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1 Ecological Interactions in Multispecies

Agroecosystems: Concepts and Rules

Chin K. Ong, Rhamun M. Kho, Simone Radersma

Key questions

1. Can agriculture mimic the beneficial functions associated with natural ecosystems?
2. What are some of the drawbacks of multispecies agroecosystems?
3. How can we know whether below-ground interactions are important?
4. How can we develop a predictive understanding of multispecies systems?
5. What are the basic rules we need to know?

1.1 Introduction culture that is completely dependent on fos-

1.1.1 Agriculture as a mimic of nature?
The idea of designing a multispecies agro-
ecosystem as a structural and functional
mimic of natural ecosystems is appealing,
because it offers a simple integrated principle
for working towards sustainable agriculture.
The hypothesis that diversity is associated
with higher productivity is not new; as early
as 1859 Charles Darwin asserted that
it has been experimentally proved that if a plot
of ground be sown with one species of grass,
and a similar plot be sown with several distinct
genera of grasses, a greater number of plants
and a greater weight of dry herbage can be
raised in the latter than in the former.
The search for new models for agriculture is
particularly attractive where modern agri-
© CAB International 2004. Below-ground Interactions in Tropical Agroecosystems
(M. van Noordwijk, G. Cadisch and C.K. Ong)
sil energy and chemical inputs is unafford-
able, unsustainable or no longer acceptable
to our quality of life (Lefroy et al., 1999). But
natural systems are much more complex
than any form of agriculture used today,
where the trend is still one of reducing com-
plexity. In a recent review, Vandermeer and
his co-workers (1998) argue that multi-
species agroecosystems are more depend-
able, in terms of production, and more
sustainable, in terms of resource conserva-
tion, than simple ones. However, despite
efforts made to prove this during the cen-
tury and a half following Darwin’s assertion,
the evidence is not yet conclusive.
In his review of the issue in the context
of the humid tropics, Ewel (1999) also con-
cluded that it pays to imitate natural sys-
tems, especially with regard to the use of
1
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2 C.K. Ong et al.
perennial plants to maintain soil fertility,
protect against erosion and make full use of
light, water and nutrients. However, there is
a trade-off between maintaining full vegeta-
tive cover and promoting the growth of
desirable plants. It may therefore be neces-
sary to accept a lower ‘crop’ yield, because
an intrinsic feature of natural systems is a
high investment in structure. On the other
hand, reducing the complexity of agricul-
tural systems to promote ‘short-term’ pro-
ductivity, by substituting external inputs for
biological functions, tends to further
increase dependence on such inputs. High
levels of fertilizer tend to switch off special-
ized mechanisms of nutrient input and
cycling, such as biological nitrogen fixation
(Chapter 13, this volume) and proteoid roots
(Chapter 7, this volume).
Ong and Leakey (1999) attempted to rec-
oncile differences between recent agro-
forestry research and interactions between
savannah trees and understorey vegetation
in the semiarid tropics. Whilst the productiv-
ity of natural vegetation under savannah
trees is generally higher than that of vegeta-
tion between the trees, the expectation
derived from this observation – that growing
trees among crops (‘agroforestry’) will boost
crop yields – has generally not been con-
firmed in experiments. Van Noordwijk and
Ong (1999) explained that because a high
proportion of the above-ground part of
mature savannah trees consists of a woody
structure, rather than foliage, they provide
shade and microclimatic improvement
whilst incurring only a low water-use ‘cost’.
This means that the amount of water ‘saved’
by the resultant reduction in soil evapora-
tion may more than offset the water ‘lost’
through tree transpiration. In recently
planted trees (‘new agroforestry’) the
amount of water used for transpiration
exceeds the reduction in soil evaporation, so
decreasing the amount of water available for
crops. A basic problem is that savannah
trees’ investments in woody structure
require time and energy, thereby reducing
returns to farmers. Thus there is a penalty,
which takes the form of a long wait before
trees mature and before any benefit is seen
in terms of understorey productivity.
Existing trees can be used for their beneficial
effect, just as they have by millions of farm-
ers in the parkland systems of West Africa.
However, the idea that this beneficial effect
can be emulated and further improved upon
in ‘designed’ agroforestry is one that has led
to much disillusionment.
How can we confidently relate the func-
tion of a mimic system to its structure when
we know so little of the underlying
processes that confer persistence and
resilience on the natural ecosystems on
which a mimic system is based? Perennial
vegetation has considerable benefits in terms
of maintaining such ecosystem functions as
‘catchment hydrology’ (Chapters 6 and 18,
this volume), ‘nutrient cycling’ (Chapter 10,
this volume), ‘nitrogen fixation’ (Chapter
13, this volume) and ‘reduction of trace
gases’. Such benefits encourage the use of
agroforestry as a technique that allows
sustainable land and water management in
areas where high-energy-input or large-
scale agriculture are impractical (Kidd and
Pimental, 1992). Thus, information on the
underlying processes in less complex sys-
tems (such as agroforestry) may provide
important clues about the same processes in
multispecies agroecosystems.
1.1.2 Multispecies agroecosystems
Multispecies agroecosystems (associations of
two or more species growing together on the
same piece of land in a certain temporal and
spatial arrangement) are widespread
throughout the tropics. In comparison with
monocrops, such systems promise the fol-
lowing three benefits to farmers: increased
productivity, increased stability and
increased sustainability. The first potential
benefit concerns total productivity, which can
be higher, i.e. output of valuable products
per unit of land and labour is increased,
through reduced damage by pests and dis-
eases (Chapter 15, this volume) and through
better use of resources. A multispecies sys-
tem often has a green canopy that is denser
for longer than that of a monoculture,
allowing it to capture light that would be
lost in a monoculture. The mixed canopy
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Ecological Interactions in Multispecies Agroecosystems
may also reduce weed competition and
reduce water loss by evaporation directly
from the bare soil, leaving more water for
productive transpiration. A deeper and
denser rooting system in a multispecies sys-
tem may exploit the soil more completely,
increasing the potential for water and nutri-
ent uptake (Chapters 4, 5, 6 and 10, this vol-
ume). Better soil physical properties and the
reduction of runoff (Chapters 9 and 18, this
volume) may conserve water, whereas
enhanced soil biological activity and nutrient
cycling may increase the availability of
nutrients (Chapters 11 and 14, this volume).
The second potential benefit of multi-
species systems is increased stability, i.e. sen-
sitivity to short-term fluctuations is reduced
by decreasing the risk of pests and diseases
(Chapter 15, this volume) and by spreading
those risks through species diversity
(Chapter 16, this volume). If one plant com-
ponent fails to produce, the production of
the other plant components may compen-
sate for it. In agroforestry systems, trees may
increase the microscale variability in soil and
in crop growth, which increases the proba-
bility that at least part of the crop will yield
successfully.
The third potential benefit of multispecies
