix organic debris and applied organic and inorganic

materials, including fertilizers, lime, and pesticides, into the soil. These worms

are very important in cycling organic matter and nutrients in forest, pasture, and

no-till ecosystems (25). Although they ingest large quantities of soil and organic

matter, they excrete most of the carbon ingested (26). They form burrows that can

improve water infiltration, drainage, and aeration of the soil profile, as well as

increasing the extent and intensity of rooting. Earthworm casts and mucus

secretions tend to stabilize burrows while providing a nutrient-rich lining of the

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burrow that may further increase root proliferation. Incorporation of surface

residues by earthworms also speeds decomposition of the residues by other soil

organisms, increasing the amount and quality of the food source available,

including plant residues, can increase earthworm populations.

Nitrogen Fixation

Inadequate soil N is common on many sites. The most practical and

beneficial means of replenishing N is through biological fixation in the soil (27).

Symbiotic N fixation can add large sustained amounts of N to the soil (28).

Nitrogen-fixing plants form a mutually beneficial relationship with certain

bacteria and antinomycetes that allow for the conversion of atmospheric N into

ammonium N. The fixed N is absorbed and translocated by roots of host plants,

increasing the N concentration in living tissue, or released into the soil (29).

“Free-living” soil organisms can also contribute to the soil N supply by

asymbiotic N fixation. These organisms inhabit the soil and rotting organic

matter, and may be found in association with other soil organisms (30).

MEASURING PESTICIDE IMPACT ON SOIL ORGANISMS

Despite the extensive research on the fate of herbicides and other pesticides

in the environment, relatively little is known about how they are affected by

specific land management practices, especially over time. Many studies have

found reductions in numbers and types of soil organisms immediately following

or several years after soil disturbance, including timber harvesting, site

preparation, or prescribed fire (31–34). While short-term results are important,

managers need to know: 1) how different are these management-produced results

from results produced from natural changes such as wildfires and blowdowns and

2) do these changes affect soil productivity or sustainability. The ability or

“redundancy” of many different soil organisms to carry out soil functions and

processes makes it difficult to predict the long-term outcome. For example,

arthropod populations in a mixed-aspen forest one and two years after a wildfire

were much different than in an adjacent clearcut, but these differences were not

evident after 30 years (35).

Pesticides that are used repeatedly on a site and are slow to degrade may

result in an accumulation of pesticide residues. Some applied pesticides undergo

rapid degradation with the expectation that the ecosystem will recover

completely. While the soil seems to possess a high degree of resiliency to

management practices involving physical soil disturbances, more far reaching

effects on soil organisms may be from chemicals such as pesticides. In general,

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pesticide chemicals are not specific poisons for the particular pest they are used to

control, but are also toxic in varying degrees to other animals and man.

Crustaceans are among the most sensitive organisms. Fish are generally very

sensitive to pesticides, followed by, in order of declining sensitivity, reptiles,

birds, and mammals.

Also important in evaluating the impact of herbicides and pesticides, is their

persistence. Thirty years after the spraying DDT (dichloro diphenyl trichloroethane)

had ceased, levels of the chemical in shrews were significantly higher for sprayed

areas than for control areas (36). However, DDT levels have declined over time.

PESTICIDE DAMAGE

Of the approximately 1500 million kg of pesticides applied in the United

States, often less than 0.1% of those applied to crops reaches target pests (37).

Based on estimates by Pimentel and Levitan (37), over 99% of applied pesticides

moves into the ecosystem to be degraded by photolysis, hydrolysis, and microbial

action. Soil biota may obtain pesticides by coming in contact with them in the soil

or in plant roots (38). Once in the soil, pesticides can be adsorbed onto soil

particles, chemically bonded to other compounds in the soil, volatilized from the

soil surface into the atmosphere, move through the soil by molecular diffusion,

leached into or transported as run off in water, taken up by plant roots, or ingested

by soil fauna, thereby either entering the food chain or degraded. Partial

degradation of some pesticides can result in toxic metabolites. Some of these

chemicals may remain in the environment for a long period. Studies of pesticide

effects on soil fauna have reported increased numbers of Collembola, due

primarily to the reduction of predaceous mites; a natural enemy of Collembola

(38). These authors also conclude 1) that herbicides can greatly influence soil

invertebrates by their effects on vegetation which provides habitat and food for

many species, 2) the more persistent residues in soil do not always have as great

an influence on numbers of animals than do transient ones, and 3) most effects of

herbicides on mites and Collembola are indirect due to effects on the flora, and

generally have little effect on numbers. Many invertebrates take up pesticides

from soil into their body tissues and some, especially earthworms and mollusks,

can concentrate pesticides from soil and debris so that their tissues contain

concentrations several times greater than those in the soil in which they live (39).

When vertebrates feed on these contaminated invertebrates, they may in turn

accumulate a dose that may kill them or affect their normal activities.

Therefore, arthropods, parasites, and predators, as well as predaceous

amphibians, reptiles, birds, and mammals, may obtain and accumulate significant

quantities of pesticides by feeding on soil biota. In one investigation, for

example, the soil contained 10 ppm of DDT, earthworms contained 141 ppm, and

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the robins that were feeding on the earthworms contained 444 ppm in their brain

tissue (40). A similar situation is believed to have occurred in a midwestern city

when the robin population declined after feeding on DDT-resistant earthworms,

which had fed on fallen leaves from elm trees treated with the chemical. There is

little evidence that pesticides with relatively short half-lives and degrades

relatively quickly accumulate in tissues of invertebrates (38).

