Cattle and Weedy Shrubs
as Restoration Tools of
Tropical Montane
Rainforest
(camargo), but the largest effect was seed addition.
Where grasses are an important barrier to regeneration, grazing can facilitate the establishment of shrubs
that create a microhabitat more suitable for the establishment of montane forest tree species.
Key words: cattle, restoration, grazing, shrubs, montane pastures, tropics.
Introduction
Juan M. Posada1,2
T. Mitchell Aide3
Jaime Cavelier4
Abstract
Over the last 150 years, a large proportion of forests in
Latin America have been converted to pastures. When
these pastures are abandoned, grasses may slow reestablishment of woody species and limit forest regeneration. In this study, we explored the use of cattle
in facilitating the establishment of woody vegetation
in Colombian montane pastures, dominated by the
African grasses Pennisetum clandestinum (Kikuyo) and
Melinis minutiflora (Yaraguá). First, we described woody
and herbaceous vegetation in grazed and non-grazed
pastures. Second, we tested the effect of grazing and
seed addition on the establishment and growth of
woody species. We also determined if the effect of grazing was different in P. clandestinum and M. minutiflora
pastures. We found that low stocking density of cattle
greatly increased density, number of branches per individual (a measure of “shrubiness”), and basal area of
woody species, but also reduced woody plant species
richness and diversity. In the grazed area, the shrubs
Baccharis latifolia (Chilca) and Salvia sp. (Salvia)
were the most abundant. The combined effect of grazing and shading from the shrubs reduced herbaceous
vegetation by 52 to 92%. In the grazing/seed addition
experiment, grazing increased establishment of woody
seedlings, particularly of the shrub Verbesina arborea
1Department
of Botany, University of Florida, 220 Bartram
Hall, P.O. Box 118526, Gainesville, FL 32611–8526, U.S.A.
2Address correspondence to J. M. Posada, email posada@
botany.ufl.edu
3Department of Biology, P.O. Box 23360, University of Puerto
Rico, San Juan, Puerto Rico 00931–3360
4Departamento de Ciencias Biológicas, Universidad de los
Andes, AA 4976, Bogotá, Colombia
© 2000 Society for Ecological Restoration
370
I
n the neotropics, extensive areas of mid-altitude tropical montane forest have been deforested for the establishment of agricultural lands (Houghton et al. 1991),
particularly coffee plantations (Parsons 1979; Molano
1992). At high elevations, forests were used for the extraction of timber and charcoal and then converted to
pastures for cattle grazing (Parsons 1975). These cattle
pastures, dominated by introduced African grasses,
have been maintained for decades by high density grazing, weeding of colonizing woody species, and the use
of fire in areas where rainfall is strongly seasonal.
Once pastures are abandoned, the rate of forest recovery depends on the degree of site degradation (Aide
& Cavelier 1994). Forest regeneration in areas subject to
intense grazing, long-term use, and soil erosion, can be
very slow or may never occur. Although many pastures
are abandoned because of reduced productivity, economic and sociopolitical changes can result in the abandonment of highly productive pastures (Stonich & DeWalt 1996). In these sites, forest regeneration can also be
inhibited because of competition with aggressive native
and introduced grasses (Aide et al. 1995). The high aboveand belowground biomass of these grass species can impede seed germination, survivorship, and growth of forest species as has been shown for abandoned Amazonian pastures (Buschbacher 1986; Nepstad et al. 1990).
