HYPOTHESIS AND THEORY
published: 26 July 2016
doi: 10.3389/fpls.2016.01095
Frontiers in Plant Science | www.frontiersin.org 1 July 2016 | Volume 7 | Article 1095
Edited by:
Alexander Bucksch,
Georgia Institute of Technology, USA
Reviewed by:
Gerald Schoenknecht,
Oklahoma State University–Stillwater,
USA
Roman Zweifel,
Swiss Federal Institute for Forest,
Snow and Landscape Research,
Forest Dynamics, Switzerland
Masha Van Der Sande,
Wageningen University and Research
Centre, Netherlands
*Correspondence:
Frank Götmark
frank.gotmark@gu.se
Specialty section:
This article was submitted to
Plant Biophysics and Modeling,
a section of the journal
Frontiers in Plant Science
Received: 08 April 2016
Accepted: 11 July 2016
Published: 26 July 2016
Citation:
Götmark F, Götmark E and Jensen AM
(2016) Why Be a Shrub? A Basic
Model and Hypotheses for the
Adaptive Values of a Common Growth
Form. Front. Plant Sci. 7:1095.
doi: 10.3389/fpls.2016.01095
Why Be a Shrub? A Basic Model and
Hypotheses for the Adaptive Values
of a Common Growth Form
Frank Götmark
1
*
, Elin Götmark
2
and Anna M. Jensen
3
1
Department of Biological and Environmental Sciences, University of Gothenburg, Göteborg, Sweden,
2
Mathematical
Sciences, Chalmers University of Technology and University of Gothenburg, Göteborg, Sweden,
3
Department of Forestry
and Wood Technology, Linnaeus University, Växjö, Sweden
Shrubs are multi-stemmed short woody plants, more widespread than trees, important
in many ecosystems, neglected in ecology compared to herbs and trees, but currently
in focus due to their global expansion. We present a novel model based on scaling
relationships and four hypotheses to explain the adaptive significance of shrubs, including
a review of the literature with a test of one hypothesis. Our model describes advantages
for a small shrub compared to a small tree with the same above-ground woody volume,
based on larger cross-sectional stem area, larger area of photosynthetic tissue in bark
and stem, larger vascular cambium area, larger epidermis (bark) area, and larger area
for sprouting, and faster production of twigs and canopy. These components form
our Hypothesis 1 that predicts higher growth rate for a small shrub than a small tree.
This prediction was supported by available relevant empirical studies (14 publications).
Further, a shrub will produce seeds faster than a tree (Hypothesis 2), multiple stems in
shrubs insure future survival and growth if one or more stems die (Hypothesis 3), and
three structural traits of short shrub stems improve survival compared to tall tree stems
(Hypothesis 4)—all hypotheses have some empirical support. Multi-stemmed trees
may be distinguished from shrubs by more upright stems, reducing bending moment.
Improved understanding of shrubs can clarify their recent expansion on savannas,
grasslands, and alpine heaths. More experiments and other empirical studies, followed
by more elaborate models, are needed to understand why the shrub growth form is
successful in many habitats.
Keywords: woody plants, stem, multi-stemmed, shrubland, scrub, tree, growth, canopy
“...since Theophrastus (born c. 370 BC), botanists have generally distinguished between trees, shrubs,
and herbs.” (
Petit and Hampe, 2006, p. 189)
“Shrubiness is such a remarkable adaptive design that one may wonder why more plants have not
adopted it.” (
Stutz, 1989, p. 325)
INTRODUCTION
Trees and shrubs are two major growth forms in many natural and semi-natural habitats. Here, we
focus on shrubs, a widespread category of woody plants, and elucidate their adaptive significance.
We present a model based on scaling relationships where shrubs are compared with trees, outline
hypotheses for the adaptiveness of shrubs, and test one of the hypotheses, based on the literature.
