BIOTROPICA 41(5): 608–617 2009
10.1111/j.1744-7429.2009.00517.x
Rapid Recovery of Biomass, Species Richness, and Species Composition in a Forest
Chronosequence in Northeastern Costa Rica
Susan G. Letcher1,3 and Robin L. Chazdon2
1
Organization for Tropical Studies, Apartado Postal 676-2050, San Pedro de Montes de Oca, Costa Rica
2
Department of Ecology and Evolutionary Biology, University of Connecticut, 75 North Eagleville Road, Storrs, CT, 06269-3043, U.S.A.
ABSTRACT
Secondary forests are a vital part of the tropical landscape, and their worldwide extent and importance continues to increase. Here, we present the largest chronosequence
data set on forest succession in the wet tropics that includes both secondary and old-growth sites. We performed 0.1 ha vegetation inventories in 30 sites in northeastern
Costa Rica, including seven old-growth forests and 23 secondary forests on former pastures, ranging from 10 to 42 yr. The secondary forest sites were formerly pasture for
intervals of o 1–25 yr. Aboveground biomass in secondary forests recovered rapidly, with sites already exhibiting values comparable to old growth after 21–30 yr, and
biomass accumulation was not impacted by the length of time that a site was in pasture. Species richness reached old-growth levels in as little as 30 yr, although sites that
were in pasture for 4 10 yr had significantly lower species richness. Forest cover near the sites at the time of forest establishment did not significantly impact biomass or
species richness, and the species composition of older secondary forest sites (4 30 yr) converged with that of old growth. These results emphasize the resilience of tropical
ecosystems in this region and the high conservation value of secondary forests.
Abstract in Spanish is available at http://www.blackwell-synergy.com/loi/btp.
Key words: biodiversity; ecological resilience; land use history; succession; tropical wet forest.
SECONDARY FORESTS PLAY AN INCREASINGLY IMPORTANT ROLE in tropical landscapes. As much as 60 percent of the world’s remaining
tropical forests are degraded or secondary forests (FAO 2005).
These ecosystems are sources of timber and nontimber forest products (Finegan 1992, Wadsworth 1997, Chazdon & Coe 1999), and
biomass accumulation in secondary forests is a sink for anthropogenic carbon emissions (Fearnside & Guimaraes 1996, Houghton et al. 2000, Silver et al. 2000, Zarin et al. 2001, Grace 2004,
Feldpausch et al. 2005). Secondary forests also provide reservoirs
for biodiversity in fragmented landscapes (Chazdon 1998, 2003),
and the potential importance of secondary forests in forestalling the
tropical extinction crisis is hotly debated (Brook et al. 2006; Wright
& Muller-Landau 2006a, b; Barlow et al. 2007; Gardner et al.
2007).
A central question in the study of tropical succession is the extent to which forests can recover from anthropogenic disturbance
(Chazdon 2003, Chazdon et al. 2007). Early studies on tropical
deforestation deemed the process irreversible; Gomez-Pompa et al.
(1972) called the tropical forest a ‘non-renewable resource’. Yet recent insights into the dynamics of tropical forests have revealed that
they are more resilient than previously thought (Lugo 1995, Chazdon 2003, Grau et al. 2003). Natural disturbances—hurricanes,
fires, floods, and droughts—have always been an integral part of
tropical forest dynamics worldwide (Whitmore & Burslem 1998,
Chazdon 2003), and indeed, the history of anthropogenic disturbance in so-called primary forests seems to be widespread (Bush &
Received 30 April 2008; revision accepted 2 January 2009.
3
Corresponding author; e-mail: suletcher@ots.ac.cr
608
Colinvaux 1994, Lugo 2002, Willis et al. 2004, Anchukaitis &
Horn 2005, Heckenberger et al. 2007).
Changes in forest structure, species composition, and ecosystem function during succession can occur at very different rates
(reviewed in Finegan 1996, Guariguata & Ostertag 2001, Chazdon
2008). Biomass generally recovers more rapidly than species richness (Guariguata et al. 1997, Aide et al. 2000, Denslow & Guzman
2000, Chazdon 2008). In many sites, the forest that grows back
after major disturbance is qualitatively and quantitatively different
from the original vegetation. Species composition of secondary forests, in some cases, may not converge with that of old-growth forest
(Aide et al. 2000, Pascarella et al. 2000, Marı́n-Spiotta et al. 2007).
Exotic species may dominate some phases of the regeneration process and eventually form a large portion of the forest canopy, especially in highly disturbed landscapes (Grau et al. 1997, 2003; Lugo
2002; Franklin 2007). Because of this decoupling between structural and floristic components of forest change, different parameters may give very different answers to the question of how well
tropical forests recover from major disturbances (Guariguata &
Ostertag 2001, Chazdon et al. 2007). Even when their structural
and floristic composition differs strongly from that of old-growth
forests, secondary forests can provide important ecosystem services
such as carbon sequestration (Grace 2004, Feldpausch et al. 2005),
protection from erosion (Fearnside & Guimaraes 1996), refugia
for biodiversity in a fragmented landscape (Chazdon 2003), and
sources of timber and non-timber forest products (Chazdon &
Coe 1999).