To accelerate forest regeneration in these productive
grasslands, competition from grasses needs to be reduced. Mechanical (machete) or chemical (herbicide)
methods can reduce grass biomass. These techniques
are effective for forest restoration at a small spatial
scale, but they are costly to implement for large-scale
projects. Although cattle ranching produced and helped
maintain these grasslands (Faminow 1998), grazing animals are a potential tool for reducing grass biomass and
facilitating the colonization of woody species (Zimmerman & Neuenschwander 1984; Janzen 1986, 1988a; Archer
1994; Belsky & Blumenthal 1997). Even if grass biomass
is reduced, forest regeneration can be limited by seed
availability (Thébaud & Strasberg 1997). Although the
majority of tropical tree species are animal dispersed
(Howe & Smallwood 1982), initial colonization in the
grasslands is dominated by wind-dispersed species (CaveRestoration Ecology Vol. 8 No. 4, pp. 370–379
DECEMBER 2000
Restoration of Montane Rain Forest in Colombia
lier & Aide, unpublished data). In these ecosystems,
most wind-dispersed species are weedy shrubs or small
trees in the Asteraceae that normally occur in frequently disturbed areas and are not the pioneer species
in mature forest gaps. Direct planting of most forest
species into the grasslands is likely to be unsuccessful,
due to slow growth rate, competition with grasses, and
physiological limitations (Cavelier & Aide, unpublished
data). The establishment of these wind-dispersed species can enhance forest regeneration by shading the
grass and creating a microclimate for the germination
and establishment of forest species (Guimãres-Vieira et
al. 1994; Lamb et al. 1997).
The goal of this project was to understand how grazing
can be used to reduce grass biomass and enhance colonization of weedy shrub species in abandoned pastures. First,
we described the biomass of herbaceous species, as well as
abundance, species composition, and canopy structure of
woody species in two pastures that had been abandoned
for 3 years. One pasture was not grazed after abandonment, while the other was grazed at a very low density and
did not receive any weed management. Second, we measured the density of woody plants occurring in neighboring farms that were managed to raise cattle. Finally, we experimentally tested the effect of grazing and seed addition
on woody seedling establishment and growth.
individuals) in abandoned pastures, most pastures were
abandoned and received no management. These pastures were dominated by the African grasses Pennisetum
clandestinum (Kikuyo) and Melinis minutiflora (Yaraguá)
that were originally introduced by ranchers to increase
cattle productivity. P. clandestinum was found on flat areas, where soils had slightly higher fertility, while M.
minutiflora was found on slopes with less fertile soils
(Cavelier & Aide, unpublished data). Three years after
abandonment, P. clandestinum had an average aboveground biomass (including stolon mat) of 18.8 tons/ha
and an average productivity of 18.4 tons ha⫺1 yr⫺1. In
contrast, M. minutiflora had an aboveground biomass of
11.5 tons/ha and a productivity of 7.5 tons ha⫺1 yr⫺1
(Cavelier & Aide, unpublished data). Aerial biomass was
similar between the two grasses, while root biomass
tended to be lower in M. minutiflora. The largest difference between the two grass types was the investment in
stolon biomass (Fig. 1).
Natural Regeneration With or Without Grazers
Natural regeneration was described in two large (20–40
ha), adjacent pastures. Cattle were completely removed
Materials and Methods
Study Site
The study was carried out at La Sierra Ranch located in
the municipality of Pijao, Department of Quindío, Colombia, at 2,000–2,200 m elevation. Average annual temperature at 2,100 m is 16.8⬚C, with an average annual
maximum of 22.3⬚C and an average annual minimum of
11.2⬚C. Between 1991 and 1995, annual precipitation varied between 1,652 and 2,135 mm/yr. Periods of low precipitation occur from December to January and June to
September. During the study period (1995–1997), we did
not observe fires in the region.
The study area was deforested between 1920 and
1930 for the extraction of timber and charcoal production. Since then, the study site had been used mainly for
cattle ranching until the early 1990s (R. Hernández 1994,
personal communication). In 1991, the Regional Corporation for development and natural resources conservation of Quindío (CRQ) bought La Sierra ranch and an
adjacent cattle ranch (La Cristalina) to protect the watershed of the Río Lejos and prevent large landslides
and avalanches in the town of Pijao. Although the CRQ
planted some exotic trees (Pinus patula [Pino Pátula]—
34,000 individuals; Cupressus lusitanica [Ciprés]—25,000
individuals) and native trees (Juglans neotropica [Cedro
Negro]—1,020 individuals; Alnus acuminata [Aliso]—279
DECEMBER 2000
Restoration Ecology
Figure 1. Distribution of above- and belowground biomass of
P. clandestinum and M. minutiflora grasses. Stolons occur above
the surface soil. The values are the mean of six samples. For P.
clandestinum, the standard error of the mean were, 147 g/m2 for
aerial biomass, 146 g/m2 for stolons and 99 g/m2 for roots. For
M. minutiflora, the standard error of the mean were, 159 g/m2
for aerial biomass, 34 g/m2 for stolons and 66 g/m2 for roots.
