Altered resource availability and the population dynamics of tree species in Amazonian secondary forests

Article · December 2009with26 Reads
DOI: 10.1007/s00442-009-1524-5 · Source: PubMed
Abstract
Despite research demonstrating that water and nutrient availability exert strong effects on multiple ecosystem processes in tropical forests, little is known about the effect of these factors on the demography and population dynamics of tropical trees. Over the course of 5 years, we monitored two common Amazonian secondary forest species-Lacistema pubescens and Myrcia sylvatica-in dry-season irrigation, litter-removal and control plots. We then evaluated the effects of altered water and nutrient availability on population demography and dynamics using matrix models and life table response experiments. Our results show that despite prolonged experimental manipulation of water and nutrient availability, there were nearly no consistent and unidirectional treatment effects on the demography of either species. The patterns and significance of observed treatment effects were largely dependent on cross-year variability not related to rainfall patterns, and disappeared once we pooled data across years. Furthermore, most of these transient treatment effects had little effect on population growth rates. Our results suggest that despite major experimental manipulations of water and nutrient availability-factors considered critical to the ecology of tropical pioneer tree species-autogenic light limitation appears to be the primary regulator of tree demography at early/mid successional stages. Indeed, the effects of light availability may completely override those of other factors thought to influence the successional development of Amazonian secondary forests.
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POPULATION ECOLOGY - ORIGINAL PAPER
Altered resource availability and the population dynamics
of tree species in Amazonian secondary forests
Lucas Berio Fortini Emilio M. Bruna
Daniel J. Zarin Steel S. Vasconcelos
Izildinha S. Miranda
Received: 19 March 2009 / Accepted: 18 November 2009 / Published online: 9 December 2009
ÓSpringer-Verlag 2009
Abstract Despite research demonstrating that water and
nutrient availability exert strong effects on multiple eco-
system processes in tropical forests, little is known about
the effect of these factors on the demography and popu-
lation dynamics of tropical trees. Over the course of
5 years, we monitored two common Amazonian secondary
forest species—Lacistema pubescens and Myrcia sylvati-
ca—in dry-season irrigation, litter-removal and control
plots. We then evaluated the effects of altered water and
nutrient availability on population demography and
dynamics using matrix models and life table response
experiments. Our results show that despite prolonged
experimental manipulation of water and nutrient avail-
ability, there were nearly no consistent and unidirectional
treatment effects on the demography of either species. The
patterns and significance of observed treatment effects
were largely dependent on cross-year variability not related
to rainfall patterns, and disappeared once we pooled data
across years. Furthermore, most of these transient treat-
ment effects had little effect on population growth rates.
Our results suggest that despite major experimental
manipulations of water and nutrient availability—factors
considered critical to the ecology of tropical pioneer tree
species—autogenic light limitation appears to be the pri-
mary regulator of tree demography at early/mid succes-
sional stages. Indeed, the effects of light availability may
completely override those of other factors thought to
influence the successional development of Amazonian
secondary forests.
Keywords Amazonia Regrowth forests Succession
Water stress Nutrient limitation
Introduction
Water and nutrient availability influence multiple ecosys-
tem processes in tropical forests. For instance, limited
water availability can increase rates of tree mortality
(Condit 1998; Chazdon et al. 2005; Nepstad et al. 2007),
reduce photosynthesis (Nepstad et al. 2002; Fortini et al.
2003; Araga
˜o et al. 2005), change leaf and reproductive
phenology (Kitajima et al. 1997; Malhi et al. 1998), and
increase the susceptibility of forests to fire (Nepstad et al.
2004). Similarly, observational and manipulative studies
have shown that nutrient availability alters patterns of tree
growth (Davidson et al. 2004), fine litterfall production
(Mirmanto et al. 1999), above-ground biomass (Laurance
et al. 1999), and resource allocation to below-ground
structures (Gower 1987; Giardina et al. 2004). Despite
considerable work investigating the individual- or ecosys-
tem-level consequences of nutrient and water availability
for tropical forests, however, little has been done to explore
Communicated by Peter Clarke.