Götmark et al. Adaptive Significance of the Shrub Growth Form
Many t h eoretical and empirical studies of trees address their
adaptive significance, for instance variability in height among
species, and maximum heig h t (e.g.,
Horn, 1971; Ryan and Yoder,
1997; Loehle, 2000
). In contrast, the adaptive significance of
shrubs is only discussed briefly in the literature. For instance,
Whittaker and Woodwell (1968, p. 11) stated that shrubs “may
have high production per unit leaf weig h t and surface... and
smaller expenditure of this production on supporting stem and
branch tissue than is the case in forest trees.” Givnish (1984, p.
78) suggested that shrubs are favored in open habitats where tree
crowns have been destroyed, by having “more meristems active,
[and] more potential points for stem regeneration.”
Another suggestion is that the shrub growth form is
“a design strategy of relatively small, low-investment, low
risk, “throwaway” stems that are expendable in high-stress
environments” (
Wilson, 1995, p. 92). Stutz (1989) stated that
shrubs usually are tall enoug h to dominate herbs and do not
need to rebuild as much biomass each year as herbs. On the
other hand, shrubs often occur in grassland, for instance savanna,
where grasses and/or fires may control woody vegetation,
including shrubs (
Bond and van Wilgen, 1996; Sholes and Archer,
1997). Shrubs are sometimes discussed on the basis of their
low, broad canopy in disturbed habitats, and Givnish (1984)
argued that such a canopy is favored by multiple stems. It is
often suggested that shrubs are associated with disturbed and
stressful environments (e.g., Rundel, 1991; Givnish, 1995; Sheffer
et al., 2014). However, elaborate hypotheses and models for
the adaptive significance of the shrub growth form seem to be
lacking. Moreover, the recent expansion of shrubs in several
regions globally (e.g.,
Naito and Cairns, 2011; Formica et al.,
2014) motivates more basic research about shrubs.
Below, we first define “tree” and “shrub.” Because shrubs have
been neglected compared to herbs and trees (see Discussion),
we briefly outline their importance. We then describe our basic
model and four hypotheses that potentially can explain the
adaptive significance of shrubs, compared to trees. Our main
contributions are the basic model (Section The Basic Model and
Hypotheses), and Hypothesis 1 and the preliminary test of it
(Section Hypothesis 1: The Multiple Stems of a Small Shrub Give
Faster Growth than for a Small Tree). The Hypotheses 2, 3 and
4 (Sections Hypothesis 2: The Fast Maturity of Shrubs Enables
Earlier Seed Production Compared to Trees, Hypothesis 3: The
Multiple Stems in Shrubs Insure Future Survival and Growth
if One or More Stems Die, and Hypothesis 4: The Short Stems
of Shrubs Improve Survival through Three Traits, Compared
to Tall Tree Stems) are complementary and also important
ideas, supported by some evidence. Finally, we discuss ecological
aspects of shrubs and trees, and identify research needs.
Delimitation and Definition
It is sometimes difficult to identify a woody plant as a tree or a
shrub, and intermediate forms exist (see Rundel, 1991; Wilson,
1995). Sheffer et al. (2014) stated “In contrast to shrubs, trees
have a single stem, but this distinction is not absolute... 9.2%
of the tree species we analyzed were also qualified as shrubs by
some contributors in the trait database.” In tropical rainforest,
the woody growth forms are diverse, with more forms than just
tree/shrub (see
Givnish, 1984, Table 4;Rundel, 1991). In South
African savanna, in a study of 23 woody species, Zizka et al.
(2014)
recognized shrubs (mean value: 13 st ems), SSTs (“shrubs
sometimes small trees,” 3.6 stems) and trees (2.2 stems). Some
shrubs are semi-woody, being woody in the lower stem parts and
herbaceous in the upper (trees also have herb-like shoots that
become woody with time).