systems is increased sustainability, i.e. long-
term productivity is maintained by the pro-
tection of the resource base. This may be the
result of, for example, reduced erosion,
input of nitrogen through biological N2-fixa-
tion (Chapter 13, this volume), retrieval of
subsoil nutrients and/or reduction of nutri-
ent losses through reduced leaching
(Chapter 6, this volume). Productivity and
sustainability are interrelated and have the
potential to conflict, especially in nutrient-
limiting environments. Increased productiv-
ity may imply an increased exploitation of
the environment and a mining of nutrient
resources. As a consequence, on infertile
soils a productive system with high outputs
will most probably not be sustainable with-
out external inputs.
A potential drawback of multispecies sys-
tems is that plant components of a lower
value to the farmer may compete too heav-
ily with those of a high value. However, by
species choice and arrangement, competition
3
can be controlled/manipulated by appropri-
ate management (Chapter 17, this volume).
Van Noordwijk and Ong (1999) commented
on the different ways ecologists and farmers
perceive ‘competition’. To the first, the term
often refers to ‘use of and dependence on
common resources’; and, competition
between individuals of the same species is
generally stronger than that between indi-
viduals of different species. To the farmer,
however, the yardstick against which com-
petition is ‘measured’ is the ‘value’ derived
from the growth of the different plants. If all
plants have an equal value per unit biomass
produced, as happens in a monoculture,
there is no perception of the occurrence of
competition. Competition becomes a prob-
lem if the difference in value increases.
Companion plants of lower use/value can
then become ‘weeds’ and competition is
seen to increase, even though the resource
base (in space and time) of these plants can
partially differ from that of the crops.
In this chapter we introduce concepts and
models that can be used to explore how and
where multispecies agroecosystems may be
able to improve the use of plant growth
resources, using experience gained from
recent agroforestry research. We will begin
by unravelling the complex interactions that
occur between trees and crops. We will then
examine how resource availability influ-
ences competition between plants and,
finally, we will define simple rules governing
success or failure when mixing trees and
crops. A list of the models and their applica-
tion for above- and below-ground interac-
tions are discussed elsewhere in this book
(Chapter 3).
In the past, sweeping generalizations
have been made, which suggested that any
multispecies system was better than any
monoculture. However, because we can
now acknowledge that sufficient evidence
exists to prove such supposition false, the
current goal of interaction research is to
determine which particular multispecies sys-
tem will realize and maximize the potential
benefits in any given environment. Before
such systems can be promoted, however, we
need to take into account the needs and
constraints imposed by the socioeconomic
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4 C.K. Ong et al.
and policy context. However, a number of
recent books (Franzel et al., 2001; Otsuka
and Place, 2001) discuss these more applied
issues, allowing this book to focus on the
biophysical aspects of interactions in tropical
agroecosystems, and especially their more
elusive below-ground aspects.
1.1.3 Land Equivalence Ratio (LER)
Farmers’ direct interests lie, particularly, in
the ‘production benefit’. The benefit of inter-
cropping is most frequently (Vandermeer,
1989) quantified by the LER, which is
defined as the relative land area in pure
stands that is required to produce the yields
of all products from the mixture. If the LER
>1, then the mixture is more advantageous
than separate monocultures. Of course, the
amount of land used is only one of the pro-
duction factors, which include labour, energy
and total cost. However, multispecies systems
that do not provide a gain in efficiency in
terms of land use have little chance of being
more efficient in these other aspects.
In tree–crop systems (agroforestry), one
component is dominant and perennial.
However, farmers are often not concerned
with maximizing both tree and crop compo-
nents; rather, they are concerned with maxi-
mizing the annual crop’s production whilst
maintaining an acceptable level of growth in
the tree component. Therefore, the produc-
tion benefit can be expressed by I, the yield
advantage of the annual crop component
only (Sanchez, 1995; Ong, 1996; Rao et al.,
1998). It is defined as the increase in crop
yield relative to the yield in monoculture. If
I > 0, then the agroforestry system is, in
terms of crop production, more advanta-
geous than the monoculture.
1.2 Separating Positive and Negative
Interactions
‘Interaction’ refers to the influence that one
or more components of a system has on the
performance both of another component of
the system and of the overall system itself
(Nair, 1993). Several classifications of interac-
tions can be made, depending on the context
and upon one’s view. Besides an ecological
classification, based on the net effect (posi-
tive, nil or negative) of each component
(Anderson and Sinclair, 1993) and the agro-
nomic partition between above-ground and
below-ground interactions, more mechanistic
classifications can be made. In terms of time,
a distinction can be made between direct (i.e.
instantaneous) and indirect interactions.
In the case of indirect interactions, a
time period exists between the cause (e.g.
depletion of soil water whilst that water
supply is ample) and the result. So, the
effect only becomes apparent later in the
season when there is a shortage of water.
According to the number of components
involved, a distinction can be made in
terms of two-way, three-way, etc. interac-
tions. A two-way interaction involves two
components (e.g. in a specific ecozone, the
presence and the characteristics of one
plant component may influence the pro-
duction of another plant component). A
three-way interaction involves three com-
ponents, in which a two-way interaction in
its turn interacts with a third component
(e.g. in a broader context, in several eco-
zones, the influence of one plant compo-
nent on another plant component may in
turn be influenced by the environment).
1.3 Assessing Plant–Environment–Plant
Interactions
Insight into plant–environment–plant inter-
actions can be obtained using different
approaches. This section describes: (i) the
separation of simple effects; (ii) the use of
resource capture concepts; and (iii) the use
of a resource balance concept.
1.3.1 Separating simple effects
The net effect of one plant component on
another plant component must be the result
of positive (i.e. ‘fertility’) effects and nega-
tive (i.e. ‘competition’) effects. So, one
approach by which we may obtain insight
into this area is to separate and quantify
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Ecological Interactions in Multispecies Agroecosystems
these effects. This idea was formalized in the
following equation (Ong, 1995):
I=F+C (1.1)
where I is the ‘overall interaction’ (i.e. the
percentage net increase in production of one
component attributable to the presence of
the other component); F is the fertility effect
(i.e. the percentage production increase
attributable to favourable effects of the other
component on soil fertility and microcli-
mate); and C is the competition effect (i.e.
the percentage production decrease attribut-
able to competition with the other compo-
nent for light, water and nutrients).
However, positive and negative compo-
nent effects are highly site specific, and
change with the environment (see Sanchez,
1995). Therefore, the insight gained with
this approach does not contribute greatly to