L. B. Fortini (&)D. J. Zarin
School of Forest Resources and Conservation, University
of Florida, P.O. Box 110760, Gainesville, FL 32611-0760, USA
e-mail: lfortini@ufl.edu
E. M. Bruna
Department of Wildlife Ecology and Conservation and Center
for Latin American Studies, University of Florida, PO Box
110430, Gainesville, FL 32611-0430, USA
S. S. Vasconcelos
Laborato
´rio de Ecofisiologia e Propagac¸a
˜o de Plantas, Embrapa
Amazo
ˆnia Oriental, Bele
´m, PA 66095-100, Brazil
I. S. Miranda
Universidade Federal Rural da Amazo
ˆnia, CP 917,
Bele
´m, PA 66077-530, Brazil
123
Oecologia (2010) 162:923–934
DOI 10.1007/s00442-009-1524-5
how these factors influence the population dynamics of
tropical trees. Elucidating these relationships is critical,
since population dynamics link individual responses to
abiotic constraints with patterns of community composition
and ecosystem processes.
‘Secondary’’ or ‘‘regenerating’’ forests account for more
than 40% of tropical forest worldwide (Brown and Lugo
1990) and play a critical role in regional C dynamics, the
maintenance of biodiversity, and income generation
(Chazdon and Coe 1999; Hughes et al. 1999; Aide et al.
2000; de Jong et al. 2001; Smith et al. 2003; Gavin 2004;
Olschewski and Benitez 2005). There are many models of
succession that attempt to explain how secondary forest
composition and structure change over time (Clements
1916; Yarranton and Morrison 1974; Pickett 1976; Noble
and Slatyer 1980). A commonality of these models is that
populations of species reach peak abundances at different
stages of succession, resulting in easily recognizable spe-
cies turnover. While light availability is a key driver of
these successional dynamics (Huston and Smith 1987), tree
populations may also be particularly susceptible to changes
in water and nutrient availability. For instance, some sec-
ondary forest species may be very susceptible to drought
because they allocate more fine roots to shallower soil,
while others may face nutrient limitation due to depletion
from past anthropogenic activities (Juo and Manu 1996;
Hopkins et al. 1996; Ayuba et al. 2000; Pavlis and Jenik
2000; McGrath et al. 2001). However, it is unclear how the
rate and magnitude of changes in abundance during suc-
cession are altered by the availability of water and
nutrients.
Unfortunately, the high cost and logistical issues asso-
ciated with establishing experiments at suitable spatial
scales, along with the need to monitor permanent forest
plots for multiple years, have resulted in few studies that
rigorously test the effects of water and nutrient availability
on the population dynamics of trees in tropical secondary
forests. Descriptions and comparisons of stands, chrono-
sequences, and observational longitudinal studies provide
limited inference regarding mechanisms underlying com-
plex forest dynamics and their potential abiotic constraints.
However, when long-term data are available, life table
response experiments (LTREs) provide a powerful
approach to disentangle how experimental factors influence
the growth and demography of populations (Burns 2008).
These analyses allow for the decomposition of each
experimental treatment’s effects on the growth rates of
populations (i.e., k); specifically, they measure the contri-
butions to the differences in kbetween treatments arising
from changes in size-class specific vital rates (Caswell
2001). Because even similar population growth rates can
result from very different demographic mechanisms (e.g.,
Bruna and Oli 2005), LTREs can elucidate the responses of
populations to environmental variability in ways that sim-
ply comparing the sizes, structures, or growth rates of
populations cannot (e.g., Bruna and Oli 2005).
In this study we used LTRE to investigate how a long-
term, stand-level experimental manipulation of nutrient
availability (via litter removal) and water availability (via
irrigation) conducted in an Amazonian secondary forest
influenced the demography and population growth of two
common tree species. These experimental manipulations
have been shown at our site and elsewhere to significantly
alter ecosystem-level (Vasconcelos et al. 2004,2007,2008;
Vasconcelos 2006; Veluci-Marlow 2007) and individual-
level processes (Fortini et al. 2003; Araga
˜o et al. 2005). We
monitored the demography of two early short-lived pioneer
species past their peak abundance and under decline,
Lacistema pubescens (Lacistemataceae) and Myrcia sylv-
atica (Myrtaceae), in dry-season irrigation, litter-removal
and control plots for a 5-year period. We then used these
demographic data to estimate kusing matrix models and
applied two-way LTREs to evaluate whether changes in
nutrient and water availability alter the rate of population
decline.