Here, we define a tree as a tall perennial plant with a single
self-supporting woody stem, and a shrub as a short perennial
plant with multiple self-supporting woody stems, branching at
or near the ground. However, trees can have multiple stems,
and the shrubs we discuss below range from very small (e.g.,
Vaccinium spp., about 0.2 m tall) to large Corylus spp. (up to
about 10 m tall). Figure 1 illustrates a shrub of a common
type (about 50 cm tall); a tree with one central stem (many
conifers and angiosperms); a tree with one short stem, branching
early t o produce a broad canopy forming >50% of the height
of the tree (e.g., Ulmus spp., savanna trees); and a tree with
multiple stems which we suggest may be distinguished by
stem form as well as height (see Discussion). Photographs
in Figure 2 illustrate two types of shrubs and two multi-
stemmed trees. Shrub-like bamboos are also relevant, some of
which have strong stems more than 25 m tall (
Wang et al.,
2014) and may also dominate trees (Griscom and Ashton,
2003), but we did not include them in our literature review
below.
Despite problems in defining some species as shrubs, the
term shrub is widely used and shrubs are important in many
ecosystems (see next section). In addition, biology and ecology
contain many terms that are difficult to define precisely (e.g.,
“forest”) but useful in research and management.
The Occurrence and Ecological
Importance of Shrubs
Shrubs are important components in at least 9 of 11 global biomes
(
Archibold, 1995; see also McKell, 1989), forming much of the
vegetation in tropical savannas, arid regions, Mediterranean
ecosystems, and polar and high mount ain tundras. They are
also frequent in terrestrial wetlands and in the understory
and canopy gaps in forests, where both shade-tolerant and
pioneer (shade-intolerant) shrubs occur (e.g., Denslow et al.,
1990).
Olson et al. (2001) classified 14 terrestrial biomes, and
“shrubland” or “scrub” occur in the name of 5 biomes. Shrubs
occur in at least 13 of the 14 biomes. Gong et al. (2013) used
satellite data to estimate global land-cover types; forest covered
28.4% of the land and shrubland covered 11.5%. Because shrubs
also occur in forest, they grow, or can grow, on about 40% of the
land surface. Shrubland was defined as having a vegetation cover
of >15%, but some bare land with sparse vegetation also contains
shrubs (see Gong et al., 2013), so the t otal area where they can
grow mig h t be close to 45% of the global land surface.
Given the vast global distribution of shrubs, they are
important for climate control, soil stabilization and production,
ecosystem water balance, carbon uptake and storage, and for
many associated species such as grazing and browsing mammals
Frontiers in Plant Science | www.frontiersin.org 2 July 2016 | Volume 7 | Article 1095
Götmark et al. Adaptive Significance of the Shrub Growth Form
A B C D
FIGURE 1 | Four types of woody plants: (A) Shrub, here with five stems, branching as in the basic model (about 50 cm tall). (B) Tree with main stem
throughout the plant. (C) Tree with short main stem with many branches, forming most of the plant. (D) Tree with multiple stems. (C,D) are from Ceco.NET, (B) is from
Natural Resources Canada (red alder; tidcf.nrcan.gc.ca), and (A) is our own drawing.
and livestock, birds, fungi, and invertebrates. “Nurse plants” favor
other plants, including trees, and in a review of such plants
“shrubs were the dominant nurse life-form” (Filazzola and Lortie,
2014). Moreover, shrubs exhibit h igh species richness in several
regions on the earth (Qian, 2015; Qian and Ricklefs, 2015; see
also Rundel, 1991). Currently, shrubs and “shrubification” are
much studied in tropical and temperate grassland and in arctic
and other cold habitats that lack trees, often in relation to climate
change (e.g.,
Hallinger et al., 2010; Ratajczak et al., 2012; Formica
et al., 2014; Ogden, 2015
).
The next section describes our basic model, which is relevant
for Hypothesis 1 in Section Hypothesis 1: The Multiple Stems of
a Small Shrub Give Faster Growth than for a Small Tree. All our
four hypotheses focus on t he adaptive value of shrubs compared
with trees. For trees, we assume that their main adaptive value
or advantage is height development, leading to elevated canopies
that shade competitors (including shrubs) and large root systems
that also help dominate shrubs. In addition, a tall tree with a large
canopy c an potentially produce more seeds and disperse pollen
and seeds more widely.
