Ecol Res (2010) 25: 723–732

DOI 10.1007/s11284-009-0658-6

SPECIAL FEATURE Plant responses to heterogeneous environments

Maureen C. Kennedy

Functional–structural models optimize the placement

of foliage units for multiple whole-canopy functions

Received: 30 March 2009 / Accepted: 26 September 2009 / Published online: 5 November 2009
Ó The Ecological Society of Japan 2009

Abstract I present examples of plant functional–struc-

tural models (FSMs) that are used to evaluate how foliage
Introduction
units affect whole-canopy functions, and I show that
Plant morphology is the consequence of many processes;
multi-criteria optimization is an effective tool for these
these include the production of foliage units and asso-
models. FSMs produce plant structures through the
ciated bifurcation, hormone regulation, carbon alloca-
repeated application of a set of rules for the placement of
tion, and the influence of the microenvironment on the
foliage units. The models are blind (rules are the same
plant. The observed morphology of a plant emerges
regardless of dynamic simulation conditions), sighted
from the cumulative activity over the plant lifespan of
(rules change with interference from other foliage units) or
individual foliage units such as the metamer (a unit that
self-regulatory (rules change depending on the conditions
includes an internode and associated buds, and leaf at
of the simulation, i.e., internal conditions). In the exam-
the distal end; Room et al. 1994), and their local archi-
ples presented, the models are used to optimize plant
tectural patterns (Table 1). The ultimate function of a
morphology for one or more measures of plant perfor-
plant is sustained growth and reproduction (which are
mance; these measures include movement of materials
correlated with a plant’s lifetime fitness), and in order to
and associated hydraulic functions, foliage display, light
achieve sustained growth, a plant’s foliage units combine
interception and net carbon, mechanical support and
to perform multiple tasks, including movement of
stability, and reproductive success. It is consistently found
materials and associated hydraulic functions, foliage
that no morphology is optimal for any single measure of
display, light interception and net carbon, mechanical
plant performance, and the rules for plant development
support and stability, and reproductive success (Niklas
are not stationary in space and time. In multi-criteria
1997a, 1997b; Pearcy et al. 2005). The relative impor-
optimization, alternative morphologies are compared
tance of each of these tasks on ultimate plant survival, as
against multiple measures of plant performance; these are
well as the morphological characteristics that relate to
optimized simultaneously using Pareto optimality, which
improved plant performance (e.g., leaf inclination an-
yields the set of mutually co-dominant solutions not
gles, clumped vs. uniform foliage distribution), would be
dominated by any other solution. Two solutions are
expected to vary among plants in different environments
considered to be mutually co-dominant if improvement
as well as throughout a plant’s life history (Niinemets
with respect to one criterion is at the expense of another
2009). In this sense, the ability of the plant to perform
criterion. I conclude that multi-criteria optimization is an
with respect to multiple tasks may be constrained. For
essential tool for the use of FSMs to relate processes at the
example, in the old-growth forests of the Pacific
foliage level to whole-canopy function and to explain the
Northwest, USA, large old trees exhibit a size limitation
structural diversity of old-growth forests.
(Ishii et al. 2000), which is possibly due to constraints in
the ability to transport materials effectively (e.g.,
Keywords Functional–structural models Æ
hydraulic limitation; Ryan and Yoder 1997) or increased
Optimization Æ Multiple criteria Æ Morphology Æ
maintenance respiration (Grier and Logan 1977). In
Architecture
contrast, a shaded understory plant is likely constrained
by its ability to intercept light. The role of plant mor-
M. C. Kennedy (&) phology in the tasks of plant growth must be considered
School of Forest Resources, University of Washington,
Box 352100, Seattle, WA 98195-2100, USA in the context of these varying constraints. In particular,
E-mail: mkenn@u.washington.edu there may exist negative trade-offs among plant func-
Tel.: +1-206-7327810 tions (Kennedy et al. 2009); a canopy design that
Fax: +1-206-7327801

