Forest Ecology and Management 109 (1998) 187±195
Effects of above- and below-ground competition of shrubs and
grass on Calophyllum brasiliense (Camb.) seedling
growth in abandoned tropical pasture
Karen D. Holl*
Environmental Studies Department, University of California, Santa Cruz CA 95064, USA
Received 11 November 1997; accepted 6 January 1998
Abstract
Early-successional vegetation is often a major factor that limits recovery of tropical forest in abandoned pastures by
outcompeting seedlings of forest trees. The goal of this study was to compare the effects of above- and below-ground
competition of pasture grasses and shrubs on the growth of tree seedlings in abandoned tropical pasture in Costa Rica.
Seedlings of Calophyllum brasiliense were planted in areas of dense pasture grass and below shrub patches. In each vegetation
type seedlings were subjected to one of four treatments: control, root trenching, above-ground clearing, or trenching and
clearing. Seedling height was measured and above- and below-ground biomass was harvested after one year. Seedling height
and biomass were higher for seedlings grown under grass than under shrubs. Above-ground clearing had a strong positive
effect on seedling height and all biomass measurements (stem, leaves, tap root, and ®ne roots). Trenching had a signi®cant
effect on height and all biomass measurements except tap root mass; however, trenching had a weaker effect on plant growth
than above-ground clearing. Root:shoot ratios were signi®cantly affected by trenching. These results suggest that both pasture
grasses and early-colonizing shrubs may slow succession of forest in abandoned pasture. Moreover, the results highlight the
importance of reducing above-ground competition to improve the success of reforestation efforts. # 1998 Elsevier Science
B.V.
Keywords: Light; Reforestation; Roots; Succession
1. Introduction
Tropical forests are being destroyed at an unprecedented rate. For example, in Costa Rica, forest cover
has dropped from 80 to 25% in the past 50 years
(Hartshorn, 1982). In Latin America, much of the
*Corresponding author. Tel.: 00 1 408 459 3668; fax: 00 1 408
459 4015; e-mail: kholl@cats.ucsc.edu
0378-1127/98/$19.00 # 1998 Elsevier Science B.V. All rights reserved.
PII S0378-1127(98)00248-5
forest is cleared for agricultural purposes, in particular
to create pasture land for cattle grazing (Amelung and
Diehl, 1992; Fearnside, 1993). These agricultural
lands are increasingly being abandoned due to declining productivity and changing economic incentives
(Aide et al., 1995; Uhl et al., 1988). This process of
clearing and abandonment has led to large areas of
highly degraded lands that are often slow to recover,
particularly in areas of intense disturbance with agricultural machinery (Buschbacher et al., 1988). In
188
K.D. Holl / Forest Ecology and Management 109 (1998) 187±195
recent years, there has been increasing interest in
understanding factors limiting recovery, in order to
develop strategies to facilitate forest succession (Holl,
1997). There has been an increase in efforts to reforest
these areas with native species in order to facilitate
forest recovery and to provide income to land owners
from future logging (Butter®eld and Fisher, 1994;
Guariguata et al., 1995; Lugo et al., 1993; Montagnini
and Sancho, 1990).
One of the primary factors (reviewed in Holl, 1997)
that limits recovery of tropical forest in abandoned
pasture is existing vegetation; however, the effects of
different types of vegetation (e.g. grasses and shrubs)
are not well-understood. Tropical pastures are often
planted or seeded with aggressive, non-native pasture
grasses. A number of studies suggest that above- and
below-ground competition with pasture grasses is
major factor that limits growth of tree seedlings in
tropical pastures (GonzaÂlez Montagut, 1996; Guariguata et al., 1995; Nepstad et al., 1991; Sun and
Dickinson, 1996; Sun et al., 1995). However, results
of other studies suggest that grasses may have some
positive effects on woody plant establishment by
moderating stressful microclimatic conditions (Aide
and Cavelier, 1994; Holl, in press).
Abandoned pastures are often rapidly colonized by
shrubs (Aide et al., 1995, 1996; Nepstad et al., 1990;
Vieira et al., 1994). These authors suggest that shrubs
facilitate forest succession in abandoned pasture. For
example, research by Vieira et al. (1994) in Brazil
suggests that shrubs may accelerate recovery by
increasing seed dispersal, elevating soil nutrients,
and creating more favorable microclimatic conditions.