Land-use history has a strong influence on rates of forest
recovery. In secondary forests at Los Tuxtlas, Mexico, a greater
duration of land use before regeneration led to slower recovery of
r 2009 The Author(s)
Journal compilation r 2009 by The Association for Tropical Biology and Conservation
Rapid Forest Recovery in Costa Rica
forest structure (Purata 1986) and aboveground biomass (Hughes
et al. 1999). In Guatemala, Ferguson et al. (2003) found lower species diversity, basal area, and density of woody stems in recently
abandoned fields that were used for intensive agriculture or pasture,
compared with agroforestry and swidden sites. In Puerto Rico,
abandoned coffee plantations, pastures, and improved pastures
show divergent tree communities, even after 50 or more years of
regeneration (Aide et al. 1995, 1996; Pascarella et al. 2000; Lugo
2002; Chinea & Helmer 2003). Land-use history explained
observed differences in forest composition in 20-yr-old patches of
secondary forest near Manaus, Brazil. Sites that had been active
pasture for 4 4 yr had Vismia-dominated forests, while less intensively used sites were dominated by Cecropia spp. (Lucas et al.
2002). These early differences in tree species composition may
affect the community structure of a secondary forest for many years.
Cecropia spp. tend to die off after 20 yr and permit other species to
regenerate, but Vismia spp. are much longer-lived and may slow the
establishment of other species in the understory (Lucas et al. 2002).
Thus, land-use history can drive different successional trajectories.
The spatial configuration of the landscape, especially the extent
and condition of surrounding forests, can also strongly impact the
recovery of biomass, species richness, and species composition
(reviewed in Guariguata & Ostertag 2001; Chazdon 2003, 2008;
Holl 2007).
Explaining patterns of succession along a chronosequence
requires an adequate level of replication at each point in the time
series. In the tropics, a relatively large plot size is essential in order
to capture variation in the context of such broad floristic diversity.
To capture diversity in secondary forests, it is essential to measure
small stems: much of the species richness in young forests is contributed by small-diameter stems (Guariguata et al. 1997). Yet most
chronosequence studies of secondary succession in the tropics have
used extremely small plot sizes, few replicates, and/or a large diameter threshold (Table S1). The few studies with large plot sizes have
relatively little replication, and the studies with good replication
generally have very small plots. The largest data set currently available (Aide et al. 2000) used a large diameter threshold, and includes
no old-growth sites for comparison. In addition, the flora of many
sites is poorly characterized, resulting in a high percentage of morphospecies (e.g., Saldarriaga et al. 1988; with 25 percent morphospecies at sites in the Amazon). No other study on forest succession
in the wet tropics combines our level of replication (Table S2), relatively large plot size (Table S1), small diameter thresholds, representation of both secondary and old-growth forest, and taxonomic
accuracy. We use these data to examine the structural and floristic
components of forest regeneration. We investigate how land-use
history impacts the biomass and species richness of secondary forests, and whether the biomass, species richness, and species composition of secondary forests approaches that of old-growth forests
along a chronosequence.
609
area centered around La Selva Biological Station (10126 0 N, 83159 0 W;
described in McDade et al. 1994). The area has an annual average temperature of 26.51C and annual precipitation of ca 3900 mm (Sanford
et al. 1994), placing it in the tropical lowland wet forest life zone
(Holdridge 1967). The landscape of the Sarapiquı́ region consists of
old-growth forest fragments surrounded by cattle pastures, extensive
banana and pineapple plantations, and patches of secondary forest
(Butterfield 1994, Guariguata et al. 1997).
We conducted vegetation inventories in 30 sites, seven in
old-growth forest and 23 in secondary forests of 10–44 yr postabandonment (Table S2). All the secondary forest sites were in
abandoned pastures, with the exception of two sites that were formerly in rice cultivation (Sites 6 and 26), and three sites that were
cut, burned, and then immediately left fallow (Sites 27, 29, and
30). Forest ages and land-use history were ascertained by a combination of aerial photographs and satellite images (where available),
and interviews with landowners and neighbors. We also used aerial
photos and satellite images to estimate the percent forest cover in a
1-km radius around each site at the approximate time of forest establishment (Table S2). The 30 sites occupied a fairly small geographic area, with o 25 km between the most widely separated
sites, with elevations of 40–200 m asl (Table S2; Fig. 1).
