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SOIL HEALTH AND SUSTAINABILITY
IS
production. As discussed earlier, warnings of potential environmental damage
associated with modem agriculture were largely unheeded until recent decades.
The concept that the method of food production can have an additional direct
impact on animal and human health has recently developed, but only tentatively
in scientific circles. The proposal that any definition of soil quality or soil health
needs to incorporate the soil’s effect on human health as a component of equal
importance with productivity and environmental impact was perhaps first publicly articulated at the Conference on Assessment and Monitoring of Soil Quality
held at the Rodale Institute, Emmaus, Pennsylvania in July, 1991 (Papendick and
Parr, 1992; Rodale, 1991). Little headway has been made since then in defining
the indicators of soil quality and associated effects on human health.
A. DIRECT
AND INDIRECTEFFECTS
There are three general avenues through which the soil may interact with and
affect the health of higher animals. First, there is the potential for direct poisoning of animals and people from contaminated soils. This is most likely to be
highly localized and may be the result of industrial accidents or improper use or
disposal of agrochemicals, industrial chemicals, or radioactive waste products.
While the seriousness of such toxic encounters with the soil is not to be taken
lightly, the likelihood of the general population being exposed to soils so highly
contaminated as to seriously affect health is very small, There are numerous
well-documented occurrences of pesticide poisoning (Hodges and Scofield,
1983; Culliney et al., 1992), but most acute farm chemical poisonings occur
before the chemicals are applied to the soil, generally during mixing, or during
the spray process itself when chemicals are air-borne (Soule and Piper, 1992;
NCAMP, 1990). Recent dramatic increases in certain fungal diseases, often
fatal, seen in patients suffering from immunodeficiency diseases such as AIDS
can be traced to soil origins (Sternberg, 1994). Although naturally occurring, and
not normally associated with unhealthy soil conditions, it appears that soil disturbances, whether natural, as from earthquakes, or human initiated, create the
conditions necessary for the spores to be propelled into the atmosphere in numbers sufficiently high to infect the human population.
A second, more widespread degree of interaction between soil health and
animal/human health occurs indirectly, through the soil’s influence on the quality
of water and air. It is well-recognized that there are serious public health concerns related to contaminated groundwater, streams, and other surface water
supplies, occasionally including acute toxicity, but more often associated with
development of cancer and other long-term debilitating diseases. Nitrate in
drinking water can cause the potentially fatal methemoglobinemia, or blue baby
syndrome, but can also have more insidious carcinogenic effects if transformed
16
J. W. DORAN ET AL.
in the body to nitrosamines (Clancy, 1986). Nitrosamines can also form from the
reaction of nitrate with atrazine, a herbicide commonly found in wells in corngrowing regions (Culliney et al., 1992). According to a U.S. Geological Survey
assessment, nitrate-N levels in groundwater were above the 10 mg liter-’ limit
determined to be safe by the Environmental Protection Agency in at least 25% of
sampled wells in 87 counties in the United States, mostly in the Midwest
(USDA, 1987). The contamination is generally thought to be a result of inefficient nitrogen management associated with crop and livestock production. The
USDA estimates that nearly half the counties in the United States have groundwater supplies vulnerable to pesticide and nitrate contamination, potentially affecting 54 million people who rely on these sources for drinking water (National
Research Council, 1989).
Air quality can be equally devastated by poor agricultural practice. The combination of dry weather and poor soil management that caused the Dust Bowl of the
1930s created “billowing red-brown clouds that eclipsed the sun and obliterated
fences and covered houses and choked animals and people” (Hillel, 1991),
degrading air quality thousands of miles away in New York. Although airborne
soil pollution on the scale of the Dust Bowl is rare, localized dust storms and
tillage-induced soil clouds due to poor soil conservation methods continue to
impair air quality and affect those with respiratory disorders worldwide. More
catastrophic occurrences related to poor soil quality include landslides, floods,
and fires due to deforestation. Desertification occurring in Sahelian Africa and
other places has placed soil management practices in the path of a daily life and
death struggle against starvation.
The third avenue of impact of soil on animal and human health is also indirect,
and occurs through the quality of food plants grown on the soil. The effect may
be due to the presence of antiquality factors, such as toxic metals (lead or
cadmium), pesticides and animal diseases, or through decreased or imbalanced
content of necessary plant nutritional compounds, such as vitamins, proteins,
and minerals.