However, research in the temperate zone suggests that
early-successional shrubs may inhibit the growth of
trees (Niering et al., 1986; Meilleur et al., 1994; Putz
and Canham, 1992). There has been very little
research comparing the roles of above- and belowground competition on succession in abandoned
tropical pastures.
The goal of this research was to determine (1) which
of grasses or shrubs provide a stronger impediment to
growth of woody seedlings in abandoned tropical
pastures and (2) whether competition is stronger
above- or below-ground. Understanding the effect
of existing vegetation on the growth of woody seedlings is essential for designing restoration and reforestation plans in these degraded lands.
2. Methods
2.1. Site description
This study was conducted in abandoned pasture
adjacent to the Las Alturas Biological Station in
southern Costa Rica (88570 N, 828500 W, 1500 m elev.).
The 5 ha pasture where the study was conducted is part
of a mosaic of agricultural land uses covering
2500 ha. The pasture where the study was conducted
was cleared 25 years ago using heavy machinery. The
land was used for 15 years for the cultivation of coffee
and for the subsequent 10 years for cattle grazing.
Cattle were removed from the pasture in February
1995. At that time, the pasture vegetation consisted
predominantly of two non-native grasses, Axonopus
scoparius (FluÈgge) Kuhlm. and Melinus minuti¯ora
Beauv.
At the time of pasture abandonment there were few
shrubs present because the land owner regularly cut
shrubs in order to maintain open pastures for grazing.
However, shrubs quickly re-grew from the base after
pasture abandonment. A survey of the pasture in
February 1996, one year after abandonment and four
months prior to the initiation of this study, indicated
that there were a total of 151 shrub patches >1 m2;
these patches covered 2.4% of the pasture. The most
common species of shrubs and small trees were Inga
spp., Piper arboreum Aubl., Rubus spp., Solanum
spp., Tournefortia glabra L., and Vernonia patens
H.B.K.
Average annual rainfall at the site is 3000 mm,
more than 95% of which normally falls between April
and December (Instituto Costarricense de Electricidad, unpublished data). Average annual maximum and
minimum temperatures are 24.6 and 13.28C, respectively (Instituto Costarricense de Electricidad, unpublished data). Previous research at this site suggests that
soil moisture does not limit plant growth during the
dry season (Holl, in press).
The soils are volcanic in origin. Surface soil samples (0±5 cm) were taken in February 1997 and were
processed at the Soils Laboratory of the College of
Agriculture at the University of Costa Rica following
standard methods currently used by soil testing laboratories in the country (DõÂaz-Romeu and Hunter, 1978).
These methods are detailed in Holl (in press). Levels
of Ca, Mg, and CECe were signi®cantly higher under
K.D. Holl / Forest Ecology and Management 109 (1998) 187±195
Table 1
Soil nutrients in grass and in shrubs at 0±5 cm depth a
Soil character
Grass
Shrub
Sig
pH (in H2O)
Ca (cmol/kg)
Mg (cmol/kg)
K (cmol/kg)
Acidity (cmol/kg)
CECe (cmol/kg)
OM (%)
N (%)
P (mg/kg)
5.70.03
6.40.6
2.20.3
0.330.04
0.710.08
9.60.7
22.21.6
0.840.04
4.20.2
5.60.04
10.21.4
3.80.4
0.540.13
0.610.08
15.11.8
22.51.3
0.920.05
4.20.2
NS
*
**
NS
NS
*
NS
NS
NS
a
CECeˆEffective cation exchange capacity; OMˆOrganic matter.
Values are means1 SE. Nˆ11 for each vegetation type. Values in
different habitats in each layer were compared using a t-test. NS
ˆnot significant;
* ˆP<0.05;
** ˆP<0.01.
shrubs (Table 1). However, P, the most likely limiting
nutrient (Holl, in press), did not differ signi®cantly
between the vegetation types.
2.2. Experimental design
To determine the effects of above- and belowground competition of shrubs and pasture grass on
the growth of tree seedlings, 1-year seedlings of
Calophyllum brasiliense Camb. were planted in areas
of grass and under mixed-species shrub patches
(monospeci®c shrub patches do not exist in the pasture). Shrub patches were selected that were comprised of a mixture of the most common species (listed
above). Shrub height ranged from 1±5 m. Grass areas
were predominantly covered by the two pasture
grasses (listed above), ranging from 0.75±1.5 m in
height.
