18 A.H.C. van Bruggen, A.M. Semenov Applied Soil Ecology 15 2000 13–24
indicators for the response to stress, since the transi- tion from eutrophic to oligotrophic conditions likely
is an important characteristic for soil health. We suggest to test the following methods to track the
bacterial succession after application of a stress fac- tor: 1 the ratio of CFUs to total microscopic counts
Fig. 1, coined the index of microbial succession stage Zvyagintsev et al., 1984; Kozhevin, 1989, 2 the ra-
tio of copiotrophic to oligotrophic CFU Fig. 2 van Bruggen and Semenov, 1999, or 3 the ratio of res-
piration to microbial biomass Visser and Parkinson, 1992 which all increase in ecosystems after pertur-
bation and decrease with soil maturity. These indica- tors, and in particular, the second indicator reflect the
nutrient stress tolerance of the species present in soil. Interestingly, measures of nutrient stress tolerance of
the plant species in various communities were posi- tively correlated with resistance to frost and drought
stress and negatively correlated with resilience after fire MacGillivray et al., 1995.
It is somewhat more difficult to track fungal suc- cession in soil. CFUs obtained from dilution plating
are more indicative of fungal sporulation than of hy- phal growth. It is therefore preferable to use a direct
soil plating technique. Since many fungi have both oligotrophic and copiotrophic capacities, it is not very
useful to distinguish trophic groups on media differ- ing in nutrient contents. However, it is easier to iden-
tify fungi than bacteria using traditional classification techniques. Characteristic ‘sugar fungi’ such as the
Mucorales and Moniliales occur early in succession, while cellulolytic and ligninolytic fungi occur typi-
cally later in succession.
The above-mentioned techniques are quite insen- sitive to subtle changes in microbial communities.
Moreover, only a small proportion of micro-organisms can be isolated from soil. Techniques assessing mi-
crobial composition by measuring phospholipid fatty acid PLFA profiles and various DNA hybridization
or DNARNA fingerprinting techniques are more sen- sitive and culture-independent Torsvik et al., 1996;
Bossio et al., 1998. For example, microbial composi- tion as assessed by PLFA profiles was more affected
by specific farming operations disturbances than by farming system organic, integrated, or conventional,
but the time to return to the initial composition re- silience was not compared for the different farming
systems Bossio et al., 1998. Besides monitoring changes in microbial succession after a perturba-
tion, PLFA and DNA- or RNA-based techniques also give the opportunity to estimate microbial diversity
Torsvik et al., 1996. These techniques can then be used to compare recovery of the microbial community
from stress for soils varying in microbial diversity Crowley, 1997.
The problem with these techniques is that the extraction efficiencies of phospholipids and DNA de-
pend on soil type and microbial community Zhou et al., 1996, and that they give little if any information
about changes in functional capabilities. Moreover, fatty acids or DNA sequences characteristic for olig-
otrophs have not been identified yet. For soil health assessment, the number and identity of phylogenetic,
physiological and trophic groups is probably more important than biodiversity as such. Hence, charac-
teristic PLFA peaks and function-specific DNA or mRNA probes or primers are necessary to track spe-
cific microbial populations after a disturbance Liu et al., 1997.
Alternatively, substrate utilization tests such as pro- vided by ‘Biolog’ could be used to trace shifts in
metabolic activities by microbial communities Bossio and Scow, 1995; Grunwald, 1997. Differences in sub-
strate utilization patterns were detected after carbon enrichment Bossio and Scow, 1995; Grunwald, 1997
and soil moisture treatment Bossio and Scow, 1995. However, segments of the microbial community are
excluded on these substrate utilization plates, in partic- ular, slower growing organisms such as gram-positive
bacteria and oligotrophs Wuensche and Babel, 1996; Verschuere et al., 1997. Thus, all biological methods
listed above have some deficiencies. It is therefore im- portant to use more than one method to monitor mi-
crobial succession in soil.
In addition to these potential indicators, inoculum levels of root pathogens and subsequent disease were
also considered as potential bioindicators of soil health Visser and Parkinson, 1992; Pankhurst et al., 1995,
but this idea was rejected by Hornby and Bateman 1997 for a variety of reasons, in particular, the de-
pendence of root pathogens on cropping history.