Of the two categories, the presence of antiquality factors is easier to detect and
trace to specific soil factors. Fruit and vegetables marketed in the United States
are mandated to be routinely screened for the presence of an array of pesticides,
but testing is random, and many pesticides are not detectable by commonly used
analytical methods (National Research Council, 1989). As of 1984, a National
Resource Council study estimated that only 10% of the ingredients in pesticides
had been thoroughly assessed for health effects. The most acute danger from
pesticide residues in food occurs when they appear in their original form, having
been sprayed directly on the produce, rather than being filtered first through the
soil medium. Dangers from soil-borne pesticides are far less apparent, as many
soil-applied pesticides are at least partially decomposed by soil organisms within
a short period of time. Nevertheless, several crops, such as potatoes, are among
SOIL HEhLTH AND SUSTAINABILITY
17
those considered to be in the high-risk category for cancer due to soil-applied
herbicides (Clancy, 1986). Additionally, metabolites from partially decomposed
soil-applied pesticides may persist in forms not tested for and whose biological
effects are unknown. Other pesticides will persist in their original form for many
years; some of these, while not particularly toxic at the original levels of application, may become concentrated in the food chain over time if they are stored in
fatty tissue. The health hazard from such bioaccumulation of agricultural pesticides remains as yet largely unquantified (Culliney et a / . , 1992).
Heavy metal and toxic element contamination, on the other hand, is generally
more identifiable as a soil quality problem. Such problems may result from
geological factors, such as high natural occurrence of the elements of interest in
bedrock, or be related to poor agricultural management (Allaway, 1975). The
Occurrence of selenium in soils demonstrates this point well. The U.S. Plant,
Soil, and Nutrition Research Lab in lthaca, New York, has carefully mapped
selenium concentrations in soils throughout the United States and has found that
areas considered to have selenium levels below optimum for plant growth coincided with areas of high rates of lung, breast, rectal, bladder, esophageal and
cervical cancer, although no direct causal link has been established. Low selenium in these soils might be considered a human antiquality factor, despite the fact
that it is due to the natural geology of the regions in which it is found. Areas
where selenium occurs in toxic levels, such as the Kesterson Reservoir in California, on the other hand, can be highly localized and generally associated with
improper water and soil management (Reisner, 1987). Grass tetany, a disease of
ruminants associated with magnesium deficiency and possible calcium deficiency, may also be due to low natural occurrence of the minerals, but is often
associated with over-fertilization with potassium and/or ammonium fertilizers
(Wilkinson and Stuedmann, 1979).
Free nitrate can occur as an antinutritive factor in food plants. Nitrate ingested
in plant tissue can react in the body as it does when dissolved in drinking water,
possibly leading to methemoglobinemia or conversion to carcinogenic nitrosamines. High nitrate content, a problem particularly in leafy greens such as
lettuce and spinach, has been linked additionally to reduced protein quality and
lowered vitamin contents of food crops (Knorr and Vogtman, 1983; Linder,
1985; Leclerc et a / . , 1991). Several studies report that vegetables grown with
biological sources of nitrogen showed significantly lower excess nitrate than
those grown under chemical fertility regimes (Ahrens el a / ., 1983; Lairon et al.,
1984; Vogtman el a/., 1984; Termine at al., 1987), but caution must be exercised
when determining whether one source of fertility is superior to another. While
conventional systems tend to provide large quantities of N in a highly soluble
form, which may lead to excess N uptake, systems which include spring plowdown of high-N green manure crops can lead to a similar situation under certain
conditions (Sarrantonio and Scott, 1988; Doran and Smith, 1991; Campbell et
18
J. W. DORAN ET AL.
al., 1994). Biologically derived N sources may lead to reduced nitrate concentrations in plants because of more gradual, microbially mediated release of soluble
N, but it is probable that any cropping system that adequately synchronizes N
availability with plant demand will less likely lead to excess nitrate in the crop
plant. Soil health assessment should include monitoring of nitrate synchrony
with crop needs throughout the year.