a predictive understanding applicable to a
broad context, and thus to other situations.
After a modification by Ong (1996), the
equation evolved (Rao et al., 1998) to give
the following:
I=F+C+M+P+L+A (1.2)
where F refers to effects on chemical, physi-
cal and biological soil fertility, C to competi-
tion for light, water and nutrients, M to
effects on microclimate, P to effects on pests,
diseases and weeds, L to soil conservation
and A to allelopathic effects.
The advantage of Equation 1.2 is that it
provides a comprehensive overview of the
possible effects involved. However, as
emphasized by those authors, many of these
effects are interdependent and cannot be
experimentally estimated independently of
one another. Such interdependence is a seri-
ous drawback because, as a result of the
overlap, quantification of the individual
terms will most probably give a sum that
exceeds I. Therefore, the equation cannot
help one determine the relative importance
of each term for a given system. Another
drawback is that the interaction with the
environment is not explicitly stated in the
equation, but is rather implicitly contained
in each term. In other words, Equation 1.2
approaches I as a two-way interaction
between two plant components. For a pre-
5
dictive understanding applicable to other
ecozones it would be preferable if I were to
be approached as a three-way interaction,
making the influence of the environment
explicit.
Cannell et al. (1996) attempted to clarify
the resource base of this equation. They
argued that part of the ‘mulch’ effect of a
tree is derived from light, water and nutrient
resources, which the tree acquired in com-
petition with the crop (Fcomp). Another part
of the mulch effect may result from the fact
that the tree can exploit resources that the
crop cannot (Fnoncomp). Similarly, a propor-
tion of the resources acquired by the tree in
competition with the crop is recycled within
the system, and may thus be used by a
future crop (Crecycl). If Fcomp were based on
the same resources as Crecycl, then in the long
run the two terms would cancel each other
out. The question of whether or not a
tree–crop combination gives yield benefits
therefore depends on: (i) the complementar-
ity of resource use; (ii) the value of direct
tree products – specifically those obtained in
competition (Cnonrecycl) relative to the value
of crop products that could have been pro-
duced with these resources; and (iii) the effi-
ciency with which tree resources are
recycled into crop products, a point specifi-
cally true for those resources obtained in
competition with the crop (Crecycl).
The main advantage of Ong’s method is
its simplicity with regard to quantifying sys-
tem performance as the result of a few main
effects, which can be directly measured with
a relatively simple experimental setup. But,
there are disadvantages. The first is the lack
of a timeframe. The assumption of Cannell et
al. (1996) that Fcomp = Crecycl may be true
once the system has reached equilibrium in
the long term. However, before that stage,
the fertility effect is more prone to delays
than the competition effect, because of slow
or low liberation of available nutrients from
recycled material. Thus in the first few years,
which are important for the assessment of
the technology by the farmer, Fcomp < Crecycl,
and there is a strong possibility that I will be
negative. The equation does not allow for
delayed effects, although it can be modified
to include a short-term and long-term fertil-
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6 C.K. Ong et al.
ity effect. Van Noordwijk et al. (1998a) esti-
mated the terms of such a modified equa-
tion, by including a treatment based on the
removal of the tree and quantification of
‘residual fertility’ effects. Under such condi-
tions, these long-term fertility effects were
substantial, but so was the competition term.
Another disadvantage of the direct
empirical approach is that the agroforestry
system performance results of this equation
cannot be transferred from one environment
to another. Kho (2000a) developed a
method to overcome the latter disadvantage
of Ong’s equation (see Section 1.3.3 below,
‘The resource balance concept’). His method
allows for the transfer of the performance
results of a specified system from one envi-
ronment to another, and is based on the
sum of positive and negative factors similar
to that used by Ong.
However, Kho’s method can be used
quite easily in a qualitative way, and com-
plements Ong’s method in terms of the
transfer of performance results from one
environment to another. The use of both
methods together may give a reasonable
idea of why systems involving tree–crop
interactions perform as they do. However,
even if the two methods are used to comple-
ment each other, there are still limitations to
their usefulness. Kho (2000a) noted that his
method focuses on resource–use interactions
and is not applicable if pests, diseases or
allelopathy (caused by the tree component
of the system) are important factors deter-
mining the system’s performance.
Neither Ong’s nor Kho’s method has a
timeframe, and a timeframe is necessary to
take into account delayed effects (such as
those mentioned above) and long-term
trends. Thus, an important aim of agro-
forestry in general is not addressed: the
methods may show that a certain agro-
forestry system works better in certain envi-
ronments than does a sole crop, but this
does not mean that such a system is really
sustainable over a longer period.
Another feature not covered by these
methods is the performance of a tree–crop
system that is highly dependent on interac-
tions between factors; thus, a simple sum of
positive and negative factors is not going to
give the right result. An example of this is
water–P interaction in P-fixing soils, in
which P-transport to roots is decreased by
decreases in soil water content. Decreases in
soil water content by trees affects the envi-
ronmental factor p, thus necessitating a W*p
term in Kho’s equation.
In cases where long-term performance
and interaction of tree factors and environ-
mental factors are important, mechanistic
research may be necessary to explain the
functioning of the system, in order to under-
stand its performance and be able to extrap-
olate that performance to longer time
periods or to other environments. However,
mechanistic research suffers from its own
pitfalls. An important one is a loss of overall
understanding as a result of focusing on one
or two factors. Another related pitfall is the
risk of getting lost in a multitude of detailed
processes, without realizing that only a few
factors may really play an important role in
determining 80–90% of a system’s perfor-
mance in a certain environment.
These pitfalls of mechanistic research
may, in turn, be (partly) overcome by start-
ing to look at the system from the perspec-
tive of Kho’s method. The first question we
should ask is ‘what are the main limiting
factors in a certain environment (including
pests and diseases)?’ The second question is
‘how do trees and crops influence each
other in general (including influences
through mechanisms like allelopathy) and
particularly via limitation of the main
resource?’ Using Kho’s method to look at
the main environmental resource limitations
and the effects trees have on the different
resources, it is possible to prioritize the
mechanisms that need to be looked at in
more detail. In this way, the use of system-
performance analysis methods can be a first
step in determining the priorities for mecha-
nistic research.
1.3.2 Use of resource capture concepts
One plant component may influence
another by changing its capture of the most
limiting resource. Another approach by
which we may gain insight is, therefore, by
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Ecological Interactions in Multispecies Agroecosystems 7