Calophyllum brasiliense was chosen as it is a tree
species present in the nearby primary forest, it naturally establishes in pastures, and is often planted in
reforestation efforts (Francis, 1995; Guariguata et al.,
1995; Nichols and GonzaÂlez, 1991). It is a wide
ranging species found from sea level to 1500 m in
much of Central America and the Carribean (Nichols
and GonzaÂlez, 1991). It fruits in June/July in the
vicinity of the study site and the seeds germinate
immediately after dispersal. Seeds were collected
within 5 km of the study site, and seedlings were
grown in a nursery located 1 km from the study site.
189
Four C. brasiliense seedlings were planted in each
of 11 shrub patches and an area of grass adjacent to
each shrub patch in June 1996. Mean seedling height
was 21 cm (range 11±35 cm). Within each patch,
seedlings were randomly assigned to one of four
treatments: reduction of root competition, reduction
of above-ground competition, reduction of both
above- and below-ground competition, and a control.
Seedlings within a patch were separated by a minimum of 2 m. Below-ground competition between
existing vegetation and seedlings was reduced by
cutting a deep circular trench (30±40 cm deep and
0.75 m diameter). To prevent roots from encroaching into this area, a double layer of 6 mil plastic was
placed in the trench before back®lling. Excavation of
plastic at the end of the study showed that no roots
penetrated the plastic. Above-ground competition of
grass was reduced by clearing grass in an 0.75 m
diameter circle surrounding seedlings with a mechanical trimmer every two months. Shading of seedlings
by shrubs was reduced by tying back large branches
and by clearing small branches with a mechanical
trimmer or machete every two months. Trenched plots
were weeded monthly to remove herbaceous seedlings
that were rooted within the 0.75 m circle. In trenched
but not cleared plots, grass and shrubs rooted outside
the trench shaded the seedlings.
Before the initiation of the study herbaceous cover
was measured in a 1 m2 quadrat centered at the
location where each seedling would be planted. Shrub
canopy cover directly over seedlings was estimated at
the beginning and end of the experiment with a
spherical densiometer. Values reported are averages
for these two measurements.
Calophyllum brasiliense seedlings were fenced
with 22 cm diameter45 cm tall chicken wire to
prevent rabbit herbivory, which is a major cause of
seedling mortality at the site (Holl and Quiros Nietzen,
in press); fences did not appear to reduce seedling
growth. Immediately after planting and applying treatments, seedling heights were measured. Analysis of
initial seedling heights indicated that there were no
signi®cant differences by treatments. Therefore, ®nal
measurements of height and biomass are reported
rather than changes in these values over time.
Seedling heights were measured every two months
until the termination of this study at the beginning
of July 1997. At that time, plant roots were carefully
190
K.D. Holl / Forest Ecology and Management 109 (1998) 187±195
excavated with small spades, knives, forks, and
®ngers. Roots were washed using a 0.27% solution
of sodium pyrophosphate (BoÈhm, 1979) to disperse
soil particles. Both above- and below-ground
biomass were dried at 708C to constant mass; stems,
leaves, tap roots, and ®ne roots were each weighed
separately.
In order to test (1) whether root trenching around
target seedlings was effective in reducing root biomass
of shrubs and grass and (2) whether above-ground
clearing affected below-ground biomass of shrubs and
grass, root biomass of existing vegetation was measured near all tree seedlings at the end of the study. A
7.4 cm diameter core was taken at a depth of 0±5 cm
within the 0.75 m diameter circle surrounding each
seedling. Roots were only sampled in the top 5 cm
because samples taken from the control sites at three
depths indicated that very ®ne roots, which are most
important to nutrient uptake, were concentrated in the
top 5 cm (grass ± 0±5 cm: 87.713.4, 5±10 cm: 33.9
4.5, 10±15 cm: 23.05.6; shrub: 0±5 cm: 40.76.9,
5±10 cm: 16.61.7, 10±15 cm: 15.52.2; units g/m2).
After removing roots of C. brasiliense remaining roots
were separated from soil by washing with a 0.27%
solution of sodium pyrophosphate followed by passage through a 0.5 mm2 sieve. Roots were separated
into three diameter classes (<0.5 mm, 0.5±2 mm, and
>2 mm) and were oven-dried at 708C to constant mass.