Materials and methods
Site description
The experimental site is located at the research station of
the Universidade Federal Rural da Amazo
ˆnia (UFRA),
located near the city of Castanhal, Para
´, Brazil. Annual
precipitation in the region is 2,000–2,500 mm, with a rainy
season that extends from December to May. Mean daily
temperatures fluctuate between 24 and 27°C. Soils in the
site are classified as dystrophic yellow latosols, stony phase
I (concretionary, lateritic) in the Brazilian soil classifica-
tion system, which corresponds to Sombriustox in US soil
taxonomy (Teno
´rio et al. 1999). At a 0–10 cm depth, soil
pH is 5.0, total N is 0.15%, and Mehlich-1 extractable P is
1.58 mg kg
-1
(Rangel-Vasconcelos et al. 2005). The
landscape surrounding the field station is characterized by
secondary forests, annual crops, and active and degraded
pastures.
Our experiment was initiated in 2001 in a 2-ha patch of
secondary forest that had been fallow for 14 years. Prior
to being abandoned, the site had undergone multiple
cycles of shifting cultivation that began about 60 years
ago when the old-growth forest was first cleared. Each
cycle included cultivation of corn, manioc, and beans for
1–2 years, followed by a fallow stage. Interviews with
local residents and field station personnel suggest typical
shifting cultivation cycles lasted 7–10 years (G. Silva
e Souza and O. L. Oliveira, personal communication).
924 Oecologia (2010) 162:923–934
123
In 2001 stand basal area was 16.7 m
2
ha
-1
, average stand
density was 208 (±33 SE) individuals [1 cm diameter at
breast height (DBH), and average species richness was 24
(±1 SE) species 100 m
-2
(Arau
´jo et al. 2005).
Study species
Lacistema pubescens Mart. and Myrcia sylvatica (G. Mey.)
DC. are early short-lived pioneer species prevalent in
secondary forest stands across the eastern Amazon.
L. pubescens is one of the earliest tree species to establish
in fallows; it typically has a single upright stem and is
shade intolerant. M. sylvatica generally appears in fallows
after L. pubescens and other early pioneer species have
become established (Coelho et al. 2004). It is noticeably
more shade tolerant than its predecessors and typically has
a highly branched architecture. L. pubescens and M. sylv-
atica are the most abundant overstory species in our
experimental plots accounting for 36 and 22% of all stems
[1 cm DBH, respectively (Arau
´jo et al. 2005).
Experimental design
The study was conducted in twelve 20 920-m plots sep-
arated by 10-m buffer strips. We randomly selected four
plots for dry-season irrigation, litter removal, and untreated
controls (n=12 plots total). The irrigation treatment
consisted of providing the equivalent of 5 mm daily pre-
cipitation during rainless dry-season days with an irrigation
tape system, corresponding to regional estimates of daily
evapotranspiration (Shuttleworth et al. 1984; Lean et al.
1996; Jipp et al. 1998). Irrigation was initiated in July
2001, which corresponded to the start of the dry season.
Measurements of gravimetric soil moisture content indi-
cated that during the dry season the irrigated plots had
slightly more than double the moisture of control plots (22
vs. 10%). Wet-season gravimetric soil moisture content
was 27% for both treatments (Vasconcelos et al. 2002). We
established four litter-removal plots in an attempt to break
the tight nutrient cycling of our forest and thus decrease
nutrient availability experienced by plants within these
plots. While we acknowledge that litter-removal treatments
may result in several secondary effects (e.g., leaching,
changes in soil microbial biomass, soil water content, or
soil organic matter), we focused our analyses on the pri-
mary effect of reducing nutrient availability as most of the
secondary effects also exacerbate nutrient limitation (Sayer
2006). In August 2001, all leaf and branch litter was
removed from the litter-removal plots with plastic rakes;
this process was subsequently repeated every 2 weeks.
Standing litter crop was low, but not entirely absent, in the
litter-removal plots. Total new non-woody litterfall
removed from August 2001 to December 2005 was
3,568 ±136 g m
-2
, leading to changes in soil nutrient
status and reductions in litterfall N content (Veluci-Marlow
2007; Vasconcelos et al. 2008).