We used a modified Gentry transect (Phillips & Miller 2002)
to survey vegetation in 0.1 ha at each site. The transect consisted of
a series of five parallel strips of 2 100 m, each separated by 10 m
(this design maintains the sampling effort in a fairly limited local
area, yet avoids oversampling clusters of clonally reproducing
plants; Phillips & Miller 2002). Within the transect, we recorded
diameter at 1.3 m height (dbh) and species identification for all
woody stems Z 2.5 cm dbh for trees/shrubs and Z 0.5 cm dbh for
lianas. We chose a smaller diameter size threshold for lianas because
they produce far greater biomass for an equivalent stem diameter
(Gehring et al. 2004), and their low diameter growth rate leads to
an absence of large-diameter liana stems in young secondary forest
(DeWalt et al. 2000). Following the methods of Gentry (Phillips &
Miller 2002), we also measured and recorded giant herbs (e.g., Heliconia spp.) if their stem diameter exceeded 2.5 cm. Where a plant
had multiple stems, we recorded it as one individual, but took separate diameter readings for each stem. The data for all stems
were used to calculate biomass and relative life form abundance,
but species richness and species composition were calculated based
on individuals.
We took a voucher specimen for each species at each site,
where possible, and we verified species identifications using the collection of the Instituto Nacional de la Biodiversidad (INB) in Santo
Domingo de Heredia, Costa Rica. All specimens are filed at INB,
with duplicates of fertile specimens at the Museo Nacional de Costa
Rica. For soil analysis, at each transect site we took three evenly
spaced 2 30 cm soil cores, one at the base of the first 2 100 m
strip, one at the center of the third strip, and one at the extreme of
the fifth strip. The three cores from each site were combined.
METHODS
METHODS.—We estimated aboveground biomass using
allometric regression equations based on diameter (in this analysis,
non-woody stems were omitted, because they generally contribute only
ANALYTICAL
STUDY SITE
AND DATA COLLECTION.—We
studied secondary and oldgrowth forests in the Sarapiquı́ region of northeastern Costa Rica, in an
610
Letcher and Chazdon
Legend
24
transect site
protected areas
12
25
14
forest cover (2000)
other cover (2000)
22
16
road
river
3
2
11
6
15
5
18
1
20 17
9
28
30
19
29
27
23
4
7
8
10
26
21
0
1
2
3
km
13
FIGURE 1. A map of the study area, showing the locations of the 30 transect sites in relation to roads, rivers, and forest cover in the year 2000. All other land uses
(pasture, plantations, and settlements) are shown in white for clarity. The protected areas are La Selva Biological Station (upper right) and Braulio Carillo National
Park. GIS coverages are from the public data base of La Selva Biological Station, available online at http://www.ots.duke.edu/en/laselva/gis.shtml.
a small amount of biomass, and accurate regression equations are not
readily available; Saldarriaga et al. 1988, Uhl et al. 1988). To select appropriate models, we used equations that were developed in similar
forest types and/or with diameter ranges overlapping the range in our
data set. For lianas, we used the equations in Gehring et al. (2004),
based on the largest available liana biomass dataset. For trees, we used
two sets of equations: Brown’s (1997) wet forest equation, calibrated
near La Selva, was used for trees Z 5 cm dbh, while Nelson et al.’s
(1999) equation, calibrated with smaller stems (1.2–28.6 cm dbh) in
secondary forest in the Amazon, was used for stems o 5 cm dbh.
To incorporate wood density variation into the estimates of
biomass accumulation, we used the equation from Chave et al.
(2004) with wood density estimates taken from Chave et al. (2006)
and Brown (1997). Of the 180 tree species with individuals
Z10 cm dbh, species-level wood density estimates were available
for 98. For 69 species, we used genus-level estimates, and for the 13
species with no reported wood density values we used the regional
average of 0.645 g/cm3 (Chave et al. 2006). Because Chave’s (2004)
equation is only valid for stems Z10 cm dbh, in this case we used
the equations from Nelson et al. (1999) to estimate biomass of trees
2.5–9.9 cm dbh. We also report basal area measurements (Table
S2), calculated from diameter of all stems, to facilitate comparison
with data from sites where no appropriate allometric regression
equations are available.
Species richness was estimated by rarefaction in order to control for differences in stem density among sites (Colwell & Coddington 1994), using the program EstimateS (Colwell 2007).
Unidentified species were excluded from species richness estimation, but we did include eight consistent morphospecies corresponding to undescribed species (N. Zamora, pers. comm.). For the
rarefaction process, we divided the data from each transect into 50
samples of 10 m each, and randomized the order of sampling 100
times. We also calculated the Abundance-Based Coverage estimator
(ACE; Chao et al. 2005), a non-parametric estimator of species
richness.
To examine chronosequence trends in biomass accumulation
and species richness, sites were grouped by age: 10–15 yr (N = 6),
16–20 yr (N = 6), 21–30 yr (N = 6), 31–44 yr (N = 5), and old
growth (N = 7). Biomass and species richness data were compared
using GLM procedures with Bonferroni post-hoc tests, using Minitab Version 14 (Minitab Inc. 2003).