Root biomass has been shown to be highly correlated
with root length within the three root classes separated
(Flietner, 1987).
3. Results
Before clearing treatments, herbaceous cover in all
grass plots was 100%, whereas in shrub plots herbaceous cover was only 111%. In grass plots cover
remained nearly 100% in uncleared plots through the
study; cleared plots had no cover. In shrub patches that
were not cleared canopy cover was 951%; average
canopy cover in cleared plots was 214%.
Only four of the 88 plants died over the 1-year study
period. Three died due to unknown causes; each of
these plants was in a different treatment combination
suggesting that there was no effect of treatment on
survival. One plant died because the cage was knocked
over by a falling shrub limb and the stem was subsequently cut by rabbits.
Plant biomass and height were signi®cantly higher
for seedlings grown in grass than under shrubs (Fig. 1;
Table 2). Above-ground clearing had a strong positive
effect on seedling height and all biomass measurements. Trenching had a signi®cant effect on height and
all biomass measurements except tap root mass.
Root : shoot ratio was signi®cantly lower in plots that
had been trenched. There were no signi®cant interactions between the three main effects (vegetation
type, trenching, and clearing) on height or any of
the biomass measurements.
As expected, trenching had a strongly signi®cant
effect on the biomass of roots of plants other than
2.3. Statistical analysis
Treatment effects were assessed using analysis of
variance with a split-plot model. The whole plot effect
was each shrub or grass block. Clearing and trenching
treatments were randomized within each block. The
effect of vegetation type was tested using the block
within vegetation type error term. The other main
effects and interactions were tested using the residual
error term. Data were log transformed when necessary
to meet assumptions of normality and homoscedasticity. Only ®nal height measurements are reported
since trends in height growth by treatment were consistent through the study. Throughout this paper,
means and standard errors are reported and p<0.05
is considered signi®cant.
Fig. 1. Total above-and below-ground seedling biomass for
seedlings grown in grass or shrubs with trenching (Tr) and/or
clearing (Cl) treatments. All treatments had a significant effect on
total biomass (veg ± p<0.01, clear ± p<0.01, trench ± p<0.01), but
no interaction terms were significant.
K.D. Holl / Forest Ecology and Management 109 (1998) 187±195
191
Table 2
Seedling biomass (g), root: shoot ratio, and final height (cm) of seedlings grown in shrubs or grass receiving trenching and clearing
treatments a
Habitat
Treatment
Tap root
Fine root
Stem
Leaves
Root:shoot
Height
Grass
Control
Trench
Clear
Trench/Clear
2.10.3
2.50.2
3.70.6
4.30.7
0.70.1
1.10.1
1.30.2
1.80.2
2.60.3
3.40.4
4.18.0
7.01.2
3.60.5
5.50.5
6.51.0
10.61.7
0.810.07
0.700.02
0.770.02
0.630.05
39.73.9
54.04.1
51.46.4
67.88.1
Shrub
Control
Trench
Clear
Trench/Clear
2.00.3
2.00.2
2.70.4
3.20.6
0.90.5
0.50.1
0.70.1
1.60.5
1.80.4
2.00.4
3.40.7
4.60.9
3.00.5
3.90.6
4.91.0
7.31.0
0.800.04
0.760.06
0.720.05
0.700.04
32.23.1
40.24.2
46.25.3
57.45.6
Effects
Veg
Trench
Clear
*
NS
***
**
*
***
**
**
***
NS
*
NS
*
***
***
**
***
***
a
Values are means1 SE. Nˆ10 or 11 for each treatment. NSˆnot significant.
*ˆP<0.05.
**ˆP<0.01.
***ˆP<0.001.
C. brasiliense in all size-classes, whereas clearing had
no effect on root biomass in any size-class (Table 3).
There was a signi®cant vegetationtrenching interaction term for all but the ®ne roots. For very ®ne roots,
the interaction term re¯ects the fact that ®ne root
biomass was much higher under grass than shrubs
in the non-trenched plots, but was similar in the
trenched plots. For the coarse roots, biomass was
higher under shrubs than under grass in non-trenched
plots, but was similar in trenched plots.
