14 A.H.C. van Bruggen, A.M. Semenov Applied Soil Ecology 15 2000 13–24
Soil health can be considered a subset of ecosys- tem health. A healthy ecosystem is characterized by
integrity of nutrient cycles and energy flows, stability, and resilience to disturbance or stress O’Neill et al.,
1986. Thus, soil health may be associated with bio- logical diversity and stability. Plant and animal disease
outbreaks can be considered as indicators of instability and poor ecosystem health. Therefore, there is likely
also a link between soil health, the ability of the bi- ological community to suppress plant pathogens, the
population density of plant pathogens in soil, and ul- timately disease incidence and severity van Bruggen
and Grunwald, 1996. For this reason, disease sup- pression could function as an indicator for a stable and
healthy soil ecosystem.
In this paper, we will first explore the concept of soil health in more detail and discuss the relationship
between soil health and soil ecosystem stability. Sec- ond, we will explore various stress factors, the micro-
bial responses and resilience to a disturbance or stress. In the ecological literature, a distinction is made be-
tween disturbance short-term and stress longer-term or chronic, but we will refer to both of them as
‘stress’. Third, we will list some characteristics that have traditionally been suggested as indicators for soil
health, and we will propose a different approach to measuring indicators for soil health. Fourth, we will
relate soil health to root disease suppression. Fifth, we will mention traditional approaches to the search for
indicators for disease suppressive soils, and finally we will discuss some alternative approaches to searching
for such indicators.
2. Soil health
According to the definition of soil health given above, a healthy soil is a stable soil, with resilience
to stress, high biological diversity, and high levels of internal cycling of nutrients Elliott and Lynch,
1994. As pointed out above, ecosystem stability has been related to biodiversity and resilience in response
to stress. Soil resilience was defined in terms of tolerance against stress, buffering capacity, and the
ability to regenerate Szabolcs, 1994, but practical methods to measure soil resilience have not been sug-
gested so far. Similarly, a relationship between soil resilience and biodiversity has been suggested Elliott
and Lynch, 1994, but methods to prove or disprove this relationship have not been proposed so far.
Biodiversity in soil refers to a variety of taxonomic groups including bacteria, fungi, protozoa, nematodes,
earthworms and arthropods, but in this review we will focus on the first two groups. Microbial diversity in
soil is normally assessed as species or genetic diversity rather than structural and functional diversity. How-
ever, these last two measures of diversity may be more relevant to soil health Visser and Parkinson, 1992.
This statement is based on the assumption that there is functional redundancy in a healthy soil Beare et al.,
1995, so that the soil ecosystem will recover from a stress factor that eliminates part of the microbial com-
munity. Besides the active microbial pool there is a reserve pool of quiescent micro-organisms more di-
verse than the active pool which can respond to a dis- turbance such as addition of foreign substances to soil
Zvyagintsev et al., 1984. Soil homeostasis is main- tained by this diverse microbial pool. The larger the
functional redundancy and diversity, the quicker the ecosystem can return to stable initial conditions after
exposure to a stress or disturbance.
De Ruiter et al. 1995 calculated food web stability for various natural and agricultural soil ecosystems.
The calculated stability was slightly higher in a na- tive shortgrass prairie soil than in some agricultural
soils at similar or higher latitudes but not at lower latitudes, and in agricultural field plots subjected to
integrated farming methods than in companion plots subjected to conventional farming techniques. Soils
of natural ecosystems and integrated farming systems are generally considered healthier than those of con-
ventional farming systems, although this has not been proven conclusively. Despite the notion that a stable
soil ecosystem would imply a healthy soil, microbial populations and species composition are seldom sta-
ble but fluctuate with changes in environmental con- ditions.
3. Soil stress factors and microbial succession
Three kinds of stress factors can be distinguished: physical, chemical, and biological. The most im-
portant physical stress factors are extreme tempera- tures, extreme matric potentials drying and rewetting
cycles, osmotic potentials, and high pressure for
A.H.C. van Bruggen, A.M. Semenov Applied Soil Ecology 15 2000 13–24 15
example, by agricultural equipment. Chemical stress factors include pH, excess or shortage of inorganic and
organic nutrients, anoxia, salinity, and biocides, such as heavy metals, radioactive pollutants, pesticides,
and hydrocarbons. Biological stress factors include again nutrient deficiency or excess oligotrophica-
tion and eutrophication, respectively, introduction of exogenous organisms with a high competitive abil-
ity, and uncontrolled growth of particular organisms, such as pathogens or predators. Individual stress fac-
tors seldom operate in isolation: physico-chemical factors may enhance or weaken biological stress fac-
tors, or multifunctional stresses may result from one particular interference, for example soil tillage or
incorporation of organic amendments.
Any disturbance of soil will lead to a succession in bacteria and fungi and the associated food web.