modelling the capture of the limiting
resource in a multispecies system. Biomass
production (W) is the product of such cap-
ture, and the efficiency with which the cap-
tured resource is converted into biomass
(Monteith et al., 1994; Ong et al., 1996):
W = εconversion  Capture (1.3)
where εconversion is the conversion efficiency
and Capture the capture of the specific
resource.
Two assumptions are usually made when
using this approach. First, the conversion
efficiency is usually considered to be species-
specific and conservative, which justifies the
use of empirically determined efficiencies.
Secondly, because biomass production W is
calculated from Capture it is regarded as the
‘dependent’ variable responding to Capture,
which is the ‘independent’ variable. These
assumptions rely on the premise that the
resource under consideration is the only
limiting resource and that all other growth
resources are in ample supply. In this spe-
cific case, the conversion efficiency is con-
stant at its maximum value (Kho, 2000a),
and the response of the plant can be entirely
attributed to the increased capture of the
resource being considered.
If other resources are also limiting (i.e. if
the response curve is a smooth curve reach-
ing a plateau gradually), the assumptions are
no longer valid. First, theoretical as well as
empirical evidence shows that increased limi-
tation of other resources will decrease the
conversion efficiency of the resource in ques-
tion (Kho, 2000a). The conversion efficiency
of nutrients equals (in the absence of nutri-
ent losses from the plant) the reciprocal of
the nutrient concentration in the plant. For
nitrogen, phosphorus and potassium, the
maximum concentration can be two to three
times the minimum concentration (Van
Duivenbooden, 1995), which shows that
conversion efficiencies are not at all conserv-
ative. In a dataset of radiation conversion
efficiencies (Azam-Ali et al., 1994), 72% of
the total variance was found to be attributed
to the environment and only 10% to species,
which indicates that conversion efficiencies
are determined more by environment than
by species. Secondly, increased capture of
one resource will always be accompanied by
increased capture of other resources. If sev-
eral resources are limiting, increased capture
of other resources must also contribute to
production, and it is not clear whether, or to
what extent, increased capture of the
resource under consideration is the cause or
the effect of increased biomass production.
Therefore, Kho (2000a) argued that the rela-
tion between production and capture is a
correlation, not a causal relation.
An approach that uses Equation 1.3 is
thus methodologically sound only if a strict
‘law of the minimum’ is applicable.
However, this is a theoretical idealization
that is, in reality, seldom true. In most envi-
ronments, a crop responds to the increased
availability of several resources, having for
each resource a smooth response curve
gradually reaching a plateau (de Wit, 1992)
(Box 1.1). Limitation is thus indicated more
by a point on a gradual, continuous scale
rather than by a discrete yes/no variable (see
Kho, 2000a, and the next section). One rea-
son for this is that plants have a certain plas-
ticity, which allows them to adapt their
architecture in order to acquire the most
limiting resource (Chapter 4), thereby mak-
ing that resource less limiting. Another rea-
son why a strict ‘law of the minimum’
occurs so seldom is that, with an increasing
timescale (from hours to seasons and