Table 3
Root biomass (g/m2) in abandoned pasture below grass and shrubs for three root diameter classes at 0±5 cm depth a
Root diameter class (mm)
Habitat
Treatment
Very fine (<0.5)
Fine (0.5±2.0)
Coarse (>2.0)
Total
Grass
Control
Clear
Trench
Trench/Clear
87.713.4
84.014.2
15.55.2
18.26.3
51.010.1
39.27.4
5.71.9
6.82.3
19.99.7
11.13.4
0.20.2
0.50.4
158.625.1
134.319.6
21.46.2
25.68.0
Shrub
Control
Clear
Trench
Trench/Clear
40.76.9
35.45.0
15.16.1
16.62.2
24.54.2
25.68.7
6.13.6
7.54.3
34.612.8
18.87.1
0.40.4
00
99.814.2
79.814.2
21.64.9
24.15.0
Effects
Veg
Trench
Clear
Veg*Trench
NS
***
NS
***
NS
***
NS
NS
a
Values are means1 SE. Nˆ11 for each vegetation type. NSˆnot significant.
*ˆP<0.05.
**ˆP<0.01.
***ˆP<0.001.
NS
***
NS
*
NS
***
NS
**
192
K.D. Holl / Forest Ecology and Management 109 (1998) 187±195
4. Discussion
These results, along with previous studies (Gerhardt
and Fredrikkson, 1995; GonzaÂlez Montagut, 1996;
Guariguata et al., 1995; Sun and Dickinson, 1996;
Sun et al., 1995), clearly demonstrate that competition
with grasses strongly limits tree seedling growth in
abandoned tropical pastures. Little previous research
has compared the effect of pasture grasses and colonizing shrubs on seedling growth in abandoned tropical pastures. Gerhardt and Fredrikkson (1995),
working in tropical dry forest, reported higher growth
rates of Swietenia macrophylla (mahogany) seedlings
in pasture compared to that in patches of secondary
tropical dry forest in Costa Rica. These results agree
with the results of the current study that, across all
treatments, seedling growth was slightly higher in
areas of pasture grass than in areas of shrubs.
There are several possible explanations for this
result. First, some shrub species may have allelopathic
effects on tree seedling growth. A few previous studies
suggest that a number of tropical shrubs and trees emit
chemicals that inhibit seed germination and radicle
elongation (Anaya Lang, 1976a; Anaya Lang, 1976b,
b; Campbell et al., 1989). However, there has been
little research on the potential for allelopathic chemical reduction of seedling growth in the tropics. It is an
area that requires further research.
A second possible explanation for the higher growth
of seedlings in grass may result from differences in
rooting depths. It has been suggested that plants that
have different rooting depths may exhibit higher
productivity when grown together than species that
exploit the same rooting depth (Berendse, 1981; Ewel
et al., 1982; Wilson, 1988). At the present study site,
grass roots are predominantly concentrated in the ®rst
5 cm of soil, whereas roots of C. brasiliense and
shrubs exploit a wider range of depths (Holl, pers.
obs.). This difference in rooting depths might explain
higher growth rates of C. brasiliense in the grass
control and cleared treatments, but would not explain
this trend in the sites where root competition was
reduced.
Higher growth in grass compared to shrubs cannot
be explained by differences in soil nutrients or root
density. Some nutrients (Mg and Ca) were actually
higher under shrubs, and the nutrient most likely to be
limiting tree growth, P, did not differ between the two
vegetation types. Very ®ne root density was higher
under grasses. Smaller diameter roots are comparatively more ef®cient in the uptake of nutrients due to a
larger surface area to biomass ratio (Ewel et al., 1982;
Jungk, 1991). Therefore, these results suggest higher
root competition for seedlings planted in grass without
the trenching treatment. Presumably, higher root competition would result in reduced growth rates for
seedlings planted under grass than under shrubs, but
the reverse was observed. However, differences in root
physiology (e.g. absorptivity, mycorrhizal associations) among species may be more important to
nutrient and water uptake than the actual number of
roots, so it is dif®cult to draw conclusions from root
biomass or root length measurements alone.