We investigated the relative abundance of different life forms
in different successional stages by assigning each species to one of
the following life form groups: giant herbs, shrubs, lianas, small
trees (usually o 15 m, not reaching the canopy in old growth),
canopy trees, understory palms, and canopy palms. The group designation is mainly taken from Chazdon et al. (2003). Species not
included in Chazdon et al.’s (2003) data set were evaluated based
on field observations and herbarium labels at INB and in the
W3TROPICOS database of the Missouri Botanical Garden (available online at http://mobot.mobot.org/W3T/Search/vast.html).
To examine species composition, we calculated pairwise
similarities between each pair of sites using EstimateS (Colwell
2007). We chose the Chao–Jaccard abundance-based similarity estimator, a probabilistic estimator that is demonstrably more
robust to variations in sample size than traditional similarity metrics (Chao et al. 2005). We used NMDS to visualize the relationships among the plots in ordination space, and the permutation
test ANOSIM (Clarke & Warwick 1994) to compare the strength
of within-group vs. between-group relationships for all the plots,
Rapid Forest Recovery in Costa Rica
using age category as the grouping variable. NMDS and ANOSIM
were implemented in Primer-E Version 6 (Clarke & Warwick
1994), with 50,000 starts for the NMDS and a maximum of 999
permutations in ANOSIM.
We used the bulked soil samples from each transect site to examine the effects of soil characteristics on species composition. The
soil samples were frozen after collection for a period of up to 2 yr,
and then air-dried for 3–4 d, sieved to remove fine roots, and
ground. Analysis was conducted at the soil lab of the University of
Massachusetts, Amherst. We measured pH, carbon, and total nitrogen by catalytic combustion, and the concentrations of the following elements from a Mehlich III extraction (Mehlich 1984) and
flame spectroscopy: K, Ca, Na, Mg, Zn, Mn, Cu, Fe, Pb, Al, Ni, B,
S, and P. Because the soils were frozen before analysis, it was not
possible to measure biologically available N and P. We performed
a canonical correspondence analysis (CCA) in PC-ORD 4 (McCune
& Mefford 1999) with log-transformed soil variables to investigate
the relationship between soil characteristics and species abundances
along the chronosequence.
To investigate the effects of landscape context, land-use history
and forest age on secondary forest formation, we compared all 23
secondary forest sites. In this analysis, it was necessary to lump sites
into rather broad categories to ensure sufficient replication and representation in each category. We divided sites into older (4 20 yr)
vs. younger ( 20 yr) and light use (0–10 yr in pasture before abandonment) vs. heavy use (4 10 yr pasture). We performed ANCOVAs, using forest cover in the 1-km buffer around each site as the
covariate, to investigate the relative effects of forest age and land-use
history on biomass accumulation and species richness. The ANCOVAs were conducted in Minitab Version 14 (Minitab Inc. 2003).
RESULTS
In the 30 transects combined, we found a total of 8898 individuals
(10,920 stems). In a few cases we were unable to collect a voucher
specimen, or unable to fully determine a species from a sterile
voucher. Nine individuals were completely unidentified, and five
were only identified to genus level. The flora of northeastern Costa
Rica is very well-characterized (Holdridge & Poveda 1975; Zamora
et al. 2000, 2004; Proyecto Flora Digital 2007), permitting high
taxonomic accuracy. Nonetheless, we found eight morphospecies
that were internally consistent among the specimens we collected,
yet could not be matched to any currently described species,
suggesting that they are undescribed species (N. Zamora, pers.
comm.). One morphospecies was found in each of the following
genera: Coccoloba, Cupania, Dussia, Licania, Odontocarya, Paullinia, Swartzia, and Unonopsis. Including these consistent morphospecies, we found a total of 477 species in 93 families (according to
the APG classification; Stevens 2006). Overall, 8791 individuals
(98.8%) were positively identified and matched to described species. When we include the eight morphospecies, this figure rises to
8889 individuals (99.9%).
Nearly all the species we collected were angiosperms. The only
exceptions were two tree ferns, Cyathea microdonta (Desv.) Domin.
and C. multiflora Sw., and the gnetophyte liana Gnetum leyboldii
611
FIGURE 2. Aboveground biomass accumulated rapidly along the chronosequence, peaking in old secondary forest sites. Bars show mean SE. Biomass
was calculated with a general allometric equation from Brown (1997), and with
an equation incorporating species-specific wood density values from Chave et al.
(2006). Although estimates were substantially higher using Chave et al.’s (2006)
equations, the pattern of rapid accumulation and overshoot did not differ. Letters show significant differences between groups; Bonferroni post-hoc comparisons and one-way ANOVA, F4, 25 = 9.30, P o 0.001 for Brown; F4, 25 = 6.26,
P o 0.01 for Chave.
Tul. The vast majority were species native to the region; only seven
exotic species (1.5%) were found, and they contributed only 15
individuals (0.15%).
Aboveground biomass recovered rapidly along the chronosequence, such that sites 21–30 yr of age already showed values not
significantly different from the biomass of old-growth forests (Fig.
