Applied Soil Ecology 15 2000 13–24
In search of biological indicators for soil health and disease suppression
A.H.C. van Bruggen
a ,∗
, A.M. Semenov
b
a
Department of Plant Pathology, University of California, 1 Shields Ave., Davis, CA 95616, USA
b
Department of Microbiology, Biological Faculty, Moscow State University, Vorob’evy Gory, Moscow 119899, Russia
Abstract
While soil quality encompasses physical and chemical besides biological characteristics, soil health is primarily an ecologi- cal characteristic. Ecosystem health has been defined in terms of ecosystem stability and resilience in response to a disturbance
or stress. We therefore, suggest that indicators for soil health could be found by monitoring responses of the soil microbial community to the application of different stress factors at various intensities. The amplitude of a response and time to return
to the current state before application of stress could serve as measures of soil health. Root pathogens are an integral part of soil microbial communities, and the occurrence of epiphytotics forms an indication of an ecosystem in distress. Disease
suppression can be viewed as a manifestation of ecosystem stability and health. Thus, indicators for soil health could possibly also function as indicators for disease suppressiveness. Previously suggested indicators for soil health and disease suppression
have mainly been lists of variables that were correlated to more or less disturbed soils ranging from conventional to organic agricultural soils, grassland and forest soils or to conduciveness to disease. We suggest a systematic ecological approach
to the search for indicators for soil health and disease suppression, namely, measuring biological responses to various stress factors and the time needed to return to the current state. © 2000 Published by Elsevier Science B.V.
Keywords: Microbial diversity; Microbial succession; Resilience; Stability; Stress
1. Introduction
The concept of soil health dates back to ancient civ- ilizations Doran et al., 1996. It has been considered
more or less synonymous to soil quality, defined as “The capacity of a soil to function within ecosystem
boundaries to sustain biological productivity, maintain environmental quality, and promote plant and animal
health” Doran et al., 1996. However, the Ad Hoc
∗
Corresponding author. Present address: Organic Farming Systems Group, Dept. of Plant Sciences, Wageningen University,
Marijkeweg 22, 6709 PG Wageningen, the Netherlands. Tel.: +31-317-478201; fax: +31-317-478213.
E-mail address: ariena.vanbruggenbiob.dpw.wag-ur.nl A.H.C. van Bruggen
Committee on Soil Quality of the Soil Science Soci- ety of America reserved this definition for soil quality
Karlen et al., 1997. Soil functions include life sup- port processes, i.e. plant anchorage and nutrient sup-
ply, water retention and conductivity, support of soil food webs, and environmental regulatory functions,
such as nutrient cycling, source of microbial diver- sity, remediation of pollutants, and sequestration of
heavy metals Bezdicek, 1996. Until recently, many researchers defined soil quality primarily in chemical
and physical terms but soil quality encompasses three basic components: biological, chemical and physical
properties while soil health is determined primarily by ecological characteristics Karlen et al., 1997. We
concur with Karlen et al. 1997 and consider soil quality a broader concept than soil health.
0929-139300 – see front matter © 2000 Published by Elsevier Science B.V. PII: S 0 9 2 9 - 1 3 9 3 0 0 0 0 0 6 8 - 8
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