It will also lead to an initial decrease and then an increase in biodiversity. The extent and duration of
the successional changes will depend on the inten- sity and duration of the disturbance. In this respect,
we have to distinguish between short-term disturbance and long-term or chronic stresses. In response to a
short-term perturbation biological communities in a healthy soil will return relatively quickly to the initial
conditions. Long-term or chronic stress will result in long-term succession leading to a new dynamic equi-
librium among ecosystem components.
Many researchers have studied effects of all kinds of disturbances like tillage, crop rotation, irrigation,
organic amendments, or application of fertilizers or pesticides on soil processes or major groups of organ-
isms in soil. For example, Bongers and co-workers studied the effects of both short-term disturbances and
long-term stresses on nematode communities Ettema and Bongers, 1993; Korthals et al., 1996; Bongers
et al., 1997. The nematode maturity index decreased and then increased after a disturbance Ettema and
Bongers, 1993, while the community structure was permanently damaged, as evidenced by extinction
of predacious nematodes, as a result of long-term stress Korthals et al., 1996. Under enriched nutrient
conditions, the maturity index decreased while the plant-parasite index increased Bongers et al., 1997,
characteristic for poor soil health.
Visser and Parkinson 1992 pointed to the impor- tance of changes in microbial community structure
and microbial and functional diversity to assess the
Fig. 1. Ratio of CFUs of copiotrophic bacteria to total micro- scopic counts of bacteria 1 day before, 1 day after and 1, 2,
3, 5, and 7 weeks after incorporation of a vetchoats cover crop ‘Cover crop’ or the same amount of vetchoats cover crop foliage
‘Fallow+debris’ into soil, or after leaving the soil unamended ‘Unamended’.
extent of degradation by surface mining and the progress in reclamation of degraded soil. However,
relatively few researchers have actually investigated changes in fungal and bacterial community structure
over time in response to disturbance or stress. Dom- sch et al. 1983 reviewed the response of soil fungi
to fungicide applications. They concluded that in soils with high fungal diversity and functional redundancy
the effects on soil respiration and decomposition of particular substrates is generally short-lived because
species insensitive to the fungicide will take over the functions of affected species. Another example is
that eutrophication by incorporation of fresh organic matter or drying and rewetting leads to a temporary
increase in microbial activity, CFU, and the ratio of CFU to total number of cells Fig. 1 Zvyagintsev
et al., 1984; Staben et al., 1997; van Bruggen and Semenov, 1999. The amplitude of the temporary in-
crease and subsequent decrease in CFU or microbial activity is larger in fallow soil than in cover-cropped
soil Fig. 1 van Bruggen and Semenov, 1999 or conservation soil Staben et al., 1997. Microbial di-
versity in terms of species evenness is expected to decline immediately after nutrient addition since a
limited number of species fast-growing, copiotrophic species respond quickly to excess nutrients Fig. 2.
Maximal biodiversity is expected in climax ecosys- tems. For soil, this means under oligotrophic con-
ditions with respect to available carbon sources and essential mineral nutrients, but mesotrophic or even
eutrophic conditions in terms of total organic carbon.
16 A.H.C. van Bruggen, A.M. Semenov Applied Soil Ecology 15 2000 13–24
Fig. 2. Ratio of CFUs of copiotrophic to oligotrophic bacteria 1 day before, 1 day after and 1, 2, 3, 5, and 7 weeks after incorporation
of a vetchoats cover crop ‘Cover crop’ or the same amount of vetchoats cover crop foliage ‘Fallow+debris’ into soil, or after
leaving the soil unamended ‘Unamended’.
This general concept was verified in a series of exper- iments in which the effects of various stress factors
temperature, mineral salts, drying-rewetting, and combinations of these factors on cellulase activity
and fungal communities were investigated for peat bogs Nizovtseva and Semenov, 1995; Semenov and
Nizovtseva, 1995. Maximal fungal diversity occurred when cellulase activity was minimal, namely under
oligotrophic conditions without addition of mineral elements or drying-rewetting stress. Any of the ap-
plied stress factors resulted in increased cellulase activity and a succession in the micromycete commu-
nity leading to an initial decrease in fungal diversity followed by an increase.
In other studies, metabolic diversity in terms of evenness as well as richness decreased after tillage
which results in an increase in available carbon compounds from necromass Lupwayi et al., 1998.
Similarly, scarification of forest soil resulted in a temporary lower metabolic diversity than in control
plots Staddon et al., 1997. Such a decline in di- versity after temporary eutrophication will likely be
followed by an increase in diversity as the soil returns to an oligotrophic state. The same may hold for other
disturbances, for example introduction of a denitrify- ing Pseudomonas fluorescens into a small-pore soil
fraction resulted in a temporary decline in microbial diversity White et al., 1994. From all these examples
it appears that consideration of microbial succession resulting from various stress factors will likely pro-
vide the means to determine the health status of a soil.
4. Indicators for soil health