371
Restoration of Montane Rain Forest in Colombia
from one pasture in September 1992, while in the other
pasture a maximum of ten cows and seven horses and
mules were allowed to graze. In this pasture, the grazer
density was 0.4–0.7 individuals ha⫺1 yr⫺1, which is almost 10 times lower than what pastures can support in
the region (3–6 individuals ha⫺1 yr⫺1; Cavelier & Aide,
unpublished data). Both pastures had steep slopes
dominated by M. minutiflora and a few scattered flat areas dominated by P. clandestinum. Other than grazing,
neither pasture was subjected to any management practices that would reduce the colonization of woody
plants (Figs. 2a & 2b).
In both pastures, woody vegetation was measured in
transects 1 ⫻ 30 m, placed perpendicular to the slope. In
each transect, all woody plants higher than 1.3 m were
identified and measured (height and diameter). Shrub
branches, which originated below 0.5 m and also attained heights above 1.3 m, were measured individu-
ally. These branches were a measure of the size of the
shrub canopy, which we refer to as plant “shrubiness.”
Ferns higher than 1.3 m were also included in the censuses. Six transects were placed on each grass type (P.
clandestinum and M. minutiflora) and in each pasture
(grazed and not grazed), for a total of 24 transects.
In both pastures and both grass types, herbaceous vegetation was described in three 1 ⫻ 1 m quadrants. In each
plot, aboveground vegetation was cut and sorted into five
categories: P. clandestinum, M. minutiflora, ferns, herbs, and
other species of grass. After sorting, each sample was dried
at 60°C and then weighed. Ferns higher than 1.3 m in
height were excluded. Samples were collected in June 1995.
Active Pastures
Woody vegetation was described in pastures of neighboring farms that were managed for cattle. We refer to
Figure 2. Natural regeneration in abandoned cattle pastures. a) There was no grazing after abandonment in this site. Note the
dominance of P. clandestinum in the flatter area and M. minutiflora on the slope. b) This pasture was abandoned at the same time,
but was occasionally grazed at low densities and is now dominated by shrubs.
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Restoration of Montane Rain Forest in Colombia
these pastures as active to distinguish them from nonmanaged pastures. In each farm, we counted and identified all individuals of woody species greater than 10 cm
in height in six 1 ⫻ 30 m transects (three in P. clandestinum,
and three in M. minutiflora). This minimum height was
much lower than in the transects done in the two nonmanaged pastures (1.3 m; see above), because farmers
frequently cut woody vegetation. Three farms were
censused in July 1996 and three more were censused in
November 1996.
Corral Experiment
To experimentally test the effect of grazing on the establishment of woody seedlings, twelve 20 ⫻ 20 m corrals
were delimited in pastures that had not been grazed for
3 years. Six corrals were dominated by M. minutiflora
and six were dominated by P. clandestinum. Within each
grass type, three sites were assigned as controls and
three sites as treatments. The treatment corrals were enclosed with a three stranded barbed wire fence, 1.5 m
tall. From February to mid-April 1995, two heifers and
two young bulls were rotated through the treatment
corrals to reduce the grass biomass to levels similar to
that in active pastures.
In mid-April 1995, we established at random 12 circular plots (1 m radius) in each corral to evaluate the effect
of seed addition. Six plots were used as controls and six
plots received seeds of five species. Each plot received
seeds of Baccharis latifolia (Chilca; ⵑ25,000 seeds), Verbesina arborea (Camargo; ⵑ800 seeds), Weinmannia pubescens
(Encenillo; ⵑ2,500 seeds), Solanum ovalifolium (ⵑ3,000
seeds), and Leandra melanodesma (Nigüito; ⵑ2,000 seeds).
Seed weight ranged from 0.2 to 20 mg. In July 1995, an additional 1,000 seeds of V. arborea were added to each seed
addition plot. From mid-April to December 1995, grazing
intensity was halved by keeping only one pair of cattle.