THE BASIC MODEL AND HYPOTHESES
To explore functional trait differences between single- and multi-
stemmed woody plants (trees vs. shrubs), we built a basic
volume-based growth model. Biomass partitioning occurs only
between above-ground woody parts, thus foliage and roots
are not included in the model. The following traits were
studied: cross-sectional stem are a, bark surface a rea, branching,
canopy development (branching), and stem bending moment
(intuitively, the strain when forces act on the stem so that
it bends). We modeled above-ground woody biomass [that is,
stem(s) and branches] using the functions V
t
(h
t
) and V
s
(h
s
,n),
which give the volumes of a tree of height h
t
, and a shrub of height
h
s
, and number of stems n. For a given volume v we can solve
V
t
(x) = v and V
s
(x,n) = v numerically and obtain heights h
t
(v)
and h
s
(v,n), compared in Figure 3A.
For simplicity, tree and shrub volumes V
t
(h
t
) and V
s
(h
s
,n) are
calculated by modeling stems and branches as truncated cones
with basal radius proportional to length, or as cylinders when
the basal radius is small enough. We explain the parameters
in Table 1; all are constants which can be varied freely. When
a stem reaches the length l
min
, branches of length p
∗
l
min
are
added, which then grow proportionally in length with the
main stem. We add a
t
branches per stem for a tree and
a
s
for a shrub, corresponding to
Whitney (1976) branching
coefficients a
t
+1 and a
s
+1, respectively (Whitney counts the
stem tip as a child branch; we do not). These branches in
turn get “child branches” in the s a me way when they grow
long enough. The model does not include thinning within
individuals during growth, so we only apply it to small trees and
shrubs.
Note that the above description is simplified: to avoid child
branches p
∗
l
min
cm long appearing out of nowhere when parent
branches reach the length l
min
cm (making the volume functions
discontinuous), child branches begin to grow when parent
branches are 2/3
∗
l
min
cm long, and grow linearly to reach the
length p
∗
l
min
cm when the parent branch is l
min
cm long. The
number 2/3 is rather arbitrary, but affects the results very little—
it only specifies how the discontinuous parts of the function are
“glued together.” The parameters r
tip
(the radius of a branch tip),
b
t
, and b
s
(the ratio of the basal radius of a stem or branch
and its length for trees and shrubs, respectively), l
min
, and p
were chosen from inspection of small trees and shrubs of several
species, to be: a
t
= a
s
= 2, p = 0.5, l
min
= 20 cm, r
tip
=
0.1 cm, b
t
= b
s
= 0.0075, g
s
= 1. All parameters probably
vary among species and habitats, but we have tried different
realistic values and the s caling relationships between trees and
shrubs seen in Figure 3 still hold. Note that to reach the same
Frontiers in Plant Science | www.frontiersin.org 3 July 2016 | Volume 7 | Article 1095
Götmark et al. Adaptive Significance of the Shrub Growth Form
FIGURE 2 | Two species of shrubs and two species of trees, multi-stemmed: (A) Cassinia arcuata (Asteraceae), Drooping Cassinia or Chinese Scrub,
an evergreen shrub in central Victoria, Australia. This species has colonized thousands of hectares in the area during the last 40 years, when land use changed
(see
Lunt, 2011). The trees are Eucalyptus sideroxylon (Red Ironbark). (B) A large Salix sp. shrub (probably a hybrid) in winter on moist ground in Sweden, with
horizontal growth by sprouts on lying stems. Deciduous Salix spp. are common especially on moist soils in cold and temperate regions in the northern hemisphere.