Nested in the center of each 20 920-m plot were
10 910-m permanent inventory plots (hereafter referred to
as ‘‘overstory plots’’). Within these plots all tree individ-
uals of the two study species with DBH [1 cm had their
height and DBH measured annually between July and
August. We randomly located four 1 91-m quadrats in
each plot to monitor individuals C10 cm high and \1cm
DBH (hereafter referred to as ‘‘understory plots’’).
Although we monitored these quadrats every 2 months
from 2001 to 2006, for our analyses we used data from the
surveys conducted in July–August of each year to best
match inventory dates for the individuals [1 cm DBH.
Here we report on results from five measurement intervals
included in the 2001–2006 yearly inventories.
Matrix model construction
We observed a strong relationship between height and
DBH for both species (r
2
=0.71 and 0.73 for L. pubescens
and M. sylvatica, respectively). However, because of the
difficulty in obtaining accurate height measurements for
some individuals and the die-off of some shoots, we used
DBH measurements as the state variable for all individuals
with DBH C1 cm. Height was the only choice for state
variable of all individuals with DBH \1.0 and height
C10 cm. Following state variable definition, we created a
four life cycle model for L. pubescens and a five life cycle
model for M. sylvatica. We defined the number of stages
and their size cut-offs based on patterns of mortality across
size, limited reproductive phenology data, height to canopy
calculations, field observations, and available number of
individuals.
Calculating vital rates
Prior to parameterizing our matrices, we calculated sep-
arate estimates of survival, growth, regression and fertility
rates for each size class in each species 9treat-
ment 9year combination. Since understory individuals
were often difficult to locate in the field, data for a small
number of them were missing in some years. Since the
exclusion of these individuals from the calculation of
mortality rates for a given transition year would artifi-
cially depress survival, we replaced all single-year gaps in
data with the average size from adjacent years. However,
we did exclude the very small number of individuals with
more than 1 year of missing data (n\10) from the cal-
culations of vital rates because of the potentially greater
errors that could result from interpolating data for longer
time periods.
Oecologia (2010) 162:923–934 925
123
We calculated survival rates for each matrix using
logistic models parameterized with all overstory and
understory data. This approach avoided the ‘‘over-parsing’
of our data (sensu Morris and Doak 2002) and perfect sur-
vival in size classes with low sample sizes and high survival
rates. A separate logistic fit was used for the understory and
overstory data, with resulting size class survival values
based on the logistic fit evaluated at median individual size
observed within each size class. To avoid poor fits to the
data, we used the standard count-based methods of survival
calculations when n\10 for either data set.
We calculated growth and regression transition proba-
bilities following standard count-based methods where the
probability of growth (regression) of any given size class is
the proportion of individuals alive at time tthat grew
(regressed) to another size class at time t?1. Growth
transition probabilities between understory and overstory
size classes were based on actual observed recruitment to
the overstory size classes at time t?1 divided by the area-
scaled number of understory size class individuals present
at time t. Seedling recruitment rates were calculated based
on the observed number of new individuals from one
measurement to the next. Lastly, we used Caswell’s (2001)
approach to calculate anonymous fertility rates with equal
reproductive weights among overstory size classes.
Analyzing differences among vital rates
To evaluate variability in estimates of vital rate, we per-
formed a bootstrapping procedure on the overstory and
understory data sets (1,000 runs). We used the resulting
bootstrapped estimates to create 95% confidence intervals
for each vital rate for each species, size class, treatment and
year.
Creating population matrices
We created a total of 30 matrix models (2 species 93
treatments 95 time intervals) based on lower level vital
rates (Morris and Doak 2002). To avoid problems associ-
ated with reducible matrices (Caswell 2001), we substi-
tuted the rare zero values for growth and survival
probabilities with the lowest bootstrapped non-zero value
of the vital rate for the respective treatment among all
measurement years. Fecundity values of zero also yield
reducible matrices. Therefore, if fecundity for any matrix
was zero we only substituted fecundity from the largest
size class with the lowest bootstrapped non-zero fecundity
value for the respective treatment among all measurement
years. Preliminary comparisons showed that while this ad
hoc reducibility fix improved the results of subsequent
analysis, it had only minor effects on estimates of popu-
lation vital rates and population growth.