The number of individuals and species of woody seedlings were counted in all plots in September 1995. In January 1996, the number and height of V. arborea seedlings
were determined for the seed addition plots. The herbaceous vegetation in the corrals was collected in 1 ⫻ 1 m
quadrants, in June 1995. The vegetation was then sorted
and weighed following the same procedure described
above.
woody seedlings in the corrals (treatment and controls)
were analyzed with a split-split-plot design. In this model,
block was considered a random effect, while grass species,
grazing and seed addition were considered fixed treatment effects. Each block included two pairs of corral and
control plots (one pair per grass species). The average
number of days with cattle and carrying capacity (individuals ha⫺1 yr⫺1) of P. clandestinum and M. minutiflora pastures were compared with a t-test. A Wilcoxon-MannWhitney test was used to test for differences in density of
woody individuals in P. clandestinum and M. minutiflora
in the active pastures.
Results
When comparing the two large pastures, density of
woody vegetation was higher in the grazed than in the
non-grazed pasture (F ⫽ 6.14, p ⫽ 0.022; Fig. 3). With
grazing, an average of 70% more individuals established in M. minutiflora and P. clandestinum, compared
to the pasture without grazing. More individuals estab-
Data Analysis
Shannon’s diversity index, Pielou’s evenness index, and
Sorensen’s similarity index were used to describe the
woody vegetation in the grazed and ungrazed pastures.
We used two-way analysis of variance models to analyze the data describing the structure of the woody vegetation, aboveground herbaceous biomass, and height
and number of V. arborea seedlings. The numbers of
DECEMBER 2000
Restoration Ecology
Figure 3. Density of woody plants (individuals/m2), basal
area (cm2), and number of branches per individual in a grazed
and a non-grazed field. Measurements were taken in pastures
of P. clandestinum and M. minutiflora. Bars represent means,
and vertical lines the standard error of the mean (n ⫽ 6
transects; n ⫽ 5 for branches per individual in P. clandestinum
pastures, in the non-grazed field).
373
Restoration of Montane Rain Forest in Colombia
Table 1. Woody species in grazed and non-grazed pastures, dominated by P. clandestinum (Pc) or M. minutiflora (Mm) grasses.*
Number of individuals, species richness, Shannon’s diversity index, and Pielou’s eveness index are reported.
No Grazing
Family
Asteraceae:
Malvaceae:
Melastomataceae:
Polypodiaceae:
Species Name
Ageratina gracilis (H.B.K.) R. M. King & H. Robinson
Astrocopatorium inulaefolium (H.B.K.) R. M. King & H. Robinson
Baccharis latifolia Pers.
Vernonia canescens H.B.K.
Sida sp.
Monochaetum hartwegianum Naud.
Dennstaedtia aff. cicutaria (Sw.) Moore
Pteridium aquilinum (L.) Kuhn
Thelypteris aff. rudis (Kunze) Proctor
Pc
Mm
2
2
5
7
6
1
1
3
1
4
1
3
4
5
Number of individuals
Number of species
Shannon’s diversity index
Pielou’s evenness index
14
7
1.81
0.93
31
7
1.84
0.95
Family
Species List
Pc
Mm
Asteraceae:
Baccharis latifolia Pers.
Salvia sp.
Leandra melanodesma (Naud.) Cogn.
sp. 1
sp. 2
4
16
14
40
8
1
1
Number of individuals
Number of species
Shannon’s diversity index
Pielou’s evenness index
20
2
0.50
0.72
64
5
1.02
0.63
Grazing
Melastomataceae:
Unidentified
* In each grass and grazing “treatment” we sampled 180 m2, in six 1 ⫻ 30 m transects.
lished in M. minutiflora than in P. clandestinum (F ⫽ 6.94,
p ⬍ 0.001), independently of the presence or absence of
grazing animals (no significant interaction; F ⫽ 1.63,
p ⫽ 0.217). Mean basal area of woody plants was higher
in the pasture with grazing than in the non-grazed pasture (F ⫽ 14.23, p ⫽ 0.001; Fig. 3). Grazing increased
basal area by 85% in P. clandestinum and by 250% in M.