724
Table 1 Description of terms used
Term
Hierarchy of plant form Morphology
Architecture
Foliage units
Types of modelsa Blind
Sighted
Self-regulatory
Basic architectural Bifurcation
parameters
h: branching angle (2D),
rotation angle (3D)
Lrat: length ratio
Internode length
Other terms Constraints
Suppressed buds
a
After Bell (1986)
performs best with respect to light interception may not
be the most mechanically sound. Therefore one must
consider how local-scale architecture affects both plant
morphology and the many tasks involved in achieving
sustained growth; these must also be considered in the
context of environmental factors and plant life history.
The clear relationship between plant form (morphol-
ogy) and function makes it tempting to evaluate which
plant morphology (and underlying local-scale architec-
ture) is ‘‘optimal’’ with respect to plant function. In
practice, this is a difficult task. For which function(s) of
plant growth will you optimize plant morphology? Do
you maximize light interception, or minimize water loss,
or minimize mechanical load? Even an aggregate measure
such as reproductive success or fitness is complicated by
the varying, often conflicting, importance of the major
plant tasks that contribute to reproductive success. Fur-
thermore, it is not clear how to calculate a single measure
from the multiple tasks a plant must perform in order to
sustain growth. Even if a single task is chosen to be
optimized, the researcher must reconcile the naı̈ve notion
of the existence of a single optimal morphology with the
vast biodiversity among plants that co-exist in similar
environments. Such diversity reflects differentiation
among species in how they accomplish major tasks of
plant growth (Ishii and Asano 2009). It is in the context of
these two issues (which task to optimize, and the existence
of multiple morphologies under similar conditions) that
most optimality studies fail. Optimality should be con-
sidered under the assumption that plant species contend
with multiple developmental, structural, physiological
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Description
Broad-scale, overall gross form of a plant canopy or branch
Local patterns of foliage unit production, defined by the
architectural parameters
A single unit upon which a plant is built, either a metamer,
or a conifer shoot
Production of foliage units is controlled by simulation
rules, with no dynamic interactions
Production of foliage units may be modified by dynamic
interactions with other foliage units (within and between
plants)
Placement of foliage units varies with dynamic conditions
of the simulation, including internal control
The mean number of foliage units produced by a parent
foliage unit
The angle between a parent foliage unit and the lateral
foliage units that it produces
The ratio in length between a parent foliage unit and the
lateral foliage units that it produces
The distance between foliage units on the same axis
External and internal conditions that may limit perceived
optimal plant performance (e.g., mechanical stability,
hydraulic functioning).
Mersitematic tissue that is reserved beyond the usual timing
of growth, and allowed to be utilized to regenerate foliage
under varying conditions
and environmental constraints simultaneously, and there
is a multitude of solutions to such multi-criteria problems
(Kennedy et al. 2009). In this paper, I describe how to
consider the effect of multiple controlling factors simul-
taneously, which improves the use of single-factor opti-
mality.
Schmitz et al. (1998) propose that multi-criteria
optimization provides a means by which variability in
optimal behavior can be reconciled (e.g., Rothley et al.
1997). The multiple tasks a plant must perform in order
to achieve sustained growth explain the biodiversity
present among organisms in similar ecosystems with
similar requirements (Niklas and Kerchner 1984; Niklas
1997a, 1997b; Niklas 1999), and in the face of multiple
constraints a plant form represents ‘‘adequate design’’
(Farnsworth and Niklas 1995). As in engineering, when
there are multiple design requirements, multiple struc-
tures can meet the requirements equally well (Niklas
1999), although this results in sub-optimal performance
if only a single criterion is optimized. In general, the
conclusion that organisms should optimize is not inevi-
table and optimality studies are best utilized to uncover
the trade-offs that prevent organisms from achieving
optimal states.
In order to evaluate how well a plant performs with
respect to multiple criteria, we require a model to
simulate alternative plant morphologies and to calcu-
late how that morphology affects whole-canopy func-
tion. Plant functional–structural models (FSMs)
provide a promising method to explore the relation-
ship between plant form and function. In FSMs,