Demographic analyses
Using our 30 matrices, we calculated kfor each spe-
cies 9year 9treatment combination, as well as the sen-
sitivities of population growth to all underlying vital rates.
We also bootstrapped our data sets using the reducibility
fix described above to estimate bias-corrected 95% confi-
dence intervals for ks per species, year, and treatment. We
used the 30 matrices to perform standard two-way full
factorial LTRE analyses to determine the effects of the
experimental treatments and study year on each species
(Caswell 2001, p. 263). Because our experimental design
does not consider the interaction between irrigation and
litter removal, irrigation and litter-removal effects were
evaluated independently through separate LTRE analyses
in the following comparisons: control versus irrigation and
control versus litter removal. For all tests, we computed the
‘reference matrices’’ (sensu Caswell 2001) and related
vital rates as the average from control plot data for all
measurement intervals. For each factor level for each
LTRE, the midpoint matrix used to evaluate the contribu-
tion of observed vital rate to kwas computed as the average
matrix between the reference matrix and related factor
matrix. Lastly, we examined the significance of treatment
effects statistically by bootstrap-derived confidence inter-
vals of the difference between treatment and reference vital
rate estimates.
Precipitation analysis
To determine whether precipitation patterns influenced
species demography or treatment effects, we performed a
multiple correlation analysis between precipitation and
demographic analysis results. Precipitation variables
included dry-season rainfall amount, maximum and median
rainless interval durations from current and previous year
to account for potential time-lagged responses (Table 1;
Vasconcelos 2006). Our demographic variables included
demographic rates by species and size class from control
plants to evaluate precipitation effect on species demog-
raphy and the difference between treatment and control
demographic rates to evaluate potential links between
yearly rainfall patterns and treatment response. Results
from the multiple comparisons where evaluated using
standard and Bonferroni-corrected a-values.
Results
Species demographic trends
Lacistema pubescens and Myrcia sylvatica had contrasting
patterns of survivorship for the smallest size classes, but
926 Oecologia (2010) 162:923–934
123
similarly high rates of survivorship for overstory size
classes. L. pubescens survival in the smallest two size
classes was low for the entire study period, typically rang-
ing from 0.4 to 0.8 (Fig. 1a). Survival in these size classes
only peaked above these low values during the 2002–2003
time interval when both dry seasons showed total rainfall
amounts considerably greater than usual. On the other hand,
nearly all of the survival rates observed for M. sylvatica are
above 0.8 and present no large differences among years or
size classes (Fig. 1b). The only minor temporal trend
observed for M. sylvatica suggests that the survival of the
largest size class is the most stable across all years.
For both species, the probability of growth from
understory to overstory size classes was extremely low and
there were no clear differences in growth transition prob-
abilities among overstory size classes (Fig. 1c, d). Allo-
metric height/DBH equations reveal that neither species
had understory individuals with heights close to the
equivalent to the minimum overstory size cut off (1 cm
DBH), lending further evidence to a clear overstory
recruitment limitation for both species. For M. sylvatica
individuals in the understory, large growth transition
probabilities from size class 1 and regression probabilities
for size class 2 reflect the large variability of measured
heights that results from the difficulties in evaluating
growth based on height (e.g., shoot die-backs, new leaf
flushes, etc.; Fig. 1d, f). However, these rates are excep-
tionally high for the 2002–2004 period, potentially related
to the high dry season rainfall years of 2002 and 2003. All
other regression probabilities for both species do not show
any clear temporal or size-related patterns, although
regression probabilities for overstory size classes of
M. sylvatica were noticeably higher and more variable than
that of L. pubescens (Fig. 1e, f).
Both species showed contrasting patterns of recruitment
across years. While L. pubescens showed constant and very
low yearly recruitment below 20 individuals 100 m
-2
,
M. sylvatica presented recruitment above 400 individuals
100 m
-2
in the first time interval (2001–2002). However,
M. sylvatica recruitment dropped across all years to 25
individuals 100 m
-2
by the 2005–2006 time interval
(Table 2).