minutiflora. Basal area was higher in M. minutiflora than
in P. clandestinum (F ⫽ 12.24, p ⫽ 0.002), but the effect
also depended on the grazing treatment (significant interaction; F ⫽ 6.25, p ⫽ 0.021). The interaction was interpreted as basal area increasing more in M. minutiflora
than P. clandestinum, with grazing (Fig. 3). The average
number of branches per individuals, a measure of “shrubiness,” was approximately two times greater in grazed
versus non-grazed pastures (ln-transformed data; F ⫽
10.30, p ⫽ 0.005; Fig. 3). Branching was not influenced by
the grass species (F ⫽ 0.64, p ⫽ 0.4). The average height
of woody vegetation ⬎ 1.3 m tall was 2 m, and there was
no significant effect of grazing (F ⫽ 1.35, p ⫽ 0.26) or
grass type (F ⫽ 0.5, p ⫽ 0.8; data not shown).
In summary, grazing caused an increase in density of
woody individuals, basal area, and number of branches
per individual, but had no effect on plant height. Density and basal area were higher in M. minutiflora than in
374
P. clandestinum pastures, while height and number of
branches per individual were the same.
The grazed and non-grazed pastures had relatively
simple community composition (Table 1). Species richness of woody plants was lower in the pasture with
grazing than in the pasture without grazing, despite the
former having more individuals. Asteraceae was the
family with most individuals, particularly in the grazed
pasture where Baccharis latifolia and Salvia sp. represented about 90% of all individuals. We found no ferns
(Polypodiaceae) taller than 1.3 m in the grazed pasture.
Pastures of M. minutiflora had about twice the number
of individuals of woody plants without grazing, and
about three times more individuals when grazed, in
comparison with areas dominated by P. clandestinum.
The number of species of woody plants was the same in
P. clandestinum and M. minutiflora in the pasture without grazing, but was higher in M. minutiflora when
grazing occurred. Species diversity and evenness were
lower in the grazed pasture, than in the pasture without
grazing (Table 1). Diversity was higher in M. minutiflora
than in P. clandestinum when grazing took place. In the
non-grazed pasture, diversity and evenness were very
similar in the two grass species. Sorensen’s index shows
that the grazed and non-grazed pastures had only 17–
Restoration Ecology
DECEMBER 2000
Restoration of Montane Rain Forest in Colombia
22% similarity (Table 2). Only B. latifolia was common
to both pastures (Table 1). The species composition was
most similar between P. clandestinum and M. minutiflora
pastures that had experienced the same grazing treatment (no grazing—71%; grazing—57%; Table 2). These
results suggest that grazing, and to a lesser extent the
dominant grass species, were important factors influencing woody plant colonization.
Grazing significantly reduced the aboveground biomass of herbaceous vegetation (ln-transformed data;
F ⫽ 80.69, p ⬍ 0.001; Fig. 4). There was no detectable
difference between the two grass species (F ⫽ 0.31, p ⫽
0.591), but there was an interaction between grazing
and grass species (F ⫽ 5.61, p ⫽ 0.045). This interaction
was interpreted as grazing reducing the aboveground
biomass of M. minutiflora more (78% reduction) than the
biomass of P. clandestinum (61% reduction; Fig. 4). In areas dominated by P. clandestinum, the percent biomass
of this grass decreased from 91% in the non-grazed pasture to 59% in the grazed pasture (Fig. 4). The decrease
in percent P. clandestinum was associated with an increase in the percentage of herbs and other grass species.
In areas dominated by M. minutiflora, the percent biomass of this grass declined from 85 to 23% when grazed
and there was a greater proportion of ferns and herbs.
In active pastures, the average density of woody individuals taller than 10 cm was 0.5 individual/m2. There
was a marginal difference between M. minutiflora and P.
clandestinum pastures (Z ⫽ ⫺1.86, p ⫽ 0.064; WilcoxonMann-Whitney test with normal approximation), suggesting that more individuals established in M. minutiflora (Fig. 5). Between farms, density varied from 0.0 to
1.0 woody individual/m2 in P. clandestinum and from
0.3 to 1.5 woody individual/m2 in M. minutiflora. The
large variance in density was due to the frequency of
weeding woody vegetation (i.e., cutting, pulling, or herbicide). Some pastures were weeded twice per year and
others only once every two years. Ferns were the most
common individuals in both grass types, followed by
individuals of the family Asteraceae (Fig. 5). Salvia sp.,
B. latifolia, and L. melanodesma, the three most abundant
species in the pasture with grazing (Table 1), were common in these active pastures.