2). The value for old-growth forests obtained in this study using
Brown’s (1997) equations (mean SE of 163 12 Mg/ha) compares favorably to the estimate of Clark and Clark (2000), of
161–186 Mg/ha for old-growth forests in the same region. Biomass
in older secondary forests, 30–42 yr, was significantly higher than
the value for old-growth forests (Fig. 2). Chave et al.’s (2006) equations incorporating wood density calculated substantially higher
values overall (Fig. 2), but the pattern of rapid accumulation and
overshoot did not differ.
Species richness also recovered rapidly along the chronosequence, although not as rapidly as biomass: it did not reach oldgrowth levels until 30–44 yr postabandonment (Fig. 3). Estimated
species richness was higher than observed for all age categories (Fig.
3), indicating that species accumulation curves did not level off at
0.1 ha in these sites. However, the behavior of the estimator was
identical to the behavior of the rarefied species richness: ACE values
increased in each successive age category for secondary forests,
reaching a level indistinguishable from old-growth values in the
30–44 yr age category.
The relative abundance of different life forms changed along
the chronosequence (Fig. 4). Giant herbs were most prevalent in
the youngest sites, and their abundance rapidly declined with forest
612
Letcher and Chazdon
FIGURE 5. Non-metric multidimensional scaling plot of Chao–Jaccard-estiFIGURE 3. Species richness increased along the chronosequence, whether mea-
mated similarity (Chao et al. 2005) among the 30 transect sites. In general, forests within an age category group together, and the youngest sites are least similar
sured by rarefaction (gray bars, number of species per 206 stems) or using the
to the oldest sites, but there is considerable overlap between groups in adjacent
Abundance-based Coverage Estimator (black bars; Chao et al. 2005). Bars show
age categories. See Table 1 for significance of between-group comparisons.
mean SE. (Letters show significant differences between groups; Bonferroni
post-hoc comparisons and one-way ANOVA, F4, 25 = 21.5, P o 0.001 for rarefaction data; F4, 25 = 14.1, P o 0.001 for ACE data.) Estimated species richness
was significantly higher than observed species richness for every age category
(sign test, P o 0.0001).
age, reaching zero in forests 4 30 yr old. Shrubs and lianas also declined with forest age, although less dramatically, and they were still
present even in old-growth forests. Canopy palms were almost
absent from young sites; the few stems found in sites o 20 yr old
probably represent remnant vegetation, because canopy palms in
this region have an extended establishment phase (DeMason 1983,
Schatz et al. 1985), during which they have no aboveground stem
extension, and thus would not have been measured in this census.
Likewise, understory palms were very rare except in old-growth
forest, where they formed approximately 6 percent of stems. Tree
ferns formed a negligible amount of the stems in any age class, and
are not shown here.
Species composition varied consistently along the chronosequence, with older sites grouping at one extreme and younger sites
at the other (Fig. 5). The NMDS plot had a 2-D stress of 0.17,
indicating a meaningful level of structure in the data set (Clarke &
Warwick 1994). The global P value from ANOSIM was o 0.001.
Pairwise comparisons (Table 1) showed few significant differences
between adjacent age groups; most significant differences occurred
between groups separated by at least 10 yr in age. This analysis indicated no significant difference between the species composition of
older secondary forests (30–42 yr) and old-growth forest.
Soils had little apparent effect on the species composition of
regenerating forests. Soil characteristics explained a cumulative total
of only 23.5 percent of the variance in species composition in the
first three canonical axes. Soils were generally nutrient-poor oxisols
with low pH and high aluminum. Site 6 was an apparent outlier,
with the highest pH (6.5), the highest P concentration (6.5 mg/kg
soil), and cation concentrations an order of magnitude higher than
in other sites (pH at other sites was 4.0–5.3, and P concentrations
1.2–4.2 mg/kg). Site 6 was on a river floodplain, and it was in rice
TABLE 1. Significance (determined by ANOSIM) for differences in species composition among sites from the five age categories. The table shows P values
for pairwise comparisons between age categories, with values o 0.05
in bold.
o 15 yr
16–20 yr
FIGURE 4. Relative abundance of life forms by age category, expressed as per-
16–20 yr
0.143
cent of individuals. Abundance of giant herbs and lianas declines significantly
21–30 yr
0.045
0.16
from the youngest to oldest forests, while abundance of understory and canopy
palms increases significantly (G test on raw abundances, P o 0.01).
4 30 yr
Old growth
0.004
0.001
0.006
0.003
21–30 yr
4 30 yr
0.004
0.002
0.077
Rapid Forest Recovery in Costa Rica
cultivation before abandonment, which may account for the unique
soil properties. Nonetheless, when Site 6 was removed, the CCA
showed even less relationship between environmental variables and
species composition: the first three canonical axes explained only
21.3 percent of the variance in species composition in the remaining 29 sites.