biological processes are coupled with spatial repre-
sentation of plant form (Godin and Sinoquet 2005).
Plant FSMs are essential tools to evaluate the
effects of processes at the level of foliage units,
including physiological factors of growth, carbon and
light interception (Kellomäki and Strandman 1995;
Nikinmaa et al. 2003; Allen et al. 2005), the biome-
chanical support required for foliage display (Ford
et al. 1990) and the associated structure required for
water transport (Früh 1997; Pearcy et al. 2005), on
whole-canopy function. These models can be inte-
grated with multi-criteria optimization to help solve
the problem of how plants are able to persist when
subject to many constraints that often conflict.
Functional–structural models provide a virtual laboratory
for plant function–structure relationships
Plant functional–structural models (FSMs) are valuable
as virtual laboratories to evaluate the effect of alterna-
tive local plant architectures on the performance of the
whole canopy. Such manipulations would be difficult, if
not impossible in the field. The processes that are
manipulated by FSMs include architectural parameters
that control branching angles and shoot lengths (Fig. 1)
and physiological processes that control the placement
of new foliage units. Honda (1971) shows that many
distinct plant architectural forms can be simulated with
a simple architectural model that varies in only three
architectural parameters (e.g., Fig. 2). Small changes in
those parameters propagate throughout the branching
structure to result in remarkable variability in plant
Fig. 1 Progress of plant development for a blind model with simple
architectural parameters. Solid lines are foliated shoots, and dashed
lines separate each year’s (or iteration’s) growth. a The model is
initialized with a single foliage structure (shoot 1). b New shoots in
this model are produced through bifurcation, whereby the main
(order 1) axis extends (to form shoot 3) as well as bifurcates to form
two new lateral axes (shoots 2 and 4; these are order-2 shoots). This
is the first architectural parameter, the bifurcation ratio (as defined
by Kennedy et al. (2004), the bifurcation here for the order-1 axis
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725
form. These changes have consequences for canopy
structure and foliage display, which impact the function
of the plant in the forest ecosystem.
I present several examples of FSMs of plant archi-
tecture that fall under the three categories (Table 1)
presented by Bell (1986). In blind models, foliage pro-
duction is controlled solely by the rules that underlie the
simulation, including the architectural parameters, with
no dynamic interactions. In sighted models, foliage
production is dynamic according to interactions with
other foliage units, including those of other plants and
within the same plant. Self-regulatory models vary the
placement of foliage according to the conditions of the
simulation itself, particularly the internal control of
the placement of foliage units. Many of these models
evaluate plant performance with respect to one or more
functions of plant morphology. I present in more detail
recent work by Kennedy et al. (2009) that incorporates
multi-criteria optimization using Pareto optimality with
a FSM of branch development in old-growth Pseudots-
uga menziesii.
Blind models evaluate plant architectural parameters
Optimization studies have shown that changes in a few
architectural parameters (Table 1; Figs. 1, 2) impact
whole-plant function, and values of architectural
parameters that optimize one function may not match
those that optimize another function when they are
considered in isolation. When Fisher and Honda (1977)
evaluated Terminalia morphology with respect to max-
imizing effective leaf area (a measure of foliage display),
(r1) is 3, because three daughter shoots are formed). The lateral
axes are produced at an angle relative to the order-1 axis (the
branching angle h), and the length of the lateral axis is reduced by a
particular ratio relative to the parent order-1 axis (lrat). c These
production rules and architectural parameters are repeated year–
year (or iteration to iteration) until a stopping point is reached.
Shoots 5–8 are all produced in the same year (iteration). In this
model, the bifurcation of lateral axes (order 2) is reduced relative to
the main axis (order 1)

726
Fig. 2 Manipulation of three
parameters (bifurcation, θ = 1.25 r1= 3
branching angle, length ratio) lrat = 0.25 r2= 1
can result in drastically different
plant forms. Branching angle is
expressed in radians, lrat is the
length ratio between shoots of
higher order relative to lower
order, r1 is the bifurcation of
order-1 shoots and r2 is the
bifurcation of order-2 shoots.
The plants differ by values of
architectural parameters
expressed at the level of
individual foliage units (i.e.,
shoots)
(a)
θ = 1.25 r1= 3
lrat = 0.5 r2= 1
(c)
they found that the optimal branching angles (e.g., h in
Fig. 1) were close to those observed in the species
(Fisher and Honda 1977; Honda and Fisher 1978; Fisher
and Honda 1979), whereas the optimal length ratios (see
Table 1) were not near those observed (Honda and
Fisher 1979). This implies that the morphology is not
optimized for effective leaf area, which was supported by
Honda and Fisher (1979). They minimized the variation
in the distribution of leaf clusters on branches (a mea-
sure of the equitable distribution of leaf clusters) and
found that the optimal length ratios matched those ob-
served, but the corresponding branching angles did not.
Furthermore, the branch morphologies that minimized
the equitable distribution of leaf clusters were unable to
achieve optimal values for effective leaf area. The ob-
served combination of branching angle and length ratio
in Terminalia implies that its morphology is sub-optimal
for effective leaf area and the equitable distribution of
leaf clusters when optimized individually. This implies
that there is some trade-off between the two measures
(effective leaf area and equitable distribution of leaf
clusters), and the observed morphology is a compromise
between them. The authors conclude that a single cri-
terion (foliage display, mechanical stability) is insuffi-
cient to explain branch architecture. Aono and Kunii
(1984) performed a similar analysis on Aucuba japonica
and reported that actual trees are similar to those sim-
ulated for optimal foliage display and attributed any
sub-optimal form to mechanical requirements.
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θ = 0.25 r1= 3
lrat = 0.5 r2= 1
(b)
θ = 1.25 r1= 3
lrat = 0.5 r2= 1
(d)
The evolutionary history of land plants has been
characterized by the progressive change in the relative
importance of multiple plant functions, including
reproductive success, light interception, water loss and
mechanical stability (Niklas and Kerchner 1984;
Farnsworth and Niklas 1995; Niklas 1997a, 1997b;
Niklas 1999). Niklas (1994, 1997a, 1997b, 1999) gener-
ated simple plant morphologies by varying the branch-
ing angle (both a bifurcation and rotation angle) and the
bifurcation rate, and calculated the performance of the
plant as the geometric mean of two or more of the four
tasks listed above. Resulting optimal morphologies
mirrored those observed in the early evolution of plants,
and the number of optimal morphologies increased with
the number of tasks included in the optimization (Niklas
1994).
Rather than use an FSM to produce plant architec-
ture, Pearcy et al. (2005) performed detailed measure-
ments on the canopies of actual plants and produced
digitized 3D replications of those canopies (Pearcy and
Yang 1996). They then applied physiological models to
the observed architectures to calculate measures of plant
performance such as light absorption, CO2 assimilation,
leaf temperature and transpiration, photosynthesis, stem
water fluxes, water potential, and biomechanical load. In
addition, they digitally varied the internode length for
the observed architectures under two conditions (a
manipulation that would be impossible in the field), with
and without compensation for the need for biome-