Aside from antinutritional factors, the quality of food is more difficult to
attribute definitively to soil health alone. Hornick (1992) addresses the problem
by classifying the numerous factors that affect food quality under the following
broad categories: crop plant and variety selection, management, postharvest
handling and storage, climate, and soil. Crop species differ markedly in their
nutritional needs and ability to absorb nutrients from the soil, and there are
tremendous varietal differences even within crop species. Lantz et al. (1958)
reported that varieties of dried beans (Phaseolus vulgaris) differed by as much
70% in protein content by variety and location. Cserni and Prohaska (1987)
found that nitrate in carrots of different varieties grown under identical conditions
ranged from 156 to 270 ppm. The architecture and efficiency of the root system
of individual plants have much to do with inherent ability to explore the soil
volume and take up nutrients. Plant breeding and selection may in fact have a
more significant effect on crop nutritional quality than the medium in which the
crop is grown (Clancy, 1986). Additionally, irrigation, weed control, crop maturity at harvest, and postharvest handling all significantly affect crop nutritional
quality in ways totally unrelated to the health of the soil (Kader, 1987). Climate
can obviously affect food quality directly in terms of plant stress, but has numerous interactions with the soil as well. Soils with higher water holding capacity,
for instance, have a greater buffering capacity against drought, which may help
maintain crop quality through prolonged dry periods.
B. LINKAGES
BETWEEN SOIL,FOODQUALITY,
AND HEALTH
The connection between soil health and food quality is not entirely straightforward. While soil fertility can have a profound effect on both crop quality and
quantity, crop plants can grow and yield well in soils supplied with inorganic
plant nutrients which have little int,eraction with the soil medium. Proponents of
food grown under production systems geared toward improving soil health, such
as organic or biodynamic systems, may feel strongly that such food is nutritionally superior, but rigorous scientific evidence to support this belief has been
difficult to obtain. In addition to the previously mentioned studies which reported
lowered nitrates in organically grown food, other studies have indicated several
different desirable food qualities associated with organic production, including
increased vitamin contents (Leclerc et a / . , 1991), increased dry matter (DeElI
SOIL HEALTH AND SUSTAINABILITY
19
and Prange, 1992), superior storage quality (Petterson, 1977; Knorr and Vogtman, 1983), and higher protein quality, as measured by EAA (essential amino
acid) indices (Eppendorfer, 1978). A nearly equal number of studies, however,
indicate that farming method per se had little effect on food quality (McSheehy,
1977; Nilson, 1979; Hansen, 1981). The USDA report on organic farming
(1980) was unable to verify that organically produced food was nutritionally
superior to conventionally grown food. Knorr and Vogtman (1983) outline the
problems involved in sifting through the volumes of available evidence on either
side of the issue. They point out that such studies are not closely linked to soil
health indicators, but are often pot experiments which test the effects of chemical
fertilizers vs organically derived fertilizers, as opposed to stabilized organic
systems. Additional problems include results reported in fresh weight bases,
which may underestimate nutritional value of crops with varying water contents,
and failure to test for trace minerals and vitamins, which may constitute subtle
but nutritionally significant differences in foods. The failure to link food quality
to actual soil health conditions, regardless of method of production, will continue
to impede an informed discussion on the relationship between soil health and
human nutrition.
Nutritional studies seeking to relate food quality to soil quality/health are
complicated by the fact that human populations rarely eat food produced from a
localized source. Experiments to test the effect of food supply grown under
different management systems are hampered by the nearly insurmountable logistical difficulties of controlling food intake in test groups long enough to show
significant differences in health. Nutritional studies additionally suffer from the
inability to make valid comparisons where food intake levels among test subjects
are unequal. The relevance of such studies is also subject to doubt given that few
individuals are likely to ever follow the prescribed diet of the test subjects in
detail.
Animal feeding studies offer some opportunities for studying, under controlled
conditions, the effect of food grown under varying soil management schemes,
but such studies have been scarce. Work by Velimirov et a / . (1992) reports the
findings of a rigorous nutritional study on three generations of rats fed on biologically produced compared to conventionally produced food. While they found no
differences in the number of offspring between the two groups, there were fewer
perinatally dead offspring in the groups fed biologically produced food, and the
mothers in that group had significantly higher weight gains during and after
lactation. In a study performed in 1926 (McCarrison), pigeons grew at a faster
rate on grains grown with organic fertilizers that those grown with chemical
fertilizers. The organically grown grain was thought to have higher vitamin A
and B contents, but analytical methods at the time could not entirely substantiate
the theory. McSheehy (1977) found that of mice fed diets from grains grown by
organic, chemical, or mixed (reduced chemical) farming, those on the mixed
20
J. W. DORAN ET AL
farming food source had the highest weaning rate, but no other parameters
differed significantly. Other studies have shown no apparent differences in animal
health or reproductivity related to the method of growing the food (Miller and
Dema, 1958).