According to Lee (41), many insecticides and fungicides are toxic to

earthworms, but many herbicides are relatively harmless. All insecticides,

nematicides, mollusicides, herbicides and fungicides, once in the soil, can

potentially change populations of soil biota either directly or indirectly. Sutton

and Sheppard (42) reported that fungicide reduced mycorrhiza and subsequently

reduced aggregation of soil particles. Herbicides may greatly influence soil

invertebrate populations indirectly by their effect on vegetation, which provides

habitat and food for many of these animals.

Aside from just being able to accumulate large amounts of pesticides in

their body tissues, arthropods, plant pathogens, nematodes, and rodents have

developed resistance to pesticides. From the early 1900’s to 1980’s, a significant

number of arthropods species has developed resistance to one or more insecticide

or acarnicide (4). Georghiou and Mellon (44) reported that the number of

reported resistant species more than double in 10 years (Table 1). About 10

species of small mammals and plant attacking nematodes are known to be

resistant. Some spider mites have overcome the toxic effects of virtually every

pesticide to which they have been exposed (44).

Table 1. Increase in Number of Arthropod Species

Resistant to Pesticides

Number of Resistant Speciesa

Pesticides 1970 1980

DDT 98 229

Cyclodiens 140 269

Organophosphorus 54 200

Carbamates 3 51

Pyrethroids 3 22

Fumigants 3 7

Others 12 41

Total 313 829

a Species resistance in some part of its geographic range

does not imply that resistance is universal for any given

species [adapted from Ref. (44)].

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Table 2. Toxicities of Forest Herbicides and Other Products for Comparison; Small

Amounts for Acute Oral LD50’s Indicate a Higher Toxicity

Trade Name

Approximate

Acute Oral LD50a

(mg/kg)

Toxicity

CategorybSignal

Word

Other products

Gasoline 150 II —

Caffine 200 II —

Aspirin 1,240 III —

Baking soda 3,500 III —

Table salt 3,000 III —

Herbicides

Aatrex 4L 1,886 III Caution

Aatrex Nine-O 1,600 III Caution

Accord 5,400 IV Caution

Acme Brush Killer 2,000 III Caution

Arsenal AC .5,000 IV Caution

Banvel CST 5,000 IV Caution

Banvel 720 1,707 III Caution

Banvel 2,629 III Caution

Chopper RTU .5,000 III Caution

Escort .5,000 III Caution

Garlon 4 2,460 III Caution

Garlon 3A 2,830 III Dangerc

Krenite 24,000 IV Caution

Krenite S .5,000 IV Warningc

Oust .5,000 IV Caution

Pathway 8,000 IV Warningc

Pronone 10G .5,000 IV Caution

Rordon 5,000–6,000 IV Caution

Tordon 101 mixture 3,000 III Caution

Velpar L 7,080 IV Dangerc

Weedone CB 2,140 III Warningc

Weedone 170 2,000 III Caution

Weedone 2,4-DP 2,200 III Caution

From Ref. (13).a Unless otherwise indicated, values are for the formulated product (as in the container

before mixing).b Estimated oral amount needed to kill average person by category (II ¼ teaspoonful to an

ounce, III ¼ ounce to a pint, IV ¼ .pint).c Severe eye irritant, which increases the severity of the signal word.

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Repeated applications of the same or closely related chemicals to soils of

low adsorption have led to the development of microbial populations with an

enhanced ability to degrade the compound so that the efficacy of the pesticide is

reduced or lost (45).

Although simple acute toxicity assessments (Table 2) are possible for many

soil microorganisms, they are of dubious relevance in evaluating field responses

(46,47). In addition to mortality, changes in behavior, growth, morphogenesis,

feeding, reproduction, and even longevity must be considered. Whether laboratory

observations of these functions give valid answers are cause for concern and even

if they do, extrapolation to field predictions is filled with difficulty. Direct field

studies introduce methodological problems and are confounded by numerous

interactions with other organisms. Thus, it is perhaps best to consider pesticide

effects on soil organisms to be qualitative, rather than quantitative. Current

thinking suggests that the measurement of processes such as nitrogen

transformation and mineralization is more useful. This introduces problems

associated with naturally occurring stresses, such as drought and water logging,

which commonly reduces these activities by over 50%, before ultimate recovery.

It has therefore been suggested that assuming a microbial population would occur

in 30 days (i.e., 3 doubling times) under favorable conditions, so effects lasting less

than 30 days can be regarded as of “no ecological significance” (47). Furthermore,

Greaves and Malkomes (47) concluded that although soil processes are very

different from orthodox toxicological concepts, it is proving to be a useful

approach to the assessment of herbicide effects on microorganisms. Also, because

of rapid reproduction or the capacity of most species of soil organisms to

regenerate, initial mortality often has little permanent effect. However, initial

mortality may not always be the best estimate to measure effects on soil biota.

CONCLUSIONS

The objective explored here was to assess the importance of soil organisms

in the soil and litter and how pesticides may affect them. Only a few references

could be found in the literature on the direct effects of pesticides on microbial

activity in the soil. More cases of secondary or indirect effects were noted. The

soil microbial population is very resilient because various soil organisms carry

out similar biological processes: thus, often reducing the possibility of detecting a

change in microbial activity. In addition to using earthworms to evaluate soil

tillage effects, earthworms, can be an important tool to evaluate soil pollution and

pesticide activity. The various soil properties and different aspects of soil

management influence pesticide activity, especially leaching, which is affected

by both adsorption and rate of degradation. If the newer forestry herbicides are

applied properly, there should be little risk of damage to the ecosystem.

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