chanical support. They compensated for biomechanical
support by increasing the diameter of the internode to
that necessary to support the increased length. When not
compensating for biomechanical support they kept the
diameter of the internode constant with increasing
length. They found drastic changes in the performance
of whole canopies with changing internode length. When
compensation for mechanical support was also inte-
grated, carbon gain showed an optimum at internode
lengths much longer than those observed. This implies
that an additional factor constrains the length of the
internode and that the observed local architecture (with
respect to internode length) appears to be a compromise
among multiple constraints. They also found strong
convergence in light absorption across a variety of plant
morphologies, which supports the assertion that multi-
ple solutions are available to plants subjected to similar
constraints.
These studies show that changes in simple architec-
tural parameters that are defined at the level of indi-
vidual foliage units can have significant impacts on the
performance of the whole plant. These architectural
parameters also clearly differentiate characteristic plant
canopy structure, which may change the function of a
plant in the greater forest ecosystem. Plants, however,
not only differ in how they display foliage through
changes in architectural parameters. Assuming a basic
architectural ‘‘plan’’, plants also make ‘‘decisions’’ for
where in the canopy to place new foliage units (i.e.,
sighted and self-regulatory models). That is, for a given
pool of meristems, which are able to successfully flush to
form new foliage? The process of preferential placement
of new foliage also has significant impact on overall
canopy structure and function.
Sighted and self-regulatory models
In collaboration with others, Honda produced a sighted
model that modified control of bifurcation and growth
through interference of neighboring plant components
(Honda et al. 1981), and a self-regulatory model that
incorporated material flux dynamics through the plant
structure (Honda et al. 1981; Borchert and Honda 1984).
In the self-regulatory model, an axis would not bifurcate
unless it achieved some threshold level of a hypothetical
material. They were able to simulate plants that exhib-
ited some of the characteristics of observed trees
including apical control and a sigmoid increase in
branch number and exponential decline in actual ter-
minal branches relative to potential. In this case, they
evaluated the consequences of different rules and flow
rates, rather than proposing any conditions for an
‘‘optimal’’ structure. In general, they conclude that
variables such as bifurcation should not be considered as
fixed properties of simulated trees.
Ford (1987) produced a sighted architectural model
with stochastic effects for a population of plants on a
gridded landscape. A node on a plant has a given
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727
probability of branching. If the node branches, then
daughter shoots are produced at a given branching angle
and with a given internode distance, which are both
specified by the modeler and are species-specific. The
probability a node branches was reduced by interference
from other nodes on the same plant or on other plants
(the interference distance). Ford simulated plants both
on a uniform grid (where all areas are available for
growth) and on a patchy grid, which consisted of areas
available to growth and areas not available to growth.
He found that the mean number of nodes per plant is
highest when the branching angle was 30°, although this
optimal branching angle was modified on the patchy
grid by the size of patches available for growth.
Ford et al. (1990) and Ford and Ford (1990) also
found that branch development is non-stationary and
cannot be adequately simulated by the repetition of
simple rules. Their model follows the progression out-
lined in Fig. 1, with two alternative rules to modify the
bifurcation value. In the first simulation type, the
bifurcation value for a shoot depends only on its
architectural status (it decreases from order-1 to order-2
shoots) and this bifurcation is constant throughout
branch development for a given architectural status.
Alternatively, bifurcation is modified by the degree of
occupancy of the space into which the new foliage units
would extend such that competition for light between
branch segments within the branch decreases bifurca-
tion. In this sense, the model is sighted. In their simu-
lation, the length of the new foliage units is also not
constant throughout branch development. It depends on
the amount of carbon available once the simulation
accounts for the amount of branch thickening required
to support the new foliage. This requirement makes the
model self-regulatory. The length of a new foliage unit
also depends on its architectural status, with the length
reduced between order-1 and order-2 shoots. Through
their simulation study they found that the static, re-
peated application of simple rules is insufficient to pro-
duce branches that were visually similar to actual
branches. They calculated the amount of net carbon
produced on the branch (i.e., the export to the trunk)
and found that the conditions under which the optimum
amount is produced depend on whether the first
(architectural status) or the second (occupancy of the
neighborhood) rule for modifying the bifurcation was
simulated. They state that it is no simple task to define
an optimum branching structure—the optimum may
need to be ‘‘specified in terms of the patterns of growth
response to environmental variation’’ (Ford et al. 1990).
Sterck et al. (2005) use an FSM to evaluate how
morphological and physiological traits affect long-term
tree growth and development for a theoretical con-
struction of a generic plant form patterned after species
in tropical forests. Their model is self-regulatory
through the calculation of flush probability that controls
whether a foliage unit produces new foliage units, and
that probability changes with different local conditions
(including hormonal effects, local light levels and carbon