It is also unlikely that the differences in growth rates
could be explained by water stress during the dry
season since gravimetric water content in areas of
cleared grass in February 1997 were well above 0.31
(Holl, in press), the level at which water potential for
this soil reached ÿ1.5 MPa, which is commonly
considered to be permanent wilting point (Taiz and
Zeiger, 1991). In other words, soil moisture did not
appear to be limiting during the study period.
Although both above- and below-ground competition reduced seedling height and biomass, aboveground competition appeared to have a stronger overall effect. Previous studies in tropical forest clearly
demonstrate that many forest trees grow faster when
exposed to higher light levels (e.g. Augspurger, 1984;
Butter®eld and Fisher, 1994). However, there have
been few previous studies comparing above- and
below-ground competition in pastures. Two studies in
tropical secondary forests (Gerhardt and Fredrikkson,
1995; Pinard et al., in press) reported that reducing
canopy cover signi®cantly increased seedling growth,
but that root trenching did not have a signi®cant effect.
Gerwing (1995) reported that the relative effect of
above- and below-ground competition on the growth
of two species of Piper in primary tropical forest
depended on the morphology of the tree species under
which they were grown.
In the temperate zone, results of studies comparing
the relative effects of above- and below-ground competition are equally variable. In a review of competition experiments, predominantly on temperate
herbaceous species, Wilson (1988) concluded that
in the majority of experiments below-ground compe-
K.D. Holl / Forest Ecology and Management 109 (1998) 187±195
tition was important, but that there were studies in
which the effects of above-ground competition were
overriding. Research in temperate old ®elds suggests
that the relative importance of below-ground competition increases with decreasing soil fertility and moisture (Putz and Canham, 1992). Clearly, the relative
importance of above- and below-ground competition
is highly site- and species-speci®c. Therefore, more
research in the tropics is necessary before generalizations can be made.
Not surprisingly, root:shoot ratios were lower for
trenched plants. Previous studies have clearly demonstrated reduced allocation to roots when there is less
competition for nutrients (Berendse, 1981; Gerhardt
and Fredrikkson, 1995).
Growth of C. brasiliense was fairly slow (25 cm/
year overall) even in plots with reduced competition.
Seedling height increases at the current study site were
much lower than the values reported for lowland
regions of Costa Rica, where C. brasiliense grew
1.5 m/year. (Butter®eld and Espinoza, 1995; Guariguata et al., 1995). In contrast, Kellman (1985)
reported growth rates of only 5 cm/year for C. brasiliense grown in a savanna in Belize. These differences
in growth rates are likely due to a combination of
differences in temperature (largely due to elevation),
rainfall, and soil fertility at the various sites.
A number of researchers have suggested that
rapidly colonizing shrubs have positive effects on
succession in abandoned tropical pastures (Aide et al.,
1995, 1996; Nepstad et al., 1990; Vieira et al., 1994).
Vieira et al. (1994) suggest that one strategy for
facilitating recovery might be to introduce early-successional shrubs. Results reported here show that
shrubs may have negative effects on some stages of
succession. Previous research, predominantly in the
temperate zone, has demonstrated that complex combinations of negative and positive interactions exist in
many plant communities (Callaway and Walker,
1997). It is clear that more research on the role of
shrubs in succession is needed before shrubs are
introduced on a wide-scale to help restore abandoned
pastures.
Results of this study highlight the importance of
reducing above-ground competition to increase the
growth of young tree seedlings planted as part of
reforestation projects. In Costa Rica, land-owners
usually clear grass around seedlings 4±8 times per
193
year for the ®rst year or two after planting (Montagnini
and Sancho, 1990; Butter®eld, 1995). Another method
that has been recommended for reducing competition
is burning in order to reduce grass competition before
planting (Nepstad et al., 1990). Although these techniques add costs to reforestation programs, they are
clearly necessary to ensure rapid seedling growth.
Acknowledgements
This research was supported in part by a Global
Change Distinguished Postdoctoral Fellowship sponsored by the US Department of Energy, Of®ce of
Health and Environmental Research. Additional funding was provided by grants from the American
Philosophical Society, Earthwatch and its Research
Corps, and the National Science Foundation (Grant
DEB-9508683).This project could not have been completed without the ®eld assistance of N. Messmore, E.
Quiros Nietzen, J. Small, and 21 enthusiastic Earthwatch volunteers. I appreciate the helpful comments
of G. Hayes, B. Lindh, M. Loik, and F. Rein.
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