Box 1.1. General principles on limiting resources and capture.

1. Limitation does not involve only one resource that, if saturated, is replaced by another resource.
Usually several resources are limiting, in which case the relationship between biomass production
and the capture of a single resource should be viewed as a correlation, not a causal relation.
2. The variation in conversion efficiencies between environments is larger than that between species,
which shows that conversion efficiencies are determined more by the environment than by species.
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8 C.K. Ong et al.
beyond) and/or space (from a single plant
organ to a field and beyond), the response
curve is the sum of several individual
response curves. Even if the latter are
Blackman-type curves, this composite curve
is, because of temporal and spatial hetero-
geneity, smooth (Kho, 2000a).
For the study of plant–environment–
plant interactions, de Wit’s approach is quite
relevant, because plants alter the availability
of several resources simultaneously and
will, therefore, alter conversion efficiencies
by changing resource limitations. Moreover,
the ‘most limiting’ resource for a plant in
monoculture is not necessarily the ‘most
limiting’ resource for a plant in a multi-
species system.
The above methodological weakness for
predicting biomass production in multi-
species systems may be avoided in two dif-
ferent ways. First, empirically obtained
efficiencies should not be used as parameters
(constants) in process-based models. Instead,
efficiencies should be studied and modelled
in relation to availabilities of the other
resources, and treated as a variable in
process-based models. Secondly, dynamic
simulation models for different resources
can be linked. These models should operate
at such a small (detailed) scale that, in the
integration step, Equation 1.3 can be
Production
W
0
0 A
Resource availability
Fig. 1.1. Response curve of biomass production in relation to availability of a certain resource (all other
factors equal) with slope (∂W/∂A) and use efficiency (W/A) for a specific environment (●).
replaced by a more realistic model (involv-
ing the capture of several resources). This is
an enormous challenge. Until it is accom-
plished, however, the present models can
give a mechanistic insight into the resource
flows in a system and may be helpful in
terms of evaluating the relative influence of
alternative multispecies designs (species
combinations, temporal and spatial arrange-
ments, etc.) on resource flows.
1.3.3 The resource balance concept
One plant influences another by changing
the availability of several resources in the
environment of the other. The effect on pro-
duction depends on the degree to which the
resources concerned are limiting (Fig. 1.1).
In an environment where the resource is
not limiting (right in Fig. 1.1), a change in
availability does not have much of an influ-
ence on production (all other factors being
constant). The more a resource is limiting
(to the left in Fig. 1.1), the greater its influ-
ence. Limitation of a resource can be defined
as the ratio between the slope of the
response curve and the use efficiency of the
resource (Kho, 2000a):
∂W / ∂A
L= (1.4)
W /A
∂W
∂A
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Ecological Interactions in Multispecies Agroecosystems
where L = limiting factor, W = biomass, and
A = availability.
On the plateau, the slope equals zero; thus,
the minimum value of limitation L equals
zero. Near the origin, the slope equals the
use efficiency, so that the maximum value of
limitation L equals one. By rearranging
Equation 1.4 it is clear that, for small
changes, the relative change in production
(∆W/W) equals the relative change in avail-
ability (∆A/A) multiplied by the limitation L
(all other factors being equal).
Each specific environment has, for a
particular species, its own balance of avail-
able resources, and can be characterized by
a set of response curves (Fig. 1.1; one
curve for each resource) on which the
environment concerned occupies a certain
point. Therefore, for a particular species,
each specific environment can be charac-
terized by the set of limitations Li for each
resource i. Kho (2000a) showed that the
limitations of all resources (CO2, radiation,
water and all nutrients) most probably
total one:
n i =1
∑L
i =1
i =1 (1.5)
That is, if for a particular species in a specific
environment the limitations of some
resources are known and add up to one, it
can be inferred that all other resources are
not limiting. Alternatively, if the sum is less
than one, it can be inferred that other
resources are still limiting. A rough approxi-
mation of limitations can be obtained by
analysing publications reporting use efficien-
cies and response to changed availability
(see Kho, 2000a).
In general, a plant component does not
change the availability of only one resource
in the environment of another plant compo-
nent; rather, it changes the availability of
several resources (light, water, nitrogen,
phosphorus, etc.). How does this influence
production? If the availability of several
resources changes simultaneously (e.g. lead-
ing to increases and/or decreases in avail-
ability), is biomass production then
determined only by the (change in) avail-
ability of the most limiting resource? Or, by
that of all limiting resources?
9
Within the temperature range at which a
crop species can grow and reproduce
(roughly from 0°C to 35°C for temperate
species and from 10°C to 45°C for tropical
species; Ong and Monteith, 1985), crop dry
matter production (W) in a specific environ-
ment is a function of resource availability:
W = f ( A1 , A2 , ... , An ) (1.6)
where Ai is the availability of resource i and
n is the number of all resources. Let z denote
an arbitrary management option that alters
resource availabilities (some resources may
be altered positively, others negatively, some
by much, others less or not at all).
For the sake of argument, we will tem-
porarily assume that the management
option used can be applied gradually, using
many small steps; but in practice this is not
essential. The effect of the management
option on production can be found by differ-
entiating Equation 1.6 with respect to z.
According to the chain rule:
n
∑ ∂∂AW ⋅
dW = dAi
dz dz (1.7)
i
Multiplying both sides by dz, and expressing
the differentials relative to their original
value (i.e. dividing both sides by production
W and multiplying the right-hand side by
Ai/Ai) gives:
n
∑ ∂∂AW
dW = Ai dA
× i (1.8)
W i W Ai
i =1
Substitution of Equation 1.4 yields:
n
∑L
dW dAi
= i × (1.9)
W Ai
i =1
which shows that, for small changes, the rel-
ative change in production (∆W/W) equals
simply the sum of the relative changes in
availability (∆Ai/Ai) multiplied by their limi-
tation Li.
Biomass production is not determined by
the (change in) availability of only one
resource (e.g. the most limiting) but by all
the limiting resources. The contribution each
resource makes to the relative change in pro-
duction is proportional to both its degree of
limitation and its relative change in availabil-
ity. This result is the basis for the framework
considered in the next section of this chapter.
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10 C.K. Ong et al.