728
status). They evaluated the effects of varying develop-
mental and environmental constraints on growth,
including a hormonal interaction that limits lateral
growth, the effects of carbon economy and leaf longev-
ity, and three light environments (open canopies, closed
canopies, and patchy canopies with closed areas and
occasional gaps). With no constraints and no hormonal
lateral inhibition, the trees grew very large. Incorporat-
ing carbon economy resulted in a size constraint,
whereby the cost of additional hydraulic architecture to
support the larger tree countered the photosynthetic
contribution of additional foliage. With incorporation
of leaf-longevity, there was a decay phase in growth
whereby the loss of foliage outpaced new foliage growth
due to the size constraint. They also found that the self-
regulatory placement of foliage units to maximize each
leaf’s carbon gain over its expected lifespan tended to
increase total biomass (Sterck and Schieving 2007), and
that the inclusion of the production of foliage units
within the crown where branches are lost resulted in an
eventual steady-state of biomass over time (new foliage
production balanced foliage loss). This was attributed to
the placement of foliage units in areas that had less
hydraulic costs. This model was innovative in its com-
parison of plant architectures relative to multiple con-
straints and differing processes of morphogenesis
relative to those constraints, yet its methodology is still
limited. It considers the multiple constraints in a step-
wise manner rather than integrating them simulta-
neously, and there was no structured comparison of the
model results to real trees.
The examples presented thus far demonstrate the
importance for the performance of plant canopies of
varying the architectural and physiological responses of
foliage units. These examples also have in common the
difficulty in incorporating the many constraints on plant
performance (that often conflict, such that improving
performance with respect to one comes at a cost to an-
other; Pearcy et al. 2005), and how processes at the level
of foliage units impact the performance of the whole
plant with respect to those constraints. Furthermore, the
utility of FSMs to facilitate theory development for
actual trees would be improved through a comparison of
model results to empirical observation. This was
attempted by a series of simulation studies by Kennedy
et al. (2004), Kennedy and Ford (2009) and Kennedy
et al. (2009) for old-growth P. menziesii.
FSM applied to a multi-criteria optimization
problem for P. menziesii
Kennedy (2008) and Kennedy et al. (2009) produce a
sighted and self-regulatory model that integrates several
internal and external factors in the placement of new
foliage for a FSM (BRANCHPRO3). This model is
designed specifically to evaluate the pattern of mor-
phogenesis in branches of old-growth Pseudotusga
menziesii in the Pacific Northwest, USA, and how that
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pattern enables persistence of the species in the old-
growth canopy. Hinckley et al. (1998) suggest that the
branch is a useful intermediate unit for scaling from the
leaf-level to the tree and stand levels, and Kennedy et al.
(2009) reduce the Pseudotsuga canopy to a single branch
and evaluate the impact of foliage units (i.e., shoots) on
performance of the branch. This FSM is unique because
it simulates branches of tall and old trees with a large
population of foliage units. The FSM also incorporates
a bank of suppressed buds that allow for regeneration of
foliage in the crown interior through the process of de-
layed adaptive reiteration (DAR; Ishii and Ford 2001).
The new foliage clusters produced after a bud is released
from suppression follow a pattern that closely resembles
the architectural hierarchy exhibited by the branch.
Kennedy 2008 and Kennedy et al. (2009) use multi-cri-
teria assessment and Pareto optimality to evaluate the
model results against both empirical and design criteria.
BRANCHPRO3 model processes
BRANCHPRO3 is a 2D stochastic model that is both
sighted and self-regulatory. The simulation of branch
growth in BRANCHPRO3 begins with a single shoot.
Every year, for every active shoot, the bifurcation (e.g.,
Fig. 1) is determined by a draw from a Poisson distri-
bution whose rate parameter depends on the local con-
ditions of that shoot (e.g., measures of hydraulic
transport, shoot architectural status, and hormonal
interactions). The relative contribution of each local
condition to the bifurcation rate is determined by a
parameter value assigned to each. A single suppressed
bud is assigned to each order 1 (Fig. 1) shoot. Each year,
buds that are still suppressed are tested for release
against a probability value that depends on the bud’s
local conditions (e.g., proximity to active foliage,
hydraulic status, and bud age). The relative contribution
of each local condition to the probability of release is
determined by a parameter value assigned to each. Once
a bud is released from suppression, it forms a foliated
shoot whose bifurcation is determined by the random
draw from a Poisson distribution. In this manner,
BRANCHPRO3 simulates the process of DAR. By
varying the parameter values associated with the local
conditions that determine the bifurcation rate and bud
release from suppression many unique branch mor-
phologies can be simulated. Kennedy et al. (2009) cal-
culate four design criteria that measure the performance
of each simulated branch morphology: the mean
hydraulic path length (a potential constraint on net
growth in large trees), the mean number of hydraulic
junctions from the base of the branch to living foliage
units (whereby each junction represents a possible
hydraulic constriction point, and may constrain net
growth), mechanical load and within-branch foliage
overlap. The goal of the optimization is a morphology
that simultaneously minimizes these four design criteria,
although trade-offs among the criteria prevent such a