In the short term, human and animal health is far more likely to be affected by
gross changes in the types of food eaten-away from high fat foods and toward
more vitamin rich ones, for instance-than by food with subtly different nutritional contents related to the way it was grown. Avery (1995) contends that the
benefits of chemically intensive agriculture in providing low cost, appealing
fruits and vegetables to consumers, thereby increasing their consumption and
utility in preventing cancer, far outweigh the small risks associated with the use
of chemicals. The presence of toxic residues on food, however, including systemic pesticides persisting in the soil, may in fact prove to be a long-term
determinant of human health. In light of this, consumers may choose a preference path that is least likely to provide unpleasant health-related surprises in the
future.
V. AGRICULTURE AND SOIL HEALTH
A. PERCEPTIONS
OF SOIL
While early civilizations and practitioners thought of the soil as a nurturing
entity (Mother Earth), a life-giver if not a deity (Lal, 1994; Soule and Piper,
1992), modern agricultural science often treats the soil as a physical medium for
anchoring plant roots, which can then be bathed in nutrient and growth regulator
solutions. It has been well proven that crops can be grown under such management systems, just as they can be grown without soil at all, in hydroponically
managed greenhouses. The short-comings of such soil management systems,
however, which neglect both the replenishment of organic matter and the maintenance of complex biological communities is readily apparent when one reviews
the role of these components in natural ecosystems. As discussed earlier, organic
matter is critical in many soils to maintenance of good soil structure, which
provides optimal drainage, water-holding capacity, and aeration for crop growth.
Organic matter also contributes significantly to cation exchange capacity (CEC),
which enables the soil to buffer nutrient concentrations in solution. While hydroponics may grow viable crops in artificially controlled aerated nutrient solutions,
large-scale agriculture is simply not feasible in soil lacking good structure and
nutrient-buffering capacity. Even on sandy soils, which have little structure and
are less vulnerable to structural degradation, production systems that rely on
inorganic nutrient supplies and neglect soil organic matter encompass inherent
SOIL HEALTH AND SUSTMNABILITY
21
inefficiencies. Soils which are incapable of storing nutrients require excessive or
continuous addition of soluble nutrients for crop growth, to compensate for
losses and inefficiencies. Soluble nutrients in excess of plant and microbial needs
will pass beyond the reach of plant roots, with potential consequences to the
groundwater already discussed, compounded by the loss of valuable and possibly
dwindling nutrient resources.
Soil organisms must be acknowledged as key architects in nutrient turnover,
organic matter transformation, and physical engineering of soil structure (see
Fig. 1). The microbial populations of the soil alone encompass an enormous
diversity of bacteria, algae, fungi, protozoa, viruses, and actinomycetes. As
many as 10,000 different species may be found in a single gram of soil (Torsvik
et al., 1990), just a small sample of the nearly two million species of microorganisms thought to exist worldwide, with a range of form and function beyond
current capacity for comprehensive study. While the specific functions and interactions of the majority of these organisms are as yet poorly elucidated, their role
as functional groups in soil health regeneration and maintenance is becoming
increasingly clear (Kennedy and Papendick, 1995).
The microbial biomass is largely responsible for mineralization and turnover
of organic substrates (Killham, 1994). It includes both primary and secondary
decomposers, aerobic, anaerobic, and switch-hitting digestors, highly specialized consumers of gourmet delicacies and feeding trough generalists, finicky
occupants of outlandish environmental niches and highly adaptable opportunists,
hard-driven frenzied achievers and slow-metabolizing plodders, diners of rich,
fatty substrates and those eking out an existence gnawing on tough lignaceous
scrap. As a group, the community of microbial populations acts without regard
for the future, but instead responds quickly to favorable conditions, reproducing
and consuming with wild abandon until substrate limitations cause population
declines, victims of their collective gluttony. They are in turn cannibalized by
their surviving compatriots. The result is a continuous cyclic ballet of nutrient
uptake and release that enables less ephemeral life forms in the soil to be supplied
with their nutritional needs in a somewhat regulated way.
The role of larger soil organisms in maintenance of soil quality and health has
finally begun to receive much deserved attention in soil science circles with the
publication of several excellent review articles in recent years (Berry, 1994;
Linden et a l . , 1994; Stork and Eggleton, 1992). Soil fauna cover a range of soil
functions beyond that of the soil microbial community. Anderson ( 1988) classifies soil invertebrates into three categories, based primarily on size. Microfauna
are those less than 100 p m in diameter and include protozoa, nematodes, and
rotifers. They are the aquanauts of the soil, existing in water films around soil
particles and free water in soil pores. They function as secondary consumers,
feeding largely on bacteria and fungi, thereby speeding the turnover of microbial
biomass and their associated nutrients. The diversity in nematode function is