In the subset of just secondary forest sites, we examined the
effects of forest age vs. land-use history (time in pasture) on biomass
and species richness, using forest cover in the 1-km buffer around
each site at time of forest establishment as a covariate. For biomass
accumulation, forest age (but not land use) had a significant effect,
explaining 49.6 percent of the variance, and the covariate was not
significant (F1, 18 = 16.2, P o 0.01 for age; F1, 18 = 0.11, P = 0.75 for
use; F1, 18 = 2.10, P = 0.17 for interaction; F1, 18 = 0.85, P = 0.37 for
forest cover). Young forests (o 20 yr) had significantly lower biomass than their older counterparts. For species richness, both age
and land-use history had significant impacts. A combined model
with age and land use explained 61.7 percent of the variance in
species richness; the interaction term and the covariate were not
significant. (F1, 18 = 17.6, P o 0.01 for age; F1, 18 = 12.9, P o 0.01
for use; F1, 18 = 0.13, P = 0.73 for interaction; F1, 18 = 1.52, P = 0.23
for forest cover). Older forests and those with lighter use (o 10 yr
pasture) had higher species richness.
DISCUSSION
Recently, much debate has centered on the conservation value of
tropical secondary forests and their potential as reservoirs of biodiversity (Wright & Muller-Landau 2006a, b; Brook et al. 2006; Barlow et al. 2007). Rates of recovery for biomass and species richness
vary widely across the Neotropics, and species composition of secondary forests often fails to converge with that of old-growth forests
nearby (Chazdon 2008; Table S1). Our work indicates an encouraging prognosis for forest regeneration in northeastern Costa Rica.
For woody vegetation, biomass and species richness recover rapidly,
and even the species composition returns to pre-disturbance levels
in a relatively short period of time.
Recent research has questioned the validity of the chronosequence approach for studying tropical forest succession (Chazdon
et al. 2007, Feldpausch et al. 2007, Johnson & Miyanishi 2008).
Chronosequences provide a cost-effective and rapid method of
investigating forest changes over time, but the critical, and often
untested, assumption is that sites of different ages represent points
along a predictable continuum. In comparing chronosequence predictions to the results of long-term dynamics studies, Chazdon et al.
(2007) found that certain stand properties are predictable from
chronosequence trends, while others fail to conform. In particular,
basal area accumulation (a conservative proxy for biomass accumulation where no locally calibrated allometric biomass equation is
available) is a highly predictable emergent property of forest stands
during succession. Species composition at a site was found to
be much less dynamic than would be predicted from a chronosequence, and hence species richness and species composition during
succession are much less predictable. Feldpausch et al. (2007) monitored secondary forests in the Amazon for 4 yr, and they found that
613
biomass accumulation was not predictable from chronosequence
extrapolations. In their study site, however, forest age was confounded with land-use intensity: the oldest forests established after
short-term pasture use, and the youngest forests established on
lands that had been in pasture for many years. In this study, we
attempted to control for the pitfalls of the chronosequence approach by rigorously verifying site ages, and by selecting multiple
sites (N Z 5) in each age category. We also ensured that, as much as
possible, forest age was not confounded with land-use history, and
we addressed the confounding of age and land-use history in our
analysis.
The rapid early accumulation of aboveground biomass
observed in these data compares favorably to the results of prior
studies (Saldarriaga et al. 1988, Guariguata et al. 1997, Pascarella et al.
2000, Silver et al. 2000, Guariguata & Ostertag 2001, Peña-Claros
2003, Feldpausch et al. 2005). According to many studies, biomass
accumulation is a saturating curve, rapid at first and then leveling
off, with the highest standing biomass in old-growth sites (Saldarriaga et al. 1988, Peña-Claros 2003, Gehring et al. 2005, Howorth
& Pendry 2006). This study, Denslow and Guzman (2000), and
Marı́n-Spiotta et al. (2007) found higher biomass in intermediateaged forests than in old growth. One might suspect that this trend
was driven by an overabundance of light-wooded pioneer species in
the canopy of intermediate-aged successional forests, but an analysis
incorporating species-specific wood density values (Fig. 2) showed
precisely the same pattern. An alternate explanation for the overshoot in biomass is that young to intermediate secondary forests
have very few large-scale gap disturbances (Montgomery & Chazdon 2001). Many species recruit from beneath the canopy rather
than exploiting gaps. Late in the process of forest maturation,
stand-level thinning may regulate aboveground biomass levels
(Roberts & Gilliam 1995, Niklas et al. 2003, Chazdon 2008). In
young forests, before density-dependent forces become strong
enough to regulate tree distributions, a high density of stems may
recruit and establish (Guariguata & Ostertag 2001, Chazdon
2008).
The biomass of secondary forests was not significantly impacted by the amount of time that the land was in pasture before
regeneration. This contradicts the results of numerous other studies
(e.g., Aide et al. 1995, Hughes et al. 1999, Steininger 2000,
Kammesheidt 2002), in which biomass accumulation was impacted
by prior land use, although Zarin et al. (2001) found no significant
difference in biomass accumulation between former pastures and
former slash-and-burn fallows. Biomass accumulation in the Sarapiquı́ region may be more resilient due to the higher soil fertility
in Costa Rica (Guariguata et al. 1997) than in other regions where
similar work has been conducted (Pascarella et al. 2000, Feldpausch
et al. 2005, Toledo & Salick 2006). Alternately, the division of
land-use categories may have been too crude to capture true differences in the effects of land-use history on biomass accumulation.