Table 2. Sorensen’s similarity index of woody species in grazed
and non-grazed pastures, dominated by P. clandestinum (Pc) or
M. minutiflora (Mm) grasses.
No grazing Pc
No grazing Mm
Grazing Pc
Grazing Mm
DECEMBER 2000
No Grazing
Pc
No Grazing
Mm
Grazing
Pc
Grazing
Mm
1
0.71
1
0.22
0.22
1
0.17
0.17
0.57
1
Restoration Ecology
Figure 4. Total dry weight of aboveground herbaceous vegetation (g/m2) in pastures with and without grazing, and in
pastures dominated by grasses of P. clandestinum and M.
minutiflora. Bars represent means, and vertical lines the standard error of the mean (n ⫽ 3).
In the corral experiment, a pair of young bulls or heifers
was kept for twice the number of days in enclosures on P.
clandestinum pastures (3.64 d/month ⫾ 1.2), than in enclosures on pastures of M. minutiflora (1.73 ⫾ 0.05; t ⫽ 3.56, p ⫽
0.023). Similarly, carrying capacity was two times larger in
P. clandestinum (6.7 individuals ha⫺1 yr⫺1 ⫾ 1.2) than in M.
minutiflora (3.3 individuals ha⫺1 yr⫺1 ⫾ 0.2, t ⫽ 3.56, p ⫽
0.023), showing that P. clandestinum pastures had higher
productivity. After six months of grazing, aboveground
herbaceous biomass was significantly reduced in comparison with the control corrals (ln-transformed data; F ⫽
29.25, p ⬍ 0.001; Fig. 6). In both the control and treatment
corrals, the aboveground biomass was greater in areas
dominated by P. clandestinum in comparison with M.
minutiflora (F ⫽ 19.59, p ⫽ 0.002) and each species responded differently to grazing (interaction; F ⫽ 11.26, p ⫽
0.010). The interaction was interpreted as grazing having
a larger negative impact on the biomass of M. minutiflora
pastures (92% reduction), than on P. clandestinum pastures (52% reduction; Fig. 6). In both grass types, grazing increased the proportion of the dominant grass species (P. clandestinum 92% to 100%; M. minutiflora 63 to
67%) (Fig. 6).
Adding seeds to grazed and control corrals dramati375
Restoration of Montane Rain Forest in Colombia
Figure 5. Density of woody plants in P. clandestinum and M.
minutiflora pastures, in actively managed cattle pastures. Each
bar corresponds to the average. The vertical lines represent
the standard error of the mean of the overall density (n ⫽ 6
farms; the mean density per farm was used in the calculations).
cally increased the number of seedlings of woody species (F ⫽ 57.64, p ⫽ 0.017, log-transformed data; Fig. 7).
There was no detectable effect of grazing (F ⫽ 7.14, p ⫽
0.116) or grass species (F ⫽ 0.68, p ⫽ 0.498) on the number of established individuals. However, we found a
significant interaction between seed addition and grazing (F ⫽ 19.32, p ⫽ 0.048), indicating that more seedlings established when seed were added to the grazing
treatment, than when added to control plots (Fig. 7). At
the end of the experiment, the most common species
was the shrub V. arborea. The effect of grazing on the
number of V. arborea seedlings was marginally significant (log-transformed data, F ⫽ 5.26, p ⫽ 0.051), suggesting that more individuals were present in the grazing treatment than in control plots (Fig. 8). More
individuals survived in M. minutiflora than in P. clandestinum pastures (F ⫽ 8.59, p ⫽ 0.019), and there was no
interaction between the type of pasture and grazing
(F ⫽ 2.17, p ⫽ 0.179). V. arborea seedlings were taller in
grazed corrals than in controls (F ⫽ 35.92, p ⬍ 0.001;
Fig. 8), suggesting that grazed areas were more favorable for growth, than non-grazed areas. Height was not
different between P. clandestinum and M. minutiflora pas376
Figure 6. Total dry weight of aboveground herbaceous vegetation (g/m2) in grazed corrals and control plots, and in pastures dominated by grasses of P. clandestinum and M. minutiflora. Bars represent means, and vertical lines the standard
error of the mean of the entire column.
tures (F ⫽ 0.51, p ⫽ 0.500), but the interaction between
grazing and grass species was significant (F ⫽ 9.05, p ⫽
0.020). When grazing occurred, V. arborea seedlings
were taller in P. clandestinum than in M. minutiflora, but
the opposite happened when pastures were not grazed
(Fig. 8).