1.4 A Framework for a Predictive
Understanding of Multispecies Systems
With regard to growth resources, one plant
component can have many effects on
another plant component in a multispecies
system (upper half of Fig. 1.2). A given
multispecies system with a given manage-
ment system has a particular canopy and
root architecture in time and space. The
mixed canopy architecture (leaf area index
and extinction coefficients of each plant
component in different layers) and root
architecture (root length densities of each
plant component in different soil layers)
determine the relative ability of each plant
component to acquire resources from their
shared environment. For each plant compo-
nent, this ultimately results in net effects on
the availability of resources. For one plant
component, the relative net change in the
availability of resource i equals:
∆Ai Ai ;multi − Ai ;mono
Ti = = (1.10)
Ai Ai ;mono
where Ti is the relative net change in avail-
ability of resource i because of the other
plant component, Ai;multi is the availability of
resource i to the plant component concerned
in the multispecies system and Ai;mono is that
in the monoculture.

Simple + shade − temperature + mulch/litter + N2-fixation

tree effects − PAR + RH + SOM + root decay
− weeds − windspeed − soil bulk density + deep capture
+ rain interception − vapour pressure deficit + dry deposition
+ microbiological activity − runoff ± erosion
+ water holding capacity + mineralization + root competition

+
+ +
− −
−
Altering (the balance of)
resource availabilities
to the crop
light water N P .

Tree effect on crop production

Fig. 1.2. Trees influence crop production by altering the balance of resources available to the crop (light,
water, N and P). The height of each shaded area relative to the height of the rectangle represents the relative
change in the availability of the resource (Ti). The width of each shaded area relative to the total width
represents the limitation of the resource in the tree–crop interface (Li). The sum of positive and negative
shaded surfaces relative to the total surface of the rectangle represents the overall tree effect I expressed as a
fraction of sole crop production. PAR, photosynthetically active radiation; RH, relative humidity; SOM soil
organic matter. (Adapted from Kho et al., 2001.)
Below-ground - Chap 01 21/4/04 10:14 Page 11

Ecological Interactions in Multispecies Agroecosystems 11

Because these coefficients are determined established simultaneous agroforestry sys-

by the mixed canopy and root architectures
they are probably ‘conservative’ when applied
to a particular multispecies system, soil depth
and slope. They most probably serve as key
characteristics of the particular multispecies
system (with one for each plant component
set), but this is a subject for further study.
When a particular multispecies technol-
ogy is placed in a specific environment (in
terms of soil, climate and topography), it
interacts with that environment. If we
approximate the differentials in Equation
1.9 by differences and substitute the defini-
tion of I and Equation 1.11 into it we may
expect for I (Kho, 2000b; Kho et al., 2001):
n availability may also become less negative or
I= ∑L
i =1
i × Ti
Equation 1.11 is represented graphically in
the lower half of Fig. 1.2. Note that Equation
1.11 only considers interactions related to
growth resources. Allelopathy and effects
caused by damage by pests and diseases fall
outside its scope. Therefore, Equation 1.11
may be extended to:
 n  the smaller its limitation (see Equation 1.4,
I =
 ∑
 i =1
Li × Ti  +P+ A


where A is the relative change in production
because of allelopathic effects (A≤0) and P is
the relative change in production (positively
or negatively) because of the influence of the
multispecies system on pests and diseases. P is
also a function of technology and of the envi-
ronment. If there are no sources of pathogens
in the environment, P will be zero.
Equations 1.11 and 1.12 explain the pro-
duction benefit associated with a multi-
species system at a certain state (time and
maturity). The relative net effects on
resource availability (Ti) may change when
the system grows to maturity. In a newly
tem, competition for light may be relatively
low, resulting in a negative effect close to
zero. However, the rooting system of the
trees is still superficial, resulting in low (neg-
ative) net effects on water and nutrient avail-
ability. As the system matures, the canopy
and the rooting system of the trees develop.
The amount of light available to the crop
decreases (the net effect becomes more nega-
tive). The net effects on water availability
may become either less negative (as a result
of less competition) or positive (if the bene-
fits offered by a more favourable microcli-
mate and soil physical properties outweigh
competition). The net effect on nutrient
(1.11) positive (as a result of less competition and
increased nutrient cycling). On sloping lands,
the potential benefit of water and soil con-
servation is greater than on a flat surface. So,
the increase with maturity of the net effects
on water and nutrient availability may be
stronger on sloping lands.
The more a resource becomes available in
the environment of a multispecies system,
(1.12) Fig. 1.1 and Box 1.2). The more other limit-
ing resources become available in the envi-
ronment of that multispecies system, the
smaller their limitation (see Equation 1.5).
Combined with Equation 1.11 this leads to
two rules (see Box 1.2) that can be viewed
as counterparts to classic principles of crop
production (Kho, 2000b).
These rules are helpful both for predicting
the performance of a multispecies technology
when it is extended to another environment
and for developing a multispecies technology
(Kho, 2002). For example, Kho (2000b)
showed that, with regard to alley cropping
technology, the net effect that trees have on
the availability (to the crop) of light, water