single solution. This is evaluated using Pareto optimal-
ity.
Pareto optimality
Pareto optimality allows for multiple criteria to be
optimized simultaneously, and through Pareto opti-
mality we can calculate all optimal weighted combina-
tions of criteria values. The central concept of Pareto
optimality is non-dominance (Cohon 1978, p. 70; Rey-
nolds and Ford 1999). Two sets of criteria are defined to
be mutually co-dominant if improvement with respect to
one criterion is at the detriment to another criterion. The
simplest case is minimizing two criteria simultaneously
(Fig. 3). If there is a trade-off between the two criteria
(i.e., better performance with respect to one criterion
corresponds to worse performance with respect to the
second criterion), then there are multiple mutually
co-dominant solutions. For example, suppose we have
measured the branches of two tree species that coexist in
a given canopy so we know each are capable of
achieving sustained growth (i.e., they both have rela-
tively high fitness). Although these two species must
accomplish the same major tasks and contend with
similar environmental conditions, the two branches ex-
hibit distinct morphologies. They therefore exhibit
varying pathways to achieving sustained growth. We can
compare the performance of these branches with respect
to a vector of two criteria composed of a measure for
hydraulics (e.g., minimize mean path length) and a
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200
180
1 2 3 4 5 6 7 relative mechanical requirements = 0.682; mean foliage over-
Z1
Fig. 3 Idealized representation of a non-dominated Pareto optimal
frontier between two criteria (Z1, Z2) that are both minimized. The
grey area is the feasible space of outcomes from the model, and the
dashed line is the set of solutions that are mutually co-dominant
and not dominated by any other solution. For example, consider if
Z1 is the number of cumulative junctions and Z2 is the mean foliage
overlap. Any improvement with respect to the mean foliage overlap
comes at the expense of the number of cumulative junctions. This
frontier becomes more complicated as the number of criteria
increases and modifies the pair-wise trade-offs
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729
measure for foliage display (e.g., minimize foliage
overlap). If one branch performs better with respect to
both measures simultaneously, then it can be considered
optimal, relative to the other branch. However, in the
more likely case that the first branch performs better
with respect to hydraulics, whereas the second branch
performs better with respect to foliage display, then the
two branches are mutually co-dominant—neither
branch is exclusively optimal. The Pareto optimal
frontier contains the set of all optimal weighted combi-
nations of criteria values, and the intersection of these
solutions with the morphologies of observed organisms
(e.g., Rothley et al. 1997; Vrugt et al. 2007) demonstrates
the combinations of criteria values that allow a given
species to achieve sustained growth.
BRANCHPRO3 pareto optimal results
Kennedy (2008) and Kennedy et al. (2009) used an
evolutionary algorithm (Reynolds and Ford 1999) to
find simulated branch morphologies that correspond to
the Pareto optimal frontier for the four design criteria.
In this solution set they found two distinct branch
morphologies (Fig. 4), and these two morphologies had
equally distinct performance with respect to the opti-
mization criteria. They used empirical criteria to com-
pare the simulated morphologies to the observed
P. menziesii pattern (e.g., number of foliated shoots,
number of reiterating foliage units, branch length, and
400 400
300 300
cm
cm
200 200
100 100
0 0
−200 0 100 200 −200 0 100 200
cm cm
(a) (b)
Fig. 4 Example branches simulated by BRANCHPRO3. The black
lines are foliated shoots, the grey lines are main axis shoots that
have lost their foliage. Lateral axes that have lost their foliage are
not shown. a Branch representative of a morphology that tends to
minimize mean hydraulic path length (mean number of junc-
tions = 5.55 junctions; mean hydraulic path length = 218.47 cm;
lap = 7.42 shoots). b Branch representative of a morphology that
tends to minimize the mean number of junction constrictions (mean
number of junctions = 2.69 junctions; mean hydraulic path
length = 281.59 cm; relative mechanical requirements = 0.772;
mean foliage overlap = 8.15 shoots). The morphology clearly
differs between the two branch types, and the first branch type (a)
more closely matches the observed P. menziesii architectural
pattern. These two solutions are mutually co-dominant because
improvement with respect to some criteria correspond to worse
performance with respect to other criteria (e.g., path length and
foliage overlap are lower for (a) relative to (b), but junctions and
mechanical load are higher)