Discussion
The colonization of woody species in abandoned pastures depends on previous land use practices, grazing
systems, and the dominant grass species (e.g., Alzérreca-Angelo et al. 1998). Active pastures with low grass
biomass due to heavy grazing are continuously colonized by many species of ferns and woody shrubs (e.g.,
Salvia sp., B. latifolia, and L. melanodesma). Once these pastures are abandoned, the relative proportion of grasses
and woody vegetation will depend on previous management practices. Pastures that were frequently weeded
will result in grasslands with high grass biomass, while
areas that have not been frequently weeded should
quickly become dominated by weed shrub species and
have lower grass biomass. Virtually all species that colRestoration Ecology
DECEMBER 2000
Restoration of Montane Rain Forest in Colombia
Figure 7. Number of individuals of woody species in corrals
(“grazing”) and in control plots (“no grazing”), in P. clandestinum and M. minutiflora pastures. Measurements were taken in
subplots where seeds were added (“+ seeds”) and in control
subplots (“no seeds”). Bars represents the average of three
corrals or control plots, and vertical lines the corresponding
standard error of the mean (note that subplots within corrals
and control plots were averaged).
onized the abandoned pastures in this study have small
wind-dispersed seeds (Bartholomäus et al. 1990), which
should facilitate dispersal not only to forest edges, but
also to large pastures.
The differences in biomass between the two dominant grass species (P. clandestinum and M. minutiflora)
also affected herbaceous and woody plant colonization.
Ferns, herbs, and other grasses were less common in areas dominated by P. clandestinum. Density and basal area
of woody species were lower in P. clandestinum than in M.
minutiflora, while height and number of branches per individual were the same. The lower density and basal area
of woody plants in P. clandestinum in comparison with M.
minutiflora was due to differences in biomass allocation.
Thirty-five percent of aerial biomass of P. clandestinum
was allocated to stolons (Fig. 1) creating a physical barrier
that appears to inhibit seed germination and seedling establishment. Seedlings that germinated within the stolon
mat rarely established due to low light and mechanical
damage by fast growing grass shoots of P. clandestinum
(Cavelier & Aide, unpublished data). Even wire flagging
was twisted and disappeared under the grass within a
few weeks. In contrast, M. minutiflora allocated much
DECEMBER 2000
Restoration Ecology
Figure 8. Number and height of V. arborea seedlings in corrals
(“grazing”) and control plots (“no grazing”), in pastures of P.
clandestinum and M. minutiflora. We considered seedlings only occurring in subplots where seeds were added. Bars represent averages and vertical lines the standard error of the mean (n ⫽ 3).
less biomass to stolons. We observed more open spaces
at the soil surface in M. minutiflora, which should have
permitted greater colonization of non-grass species. The
greater allocation to stolons may explain why aboveground biomass of P. clandestinum was less affected by
grazing in comparison with M. minutiflora (i.e., statistical interactions between grazing and grass species).
Many studies have reported decreases in grass biomass and changes in the composition and density of
colonizing woody species with the presence of livestock
grazing (Smith 1967; Zimmerman & Neuenschwander
1984; Janzen 1988b; Archer 1994; Belsky & Blumenthal
1997). After reviewing the available studies, Archer
(1994) concluded that selective grazing by livestock was
the major factor favoring the establishment of unpalatable woody species over graminoids in western temperate grasslands of North America. Similarly, Belsky and
Blumenthal (1997) concluded that livestock grazing was
a central factor in favoring the establishment of woody
species over grasses in open coniferous forests of the
western United States. The same pattern was observed
in this study, when comparing the grazed and nongrazed pastures. In both P. clandestinum and M. minutiflora, grazing reduced grass biomass by more than 50%
377
Restoration of Montane Rain Forest in Colombia
and increased the number of woody plants, herbs and
other grass species. These changes were greater in M.