Population growth patterns across time and treatments
We found that with one exception—the irrigated L. pu-
bescens population in 2003–2004—there was no significant
difference in kamong populations of the two study species
in different treatments (Fig. 2). Furthermore, we found that
only the control M. sylvatica population in the 2001–2002
transition year included positive, albeit non-significant,
population growth (i.e., k[1). The population growth rate
for L. pubescens ranged from 0.8909 (population in the
irrigation treatment in the 2005–2006 period) to 0.9913
(population in the control treatment in the 2003–2004
period). Results for M. sylvatica were similar, with k
ranging from 0.8906 to 1.006 and little difference among
treatments and years.
Two-way LTRE results
For both species, treatment differences in vital rates were
small and mostly fell within 0.05 of control values. Fur-
thermore, LTRE analysis showed that because of the dif-
ferential impacts of vital rates on population growth,
treatment effects on growth and mortality often did not
result in commensurate population growth effects for either
of the two studied species (Fig. 3). For both species, the
Table 1 Rainfall patterns for
Universidade Federal Rural da
Amazo
ˆnia research station,
Castanhal, Para
´, Brazil
Year Season Total
rainfall (mm)
Median rainless
period length (days)
Maximum rainless
period length (days)
1999 Dry 352 3 10
2000 Wet 1,922.9 1 9
2000 Dry 223.5 4.5 11
2001 Wet 3211 2 7
2001 Dry 438.9 5 32
2002 Wet 1,813.2 2 7
2002 Dry 679.4 5 16
2003 Wet 1,718.6 1 11
2003 Dry 696.8 5 21
2004 Wet 2,881.5 2 11
2004 Dry 444.9 4 25
2005 Wet 2,177.2 2 11
2005 Dry 225.2 9 19
2006 Wet 2,234.9 2 4
Oecologia (2010) 162:923–934 927
123
survival and regression probabilities make the largest
contributions to Dkacross time and treatments, with tran-
sition probabilities describing growth having a relatively
smaller impact on population growth. In addition, post hoc
bootstrapping of differences in vital rates between the
experimental and control treatments indicate that no
treatment differences in vital rates were significantly dif-
ferent when averaging data across years. However, the
evaluation of the interaction effect between treatment and
time suggests significant treatment impacts for specific
time intervals (Fig. 4). Of these time-dependent treatment
effects, only the irrigation growth of M. sylvatica’s seed-
ling size class 1 showed a constant unidirectional response
over the course of the experiment.
While vital rates varied considerably from one time
interval to the next, we found that—for both species—pat-
terns of ‘‘time’’ effects on vital rates were idiosyncratic. The
only consistent temporal pattern observed was a decrease in
the survival of all size classes of M. sylvatica during the
2003–2004 measurement interval. Surprisingly, inter-annual
rainfall patterns were not significantly correlated to size-
class specific species and treatment variability of vital rates.
Discussion
To our knowledge, our study is the first large-scale and
long-term experimental investigation of how irrigation and
litter removal influence the population dynamics of tropical
trees. We found that although previous work has docu-
mented large ecosystem-level (Vasconcelos et al. 2004,
2007,2008; Vasconcelos 2006; Veluci-Marlow 2007) and
individual-level effects (Fortini et al. 2003; Araga
˜o et al.
Fig. 1 Size class (Sz) annual
rates of survival, growth and
regression with 0.975 and 0.025
quantiles of Lacistema
pubescens (a, c, e) and Myrcia
sylvatica (b, d, f). Hgt Height,
DBH diameter at breast height
Table 2 Offspring per 100 m
2
for Lacistema pubescens and Myrcia
sylvatica across time intervals. Given no treatment differences, only
control data are shown
Year interval L. pubescens M. sylvatica
2001–2002 6.25 406.25
2002–2003 0 181.25
2003–2004 12.5 143.75
2004–2005 18.75 100
2005–2006 6.25 25
928 Oecologia (2010) 162:923–934
123
2005) of altering dry season water availability and litter
abundance in our experimental plots, the patterns and
significance of these manipulations on demography over
our 5-year experiment were generally negligible. Further-
more, the transient effects of treatment on demography
were neither related to inter-annual rainfall patterns nor
drove significant changes in population growth.