Steininger (2000) detected a significant difference in the biomass
accumulation after 1 yr vs. 4 yr fallows. There may be a threshold
level above which further use no longer affects biomass accumulation, and having too few sites in the light-use category, we may have
failed to capture that effect. However, it would be difficult to make
614
Letcher and Chazdon
a finer-scale test of the effects of land-use history on biomass accumulation in this region of Costa Rica, because use intensity is confounded with forest age here (Guariguata et al. 1997). Due to the
economic history of the region, very few recently abandoned forest
sites had light use: most of the clearing took place in the
1960s–1980s, and regeneration has begun sporadically since then
(Butterfield 1994, Guariguata et al. 1997, Read 1999).
Similarly, we found that biomass accumulation was not
affected by the amount of forest cover in the 1-km buffer around
each site at the time of forest establishment. This result again contradicts many studies showing that forest regeneration is slower
in landscapes with less existing forest cover (e.g., Aide et al. 1995,
Hughes et al. 1999, Steininger 2000, Kammesheidt 2002, Holl
2007, Martı́nez-Ramos & Garcı́a-Orth 2007). Compared with
other tropical regions, though, deforestation in the Sarapiquı́ area
has been relatively modest (Read 1999). Forest clearing was mainly
conducted by smallholders (Butterfield 1994). Deforestation spread
out from the road network, but remote areas remained under forest
cover, leaving large forest remnants in the landscape (Butterfield
1994, Read 1999; Fig. 1). In the San Juan Biological Corridor, a
roughly 30 60 km strip of land overlapping most of the study region, an estimated 26 percent of the area was forested in 2001 (this
figure includes old-growth and secondary forest; Wang 2008).
None of our study sites were established in completely denuded areas; the lowest forest cover in the 1-km buffer around a site at the
time of establishment was 20 percent (Sites 17 and 18; Table S2).
Landscape context also had no apparent effect on the aboveground
biomass or species richness of old-growth forests. Sites 22, 28, and
25 were located in forest fragments, with site 25 being closest to a
forest edge (Fig. 1). Sites 8, 9, 10, and 11 are located in a large
contiguous area of protected old-growth forest. Yet the distribution
of species richness (site 25 4 8 4 28 4 11 4 9 4 22 4 10) and
biomass (site 8 4 25 4 28 4 9 4 11 4 22 4 10) does not reflect
any negative effects of the landscape context on these parameters in
old-growth forest. Schedlbauer et al. (2007) also failed to detect any
edge effects on biomass in 20–30 yr old edges between old-growth
forest and pasture in the Sarapiquı́ region. Perhaps in a more fragmented landscape the effects of fragmentation would be easier to
detect.
Guariguata et al. (1997) estimated that up to 15 percent of the
secondary forest biomass in this region of Costa Rica may be contributed by remnant trees. This may have contributed to the rapid
biomass accumulation we observed, and our failure to detect any
effect of surrounding forest cover on forest recovery. Lacking highly
detailed records of the location of remnant trees before regeneration, however, it is difficult to develop objective criteria for separating remnant trees from true secondary forest. Growth rates are
extremely rapid in the humid tropics—Piotto et al. (2003) report
annual diameter increments of 1.5 to almost 3 cm/yr for plantation
trees in this region of Costa Rica, and growth rates may be even
higher in isolated trees during early regeneration. It is possible for
trees to reach diameters 4 60 cm in the first 20 yr of growth. In
some cases, remnant trees can be identified based on their species
identity: large individuals of slow-growing, non-pioneer species can
be safely considered remnant trees. However, in our data set, the
large-diameter trees (4 60 cm) in secondary forests were all species
that are commonly found in secondary forests in the region: Pentaclethra macroloba (Willd.) Kuntze, Stryphnodendron microstachyum Poepp. & Endl., Tapirira guianensis Aubl., Vochysia
ferruginea Mart., and V. guatemalensis Donn. Sm. Omitting the
seven individuals 4 60 cm dbh in secondary forests from the analysis (two in forests 16–20 yr, one in forests 21–30 yr, and four in
forests 31–44 yr) reduced the estimates of biomass accumulation,
but did not change the pattern of rapid increase and overshoot (data
not shown). Remnant trees in some sites may have facilitated the
rapid successional process documented in this study: Schlawin and
Zahawi (2008) found higher species richness and stem density in
secondary forests in the vicinity of remnant trees in northeastern
Costa Rica.
Woody species richness recovers rapidly, reaching the level of
old-growth forest after as little as 30 yr, although the recovery is less
rapid in sites with more intense land use. These results corroborate
many published studies (e.g., Purata 1986, Aide et al. 2000, Pascarella et al. 2000, Guariguata & Ostertag 2001, Peña-Claros 2003,
Feldpausch et al. 2005, Toledo & Salick 2006, Marı́n-Spiotta et al.