730
basic architectural model), and the simulated morphol-
ogy that more closely resembled P. menziesii tended to
achieve the lowest values for hydraulic path length
(Fig. 4a). The branch example shown in Fig. 4a exhibits
extensive reiteration all along the major branch axis, and
limited foliage proliferation on lateral axes. The other
major morphology they found tended to minimize the
mean number of junctions. This is akin to evaluating
solutions along the dashed line in Fig. 3 and observing
the morphologies that correspond to solutions in the
upper-left corner, and how they differ from morpholo-
gies that correspond to solutions in the lower-right
corner. This result shows that DAR has the effect of
reducing mean path length to terminal foliage relative to
other, similar morphologies. Although this may be an
obvious result given how the process of DAR occurs,
their analysis shows that this reduction in path length is
the most important feature that distinguishes the
P. menziesii morphology. Despite the clear difference in
morphology, the two branch types exhibited a similar
range of performances with respect to foliage display
and relative mechanical requirements (Kennedy et al.
2009; the measure of relative foliage requirements was
calculated for main axes only, and did not incorporate
the additional requirement of lengthening lateral axes).
In the solution set, the performance of each branch type
with respect to foliage display and mechanical require-
ments depended on the level of reiteration. This was
interpreted to mean that the level of reiteration exhibited
by P. menziesii is the result of the trade-offs among the
four design criteria that were optimized.
The second morphology in the solution set (Fig. 4b) is
reminiscent of true firs (i.e., Abies) that co-exist in the old-
growth canopy. This simulated branch clearly relies on
foliage proliferation across existing lateral axes to achieve
shoot levels commensurable with Pseudotsuga branches,
and it does not produce foliage through DAR. Kennedy
et al. (2009) propose that the different life histories of
Abies and Pseudotsuga in part explain how their mor-
phologies balance the multiple criteria. Individuals of
Abies establish in the understory, and have the ability to
grow rapidly in relatively low light conditions and to
quickly fill gaps. These species exhibit more determinate
growth, and in the simulation the simulated branches
occupy a space with foliage and remain in that space
indefinitely. This is in contrast to the opportunistic pro-
cess of DAR. This example also demonstrates that it is
insufficient to optimize a single value such as hydraulic
efficiency, because there may be multiple pathways by
which hydraulic efficiency is achieved. Although the first
two criteria (path length and junctions) both impact
hydraulic efficiency, the contrast between the two major
morphologies in the solution set shows that it is important
to distinguish the criteria when evaluating the perfor-
mance of plant morphologies. If the criteria had been
integrated into a single value, then this important contrast
would have likely been overlooked. This analysis dem-
onstrates that there is more than one possible optimal
solution when multiple functions are included in the
14401703, 2010, 4, Downloaded from https://esj-journals.onlinelibrary.wiley.com/doi/10.1007/s11284-009-0658-6 by Mikail YEDIREN - Universite De Reims , Wiley Online Library on [10/05/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
optimization, which provides insight into the role of
morphology in the variability observed in forest canopies.
The example of multi-criteria optimization applied to
an FSM that was based on empirical observations of
real branches shows the potential of how FSMs can be
used as virtual laboratories to evaluate the consequences
of shoot-level processes on whole-canopy performance,
and enable an integrated theory of how shoot-level
processes contribute to canopy structure and species
persistence. Not only were Kennedy et al. (2009) able to
find multiple optimal solutions with respect to four de-
sign criteria, they were also able to differentiate the two
simulated branch morphologies with respect to the ob-
served P. menziesii morphology through comparison of
the simulations to empirical criteria. This has conse-
quences for theory development in the role of mor-
phology in the persistence of P. menziesii, and the
relative importance of the design criteria for large, old
species (Kennedy et al. 2009).
Discussion
Overwhelmingly, modeling exercises show that small
changes in local plant architecture and the process of
morphogenesis have clear impacts on plant morphology
(Fig. 2) and the many measures of plant performance.
Blind models show that the bifurcation, branching angle,
length ratio between axes of different order, as well as the
internode length all change how foliage is distributed and
displayed within plant canopies. Sighted and self-regu-
latory models show that these architectural parameters
are non-stationary as a plant develops and at different
positions within a plant in a given year. In sighted and
self-regulatory models, the placement of foliage units can
be governed by conditions such as space occupancy or to
maximize the net carbon gain. Direct manipulation of
plant architecture is difficult, if not impossible, in the field.
By evaluating the effects of these parameters using a
simulation model, we are able to show the relative
importance of each on overall plant performance.
FSMs have not yet fulfilled their potential to illumi-
nate function and structure relationships in plant cano-
pies; a deficiency in the explanation models can provide
has been the case in general with many other kinds of
ecological models (Grimm 1999; Reynolds and Ford
1999; Ford 2000). Until recently, FSMs have been lim-
ited in their application to observed plant species, for
larger and older trees, and for plants in varying eco-
logical environments. That limitation has improved first
with attempts to link FSM outputs to empirical mea-
surements (Borchert and Honda 1984; Evers et al. 2007;
Kennedy 2008). Kawamura (2009) presents a conceptual
model for investigating modular responses to local
environmental heterogeneity, which includes many
concepts that are incorporated into functional–struc-
tural models (e.g., apical dominance and positional
control). It is important to integrate empirical studies
under frameworks such as this with the development and