minutiflora, probably due to the lower productivity and
greater sensitivity of this species to grazing. The establishment of weedy shrub species in the low density
grazed pasture also contributed to the decrease in grass
biomass possibly because of an increased in “shrubiness” leading to greater shading. Although the dominant grass species had an important effect on woody
species colonization, the species composition of a pasture was mainly determined by the presence or absence
of grazing. The density of woody species was much
greater in the grazed pasture, but the diversity was
much lower. The low-density grazed area was dominated by B. latifolia and Salvia sp., two species that were
also present in the active pastures. These species have
strongly aromatic leaves, and species of both genera are
known to have secondary compounds that might be
toxic for grazing animals (Idrobo 1992; Viola et al. 1997;
Rizzo et al. 1997).
Although grazing increases the establishment of
woody species, the corral experiment demonstrated
that increased seed availability might be a more important limiting factor for forest recovery. Although weedy
shrubs, like V. arborea, are wind dispersed and seeds are
produced in great numbers, seed addition of these species could accelerate woody plant establishment. Once
these shrub species are established in the abandoned
pastures, they will act as perches for small birds that
can increase seed dispersion, as has been shown for the
shrub Cordia multispicata in Amazonian pastures (Guimarães-Vieira et al. 1994) and large isolated trees in lowland
pastures of Mexico (Guevara et al. 1986). In addition to attracting dispersers, these shrubs shade out the herbaceous vegetation creating a microhabitat that can enhance
the survivorship of forest species. For example, seedlings
of Billia columbiana (Hippocrateaceae) and Pouteria sp. (Sapotaceae) planted in open pastures produced symptoms
of photoinhibition and water deficit within a few weeks,
but individuals planted under the partial shade of Baccharis latifolia or Leandra melanodesma showed no symptoms
(Cavelier & Aide, unpublished data).
Conclusions/Implications
The complete elimination of grazing in highly productive grasslands can result in areas of high grass biomass
that inhibit the colonization of woody species. Grazing,
even at low density, can reduce grass biomass, facilitating the establishment of weedy shrubs that can further
reduce grass biomass by shading and create a microclimate suitable for the germination and establishment of
forest tree species. This process can be accelerated by
adding large quantities of seeds of shrub species. Seed
addition will be most successful when grass biomass is
378
low, immediately after abandonment or during a grazing treatment. By combining the use of cattle and weedy
shrubs it might be possible to reduce the main barrier for
forest regeneration in these highly productive grasslands. Once shrubs are established, seed rain of forest
species may increase due to increased occurrence of seed
dispersers as has been reported in shrubby pastures in
Amazonia (Silva et al. 1996; Guimãres-Vieira et al. 1994).
For many forest species, direct seeding or planting will
be necessary (Lamb et al. 1997) since dispersal from the
parent tree, particularly for large-seeded species, is usually a limiting factor for colonizing open sites (Wunderle
1997). The site preparation to the shrub phase can be accomplished on a large spatial scale with few resources.
In contrast, much effort must be invested in collecting,
germinating, and growing large quantities of many tree
species to restore a high diversity montane forest.
Acknowledgments
Financial support for this project was provided by COLCIENCIAS (convenio/contrato RC No. 121-93, código
1204-13-028-92 to J. Cavelier and T. M. Aide) and NASAIRA to T. M. Aide. We thank the Corporación Autónoma
Regional del Quindío CRQ for providing logistical support in the study area and for allowing us to use the facilities at La Cristalina. In particular, we thank Aureliano
Sabogal, head of the Natural Resources Division at CRQ
for his support. Hildebrando Castaño and his family
were always helpful and made our stay at La Cristalina a
very special and happy experience. The assistance of
Carolina Santos and Giovanny Marín was instrumental
in the establishment and development of this project. We
also thank Jay Harisson, from the Institute of Food and
Agricultural Sciences (IFAS),University of Florida, for
his help with the statistical analysis. This paper also benefited from comments from W. A. Niering and F. Putz.
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