5. Soil health and disease suppression
Despite the fact that plant disease suppression can- not be equated with soil health according to Hornby
A.H.C. van Bruggen, A.M. Semenov Applied Soil Ecology 15 2000 13–24 19
and Bateman 1997, disease suppression can be an important function of a healthy soil. Disease suppres-
sion is the phenomenon that less disease is incited than would be expected in the presence of a suscep-
tible host and a virulent plant pathogen, in a physi- cal environment conducive for infection. Various soil
factors, including physical, chemical and biological factors, can contribute to disease suppression or en-
hancement Hoeper and Alabouvette, 1996. In this review, we focus on biological factors contributing
to disease suppression, although we realize that the extent of biological suppression is affected by envi-
ronmental conditions, for example mineral nutrients Hoeper and Alabouvette, 1996.
Analogous to the distinction between general and specific indicators of soil health, there are two kinds of
disease suppression in soil: general and specific Cook and Baker, 1983. General suppression is a function of
antagonism and the nutrient and energy supply avail- able for growth of the pathogen through soil and on the
root surface. This kind of root disease suppression has often been observed in natural ecosystems or organi-
cally compared to conventionally farmed soil Fig. 3 Workneh et al., 1993; van Bruggen, 1995. The mech-
anisms and organisms responsible for this form of sup- pression are mostly unknown. Specific suppression,
on the other hand, is due to a specific interaction be- tween a plant pathogen and one or more antagonists,
for example an antibiotic producer or parasite. Spe- cific disease suppression can occur after monocrop-
ping, this kind of suppression is called disease decline. A well-known example is decline in take-all of cereal
crops caused by Gaeumannomyces graminis Cook and Baker, 1983; Hornby and Bateman, 1997. This
decline phenomenon has been attributed to increases in populations of specific antagonists like phlorogluci-
nol producing fluorescent pseudomonads Raaijmak- ers and Weller, 1998.
Although researchers often focus on one group of organisms at a time, general disease suppression can
be dependent on communities of micro-organisms. These communities may be associated with a sub-
strate at a particular stage of decomposition under certain environmental and management conditions
Boehm et al., 1993, 1997. The composition of func- tional groups rather than individual species may
determine the character of the community while indi- vidual species within a functional group may be in-
Fig. 3. Number of corky root Pyrenochaeta lycopersici lesions per tomato root A, and percentage of root tips with softrot
Phytophthora or Pythium sp. B in organic 4-year rotation, low-input 4-year rotation, conventional 4-year rotation, and con-
ventional 2-year rotation plots at the sustainable agriculture farm- ing systems SAFS field site at UC Davis in 1997 and 1998.
terchangeable. This functional composition is tightly linked to microbial succession during decomposition
of organic matter. Thus, similar to soil health, disease suppression is likely associated with particular stages
in microbial succession depending on the pathogen in question. It has long been known that the effects
of organic amendments on disease depend on the specific material used, its chemical composition and
C:N ratio, and the time elapsed since incorporation Papavizas et al., 1968. Many plant pathogens are
facultative saprophytes and can compete quite well with the soil microflora for colonization of fresh or-
ganic matter. If a cash crop is planted too soon after incorporation of a cover crop, the cash crop may
succumb to damping-off caused by Pythium spp. or Rhizoctonia solani Cook and Baker, 1983. We now
look at this established concept in a new light. Dur- ing the decomposition process of organic matter in
20 A.H.C. van Bruggen, A.M. Semenov Applied Soil Ecology 15 2000 13–24
Fig. 4. Damping-off of tomato seedlings caused by Pythium ultimum and Pythium aphanidermatum naturally occurring in soil
collected 1 day before, 1 day after and 1, 2, 3, and 5 weeks af- ter 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’ no
soil collected 7 weeks after incorporation, compare with Figs. 1 and 2.
soil, the soil ecosystem is subjected to oligotrophi- cation, and the ratio of oligotrophic to copiotrophic
micro-organisms changes during microbial succession Grunwald, 1997; van Bruggen and Semenov, 1999.
It is therefore likely that a particular range of this ratio is associated with general disease suppression.
The actual range may depend on the pathogen and its position on the scale from R- to K-strategists. For
example, Pythium ultimum, a typical R-strategist, was not suppressed immediately after cover crop incor-
poration Fig. 4, but also not in highly decomposed peat, when the proportion of ‘putative’ oligotrophs
was high Boehm et al., 1997. Soil with organic mat- ter at an intermediate level of decomposition may be
most suppressive in this case. On the other hand, R. solani, a typical K-strategist, was suppressed at later
stages of decomposition of organic debris in soil and at higher ratios of oligo- to copiotrophic bacteria than
Pythium aphanidermatum Grunwald, 1997.
6. Indicators for disease suppression