2007). However, it is important to note that the analysis of species
richness presented here made no consideration of stem size. Much
of the diversity in older secondary forests comes from stems in small
size classes (Guariguata et al. 1997, Peña-Claros 2003; this study),
and it may take hundreds of years for the size class distributions of
individual species to match those displayed in old-growth forests. In
addition, secondary forests lack some of the structural characteristics of old-growth forests—standing dead trees, large woody debris,
etc.—that form important wildlife habitat (Saldarriaga et al. 1988,
Dewalt et al. 2003, Dunn 2004). Faunal succession may be more
delayed than vegetational succession, due in part to the structural
differences between old-growth and secondary forests (DeWalt
et al. 2003, Dunn 2004, Barlow et al. 2007).
Species composition in secondary forests of northeastern Costa
Rica converges with the composition of old-growth forests, rather
than taking divergent successional pathways (Fig. 5). This is an encouraging indication of forest recovery. In Puerto Rico, numerous
studies have documented the incursion of exotic invasive species
into secondary forests (e.g., Aide et al. 2000, Pascarella et al. 2000,
Marı́n-Spiotta et al. 2007). The species richness of the forest may
recover, but the constituent species are different. In this study, we
documented a very small number of non-native species, which contributed only a vanishing percentage of the species richness in secondary forests. One of the most pernicious invasives in Puerto Rico,
Spathodea campanulata P. Beauv. (Aide et al. 2000, Pascarella et al.
2000), is widely planted as an ornamental tree near some of the sites
included in this study (S. Letcher, pers. obs.), but it was not present
in any of the transects and not observed in the forest. The absence
of invasives in these sites does not guarantee that the forest will remain free of them: elsewhere in the Sarapiquı́ region, invasions of
numerous exotic species have been observed: Euterpe oleracea Mart.,
Hevea brasiliensis (Willd. ex A. Juss.) Müll. Arg., Coffea canephora
Pierre ex Froehner, and Musa velutina H. Wendl. & Drude (Chazdon et al., in press). Also, the small diameter threshold used in this
study may have contributed to the high similarity between late
Rapid Forest Recovery in Costa Rica
secondary and old-growth sites. In secondary forests in our study
area, Guariguata et al. (1997) found stronger similarity to oldgrowth species composition in the sapling layer (stems Z1 m tall
and 5 cm dbh) than in the canopy (stemsZ10 cm dbh), suggesting
that the inclusion of small stems makes it easier to detect convergence between the species composition of secondary and oldgrowth forest.
This study underscores the importance of secondary forests as
reservoirs of biodiversity in tropical landscapes. At least in northeastern Costa Rica, tropical forests are highly resilient systems (sensu
Holling 1973): after anthropogenic disturbance, they are capable of
rapid recovery. After as little as 30 yr, secondary forests harbor as
many woody species as old-growth forests, and in this region, the
species composition converges with that of old-growth forests as
well. Secondary forests contain large numbers of useful timber species (Redondo et al. 2001, Chazdon 2003) and non-timber forest
products (Chazdon & Coe 1999), and the use of secondary forests
as extractive reserves could take some pressure off old-growth forests (Kammesheidt 2002). Although many conservation plans still
focus almost exclusively on old-growth forests, it is imperative to
take a more holistic view of tropical landscapes (Chazdon 2003,
Bawa et al. 2004, Chazdon et al., 2009). The rapid recovery of biodiversity and forest structure in secondary forests provides hope that
they may, after all, help to stem the tide of extinctions in the tropics
(Wright & Muller-Landau 2006a, b).
ACKNOWLEDGMENTS
D. Perez-Salicrup and two anonymous reviewers provided useful
suggestions on earlier versions of this manuscript. We gratefully acknowledge the field assistance of M. Luna, A. Thrall, B. Lewis, and
J. Foley, and the logistical support of the Organization for Tropical
Studies, CATIE, and the Instituto Nacional de Biodiversidad. In
addition, we thank the following landowners and organizations for
granting access: C. Arce, M. Lopez, R. Murillo, J. Garmin and M.
Mora, T. Ray, Selva Verde Lodge, Reserva Forestal Tirimbina, and
Pozo Azul Resort. Financial support came from the University of
Connecticut, the Ronald Bamford Endowment to the UCONN
EEB Department, the UCONN Center for Conservation and Biodiversity, the Organization for Tropical Studies, a National Science
Foundation Graduate Fellowship to SGL, and NSF DEB 0424767
and NSF DEB-0639393 to RLC.
SUPPORTING INFORMATION
Additional Supporting Information may be found in the online
version of this article:
TABLE S1. Published chronosequence data sets for neotropical rain
forests.
TABLE S2. Description of sites.
Please note: Wiley-Blackwell are not responsible for the content or
functionality of any supporting materials supplied by the authors.
615
Any queries (other than missing material) should be directed to the
corresponding author for the article.
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