Box 1.2. Simple rules for predicting the performance of multispecies systems.

Rule 1. The greater the availability of a resource in the environment of a multispecies system, the
smaller its relative importance in the overall interaction.
Rule 2. The greater the availability of other limiting resources in the environment of the multispecies
system, the greater the relative importance of a resource in the overall interaction.
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12 C.K. Ong et al.

and phosphorus is most probably negative,
whereas for nitrogen it is most probably posi-
tive. Consequently, in a (sub-)humid climate
on nitrogen-deficient soils, the overall effect
of alley cropping will most probably be posi-
tive, because of the positive nitrogen effect
and the negative net effects on other
resources (Fig. 1.3a). In the same climate,
but on acid soils, phosphorus is relatively less
available; this will increase the negative
phosphorus effect (Rule 1) and decrease the
positive nitrogen effect (Rule 2), resulting in
a negative overall effect (Fig. 1.3b).
When designing and developing a multi-
species technology, we want to increase the
share of positive net effects and decrease the
negative net effects. This may be done in
one of two ways. First, in the design phase,
we can try to make the net effects on
resource availability (Ti) both positive and as
large as possible. This can be done by choos-
ing the right species combinations, the right
temporal and spatial arrangements and the
right management techniques, which are a
unique part of the technology (e.g. prun-
ing). Herewith, process-based models may

(a) N-deficient soil (b) Acid (P-deficient) soil

+ +

− −
− − − −

R W N P R W N P

I = +23% I = −17%

(c) N-deficient soil + N fertilizer (d) Acid (P-deficient) soil + P fertilizer

+ +

− −
− − − −

R W N P R W N P

I = −27% I = +13%

Fig. 1.3. Possible tree effect balances of alley cropping technology in a humid climate (a) on nitrogen-
deficient soils; (b) on acid (phosphorus-deficient) soils; (c) on nitrogen-deficient soils with nitrogen fertilizer
being provided to the alley crop and the sole crop; and (d) on acid soils with phosphorus fertilizer being
provided to the alley crop and the sole crop. The relative net tree effects on availability of each resource (Ti)
are equal in (a)–(d); only the environment (i.e. resource limitations, Li) changes explain the different overall
effects (I ). R, radiation; W, water; N, nitrogen; P, phosphorus resources. (Source: Kho, 2002.)
Below-ground - Chap 01 21/4/04 10:14 Page 13
Ecological Interactions in Multispecies Agroecosystems
be very helpful. These models should thus
be built in such a way that the effect these
factors have on (relative changes in)
resource availability can be evaluated easily.
Note that relative changes in availability are
sufficient to explain a relative change in pro-
duction (Equations 1.9 and 1.11). Therefore,
absolute values of availability are not neces-
sary, and the models are allowed to give pre-
dictions of availability that are based on one
or more constant multiplication factors.
With the calculation of the relative net
change (Equation 1.10) the multiplication
factors appear in the numerator and denom-
inator and vanish from the equation. This
property may thus reduce the effort neces-
sary to produce such a model.
The second way to increase positive net
effects and decrease negative effects involves
the following. In the development phase, we
can increase the limitations (Li) of the posi-
tive net effects and decrease those of the neg-
ative net effects by choosing appropriate
management options that are not unique to
the technology, but that can be applied to
both a multispecies system and a monocul-
ture. Management options can be translated
into effects on the availability of resources,
which allows one to manipulate the share of
the different resources in the overall interac-
tion. For example, with regard to alley-crop-
ping technology, options such as phosphorus
fertilization, water-conserving tillage and/or
weeding of superficially rooting weeds are
probably appropriate. These management
options will increase the availability of phos-
phorus and water, and thus will reduce the
negative phosphorus and water effects (Rule
1) and increase the positive nitrogen effect
(Rule 2). To illustrate this, compare Fig. 1.3b
and 1.3d in terms of the effect that phospho-
rus fertilizer has when applied to both an
alley-cropping system and a monoculture. On
the other hand, external inputs of organic or
inorganic nitrogen are probably inappropriate
in such systems, because they will reduce the
positive nitrogen effect (Rule 1) and increase
the share of the negative effects (Rule 2; cf.
Fig. 1.3a and 1.3c).
Simply being able to identify as positive
or negative (+ or ) the net effects that
plant components have (in terms of the
13
availability of resources) on another, spe-
cific, plant component (TI) can be very use-
ful. In this sense, even very limited
knowledge can be helpful for the prediction
of overall interaction and the development
of multispecies systems, in a qualitative
sense. Fortunately, much of this information
is already available, hidden in the literature
on this subject. Kho (2000b) developed rules
(see Box 1.2) to ‘reveal’ this information. By
analysing the direction of the change of I, in
response to a change in the availability of a
resource (when all other factors remain con-
stant), the sign of the net effect on this
resource can be derived (Fig. 1.4).
For example, suppose that a particular
agroforestry system has an I equal to +5% in
a season with good rains, but an I equal to
25% in a season with poor rains. So, with
decreased water availability, the overall
interaction decreased. According to Fig. 1.4,
the net effect that trees have on water avail-
ability is probably negative (TA < 0), while
the net effect trees have on another resource
is probably positive (TB > 0). Because I was
positive, the last statement (e.g. that there is
a positive net effect on the availability of
another resource) is most probably true.
However, I changed its sign, so we can be
sure that the net tree effect on water avail-
ability in this particular system is negative.
The net effects that plant components
have on resource availability (Ti) can easily
be empirically quantified. The availability of
a resource to a crop in a multispecies system
and to a crop in monoculture are estimated
and Equation 1.11 applied. Our interest lies
not in absolute values of availability, but in
relative changes in availability; hence, it is
immaterial if the estimations of availability
are biased with constant multiplication fac-
tors (Kho et al., 2001).
When quantifying the limitations (Li) we
have to consider certain factors.
Approximation of the differentials of
Equation 1.9 resulted in Equation 1.11. This
approximation is justified for small reductions
in availability. However, especially in agro-
forestry systems, one plant component (the
tree) may greatly influence resource availabil-
ity to the other plant component (the crop).
The limitations for the crop in the agro-
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14 C.K. Ong et al.