assessment of FSM processes. Further improvement has
been made when the results of FSMs are evaluated
against multiple measures of model performance (Ken-
nedy 2008; Kennedy and Ford 2009; Kennedy et al.
2009). This progress in the use of models in the analysis
of plant form and function requires that models be tes-
ted against multiple criteria simultaneously.
Kennedy et al. (2009) demonstrate that explanations
in ecology require the integration of many factors
(Schmitz et al. 1998). In the case of plant morphology,
for example, it is recognized that multiple factors act
simultaneously on system function. In order to under-
stand the relationship between plant form and function,
therefore, these multiple factors cannot be considered
one-at-a-time under strictly controlled circumstances.
For example, Kennedy et al. (2009) use Pareto opti-
mality to show that multiple plant morphologies are
possible solutions to the multi-criteria optimization
problem (Fig. 4), and that each morphology balances
the competing priorities. One solution is not considered
singularly optimal, because the constraints compete
(such as the mean number of junctions and the mean
path length to terminal foliage). This provides an
explanation for the structural diversity found in old-
growth conifer forests, which is evident only when the
multiple factors are optimized using Pareto optimality.
This biodiversity and variability of the performance of
plants in forest ecosystems yields further biodiversity in
animal habitat, epiphytic distributions, arthropod
diversity, and plant distributions (Schowalter 1989;
McCune 1993; Hamer and Nelson 1995; Esseen et al.
1996; Hershey et al. 1998; Sillett and Rambo 2000;
Lehmkuhl 2004; Ruth 2005).
Acknowledgments The author would like to thank E. David Ford,
Mark Kot, and Thomas Hinckley for their help in developing the
ideas for this paper. Hiroaki Ishii and E. David Ford and two
anonymous reviewers provided valuable advice for the preparation
of the manuscript.
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