(C) Chamaecyparis lawsoniana (Cupressaceae) or Port-Orford-cedar, an evergreen conifer from western North America. It is normally single-stemmed but may
become multi-stemmed after damages, e.g., from browsing (picture from botanical garden, Sweden). (D) Betula pendula (Betulaceae), Silver Birch or Warty Birch in
multi-stemmed version probably caused by browsing or cutting damage on seedling/sapling (Pixbo, SW Sweden). Note self-thinning (dead stems). Normal
single-stem birches grow in the background. Note also uprising stems of the multi-stemmed trees in (C,D), which would reduce the bending moment of heavy leaning
stems (see Discussion and Figure 4). Photographs: Ian Lunt (A) and Frank Götmark (B–D).
height as a tree, a shrub with n stems and with a
t
= a
s
, b
t
=
b
s
, must increase in above-ground woody volume n times as
fast as a tree (that is, g
s
= n). This follows since one shrub
stem with its branches is modeled the same as a tree stem with
branches.
Once we have h
t
(v) and h
s
(v,n) we can calculate other
important tra its, for example the basal radius of a stem a nd thus
the total cross-sectional area at stem base(s). Investing in multiple
stems, compared to a single stem, gives a greater total cross-
sectional area at the stem base(s), increasing with n (Figure 3B).
We can also calculate the total surface are a of stem(s) and
branches. Investing in multiple stems gives a greater total bark
surface area, increasing with n (Figure 3C). The same holds for
the stem-photosynthetic area, the area of vascular cambium, and
area for sprouting, e.g., on the lower 25% of the stems (all graphs
would be similar to Figure 3C). All these results are illustrations
of the general mathematical principle that volume and area
scale differently. The number of twigs (outermost generation
of branches) is larger for shrubs than for trees, given the same
above-ground woody volume (Figure 3D). A more realistic twig
model requires knowledge of the relative thinning and allocation
strategies of trees and shrubs.
Our model uses a simple proportional relationship between
stem height and basal radius for small stems (
Whittaker and
Woodwell, 1968; Niklas, 1994). In Equation (5) in Niklas
and Spatz (2004) a relationship L = k
5
D
2/3
− k
6
is derived
between height L, basal stem diameter D, and empirically
determined constants k
5
and k
6
. This relationship is a good
model for both small and large trees (as opposed to the
common model L = kD
2/3
for large trees). Substituting this
relationship instead of the simple proportional function in
our model, the functions V
t
(h
t
) and V
s
(h
s
,n) will change, but
the height and are a comparison between trees and shrubs
will not be much affected (see graphs in Data Sheet 1 in
Frontiers in Plant Science | www.frontiersin.org 4 July 2016 | Volume 7 | Article 1095
Götmark et al. Adaptive Significance of the Shrub Growth Form
A B
C D
FIGURE 3 | (A) Trees are taller than shrubs with the same above-ground woody volume. (B) A small shrub with the same above-ground woody volume as a small tree
has a larger total cross-sectional area at stem base(s), increasing with number of stems. (C) A small shrub with the same above-ground woody volume as a small tree
has a larger surface area, increasing with number of stems. This is true for bark (epidermis) as shown here, but also for sprouting area, cambium area, and area of
photosynthetic tissue on and within s tem. (D) A small shrub with the same above-ground woody volume as a small tree produces twigs (outermost generation of
branches) faster than a tree. The parameter values in (A–C) are: a
t
= a
s
= 2, p = 0.5, l
min
= 20, r
tip
= 0.1, b
t
= b
s
= 0.0075, g
s
= 1.
Supplementary Material). That is, th e graphs in Figure 3 would
be similar.
The bending moment around the origin of a point-mass
at location a is |F|·|b|, where F is the force applied to
the mass, and b is the component of a which is at right
angles to F. We set the origin at the stem base. In our case
the force will be gravity which acts vertically, so that the
bending moment increases the farther we get from the origin
horizontally. This is why a straight stem will have higher
bending moment the more it leans outwards. Since a stem
is not a point mass, we have to add all the contributions
along its length, which leads to an integral. For simplicity,
we omit the branches, and we use the stem taper function
from
Niklas and Spatz (2004; Figure 4; calculations in Data
Sheet 1 in Supplementary Material). We use these results in
Hypothesis 4.
All calculations are implemented in Matlab (see Supporting
Information).
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