The availability of resource A

decreases increases

If I decreases I increases I decreases I increases

(more neg.) (more neg.)

then‡
TA < 0 TA > 0 TA > 0 TA < 0
TB > 0 TB < 0 TB < 0 TB > 0
If I changes in sign

If a positive I a negative I a positive I a negative I

becomes becomes becomes becomes
negative positive negative positive

then
TA < 0 TA > 0 TB < 0 TB > 0

TA refers to the net effect on changed resource; TB to that of another limiting resource.
‡ Both statements may be true. However, if I is negative, the statement with the negative T value is

most meaningful; if I is positive, the one with the positive T value is most meaningful.
If the overall interaction I changes in sign, then certainty about the net effects is given.
Fig. 1.4. Diagram used to derive the sign of the net effect on availability of a resource (other factors being
equal). (Adapted from Kho, 2000b, with permission from Elsevier.)

forestry system may thus differ from the limi-
tations for the monoculture, and the appro-
priate limitations for use in Equations 1.11
and 1.12 must be somewhere in between the
values in the two systems. To be consistent,
the partial derivatives in the limitation
(Equation 1.4) should also be approximated
with the right variations of the same order.
For details and an example of the quantifica-
tion of Equation 1.12, see Kho et al. (2001).
1.5 Conclusions
In this chapter, using experience gained in
agroforestry research, we have used specific
concepts and simple rules to explore how
and where multispecies agroecosystems may
be able to improve the use of growth
resources. It is clear that simple rules (Box
1.2) are helpful both for predicting the gen-
eral performance of a multispecies technol-
ogy when it is extended to another
environment and for developing a multi-
species technology. For more subtle interac-
tions, however, it will be necessary to use a
combination of simple rules and a process-
based model. For example, Radersma (2002)
demonstrated, on a P-fixing Oxisol in west-
ern Kenya, that a 2–3% decrease in soil
water content as a result of the influence of
associated trees may cause a 30–40%
decrease in maize production. In such situa-
tions, trees are likely to affect crop growth
by inducing P deficiency through drying the
soil. Further understanding of the processes
underlying multispecies ecosystems are
needed in order to evaluate their relative
importance at the ecosystem and landscape
levels (which are described in other chapters
of this book).
It should also be pointed out that we
have drawn our evidence from the limited
number of species (usually two or three)
currently used in agroforestry research.
More progress is needed in the development
of the theory and concepts dealing with how
the number and composition of plant species
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Ecological Interactions in Multispecies Agroecosystems 15

influence ecosystem processes before we can
extrapolate them to more complex systems.
Recent advances in theoretical models based
on simple but well-known mechanisms of
interspecific competition may provide
important new insights. For example, the
models developed by Tilman and Lehman
(2001) support the long-standing hypothesis
that the number of species in a community
may increase overall productivity, resource
use and stability. However, they pointed out
that traits that allow species to coexist when
exploiting and competing for limited
resources do not automatically give rise to
greater productivity or stability (because
these interactions are also highly dependent
on species composition). See Chapter 4 for
more discussions of the importance of
species diversity and ecosystem perfor-
mance. Finally, our current understanding of
how multispecies agroecosystems function
should be integrated into the enormous
wealth of local ecological knowledge known
to exist (see Chapter 2, this volume).

Conclusions

1. Well-chosen multispecies agroecosystems are probably more productive and sustainable than the
best-performing monocultures. However, the evidence for this is not yet conclusive.
2. The drawbacks of multispecies systems include lower yields in annual crops (because of higher
investments in vegetation structure) and a long wait for trees to mature and yield products.
3. Simple rules for predicting the general performance of multispecies systems exist, including rules
for predicting the balance between above-ground and below-ground resource-use limitations.
4. For the prediction of a more specific level of performance, it is necessary to combine simple rules
with process models.

Future research needs

1. How important are the number of species and species composition in determining overall produc-
tivity and stability?
2. How important is ecosystem structure in determining multispecies-agroecosystem function?
3. How can we incorporate local ecological knowledge into the scientific rules and concepts associ-
ated with modellers’ ecological knowledge?