Our results suggest that the ability to intuit the conse-
quences of environmental change for population dynamics
on the basis of short-term experiments is limited. For
instance, the high unexplained temporal variability in
demographic rates resulted in time-dependent treatment
differences; were it not for our long-term and demographic
approach we could have easily misinterpreted these dif-
ferences as persistent and biologically meaningful. Fur-
thermore, the potential disconnect between changes in
individual vital rates and actual changes in population
dynamics is a cautionary tale for experimental studies that
either utilize only a subset of life stages or analyze
demographic rate responses separately (see also Halpern
and Underwood 2006). Our results also highlight the utility
of matrix models, whose integrative nature reveals long-
term patterns that would not have been detected by com-
parison of changes in population size and the distribution
or a limited subset of life history stages (Caswell 2007).
These models allow us to understand the relative impor-
tance to population dynamics of different vital rates; in
doing so they link observed shifts in population distribution
and abundance to underlying demographic mechanisms.
Furthermore, estimates of kcan be interpreted as a measure
of relative fitness (McGraw and Caswell 1996), allowing
one to better understand successional trends resulting from
altered competitive balance between species.
Previous research in tropical forests has shown that there
can be major physiological responses to water availability
(Engelbrecht and Kursar 2003; Bunker and Carson 2005;
Nepstad et al. 2007; Tanner and Barberis 2007; Yavitt and
Wright 2008). However, our understanding of how drought
impacts tropical tree populations is rudimentary. Nepstad
et al. (2007) argue that the effects could be large, in part
because large trees are at greater risk due to greater
evaporative demand of canopy exposure. This idea is
corroborated by their dry season rainfall-exclusion studies
conducted in Amazonia, which resulted in substantial
Fig. 2 Population growth rates (k)ofaL. pubescens and bM. sylv-
atica in stands with water addition and litter removal. Values are
mean ±95% confidence interval
Fig. 3 Impacts of irrigation and
litter-removal treatments on
survival, growth and regression
probabilities on population
growth of aL. pubescens and
bM. sylvatica
Oecologia (2010) 162:923–934 929
123
mortality of large trees and canopy-bound lianas (Nepstad
et al. 2007). On the other hand, irrigation experiments in
Panama and elsewhere have suggested it is actually the
seedling stages of tropical trees that are most vulnerable to
drought due to their limited root systems (Engelbrecht and
Kursar 2003; Yavitt and Wright 2008). If so, the long-term
effects of occasional droughts on population dynamics may
be limited, owing to the generally low elasticity values of
seedling-related vital rates (e.g., Bruna 2003).
Our experimental and demographic design allowed us to
explore the responses to drought of stages spanning the
seedling-adult continuum. Our results suggest the impacts
of drought on tree demography are far more complex than
simply influencing primarily seedlings or adults. On the
one hand, many of our larger adult trees were exposed to
direct sunlight, resulting in increased evaporative demand
under drought conditions. They also grew in shallow lat-
eritic soil formations that appear to limit the development
of deep root systems. Nevertheless, these conditions did not
translate into reduced growth and survivorship. On the
other hand, our study shows only limited evidence sup-
porting the notion that seedlings are highly drought sensi-
tive. Only the growth of the smallest M. sylvatica seedling
size class showed a constant increase in response to irri-
gation, which probably resulted from large changes in C
assimilation (Fortini et al. 2003). However, this effect only
lasted for 3 of the 5 years of monitoring and was shown to
be inconsequential in terms of contributions to M. sylvatica
population growth.
Large-scale, long-term natural litter-removal experi-
ments designed to explore the role of nutrient constraints
are rare in tropical ecosystems (Sayer 2006). Other
research at our study site has found relatively rapid
responses of nutrient availability, possibly reflecting the
quick and tight cycling of nutrients common in the tropical
forests (Vitousek and Sanford 1986; Veluci-Marlow 2007;
Vasconcelos et al. 2008). Our analyses suggest secondary
forest tree populations are very tolerant to these changes.
Although this tolerance is supported by fertilization
experiments demonstrating limited effects of reduced
nutrient availability on tropical forest vegetation (Mayor
and Roda 1994; Pearson and Vitousek 2001), our results
are nevertheless at odds with several other studies that have
shown clear increases in growth and survival following
nutrient addition (Gehring et al. 1999; Lawrence 2001;
Ceccon et al. 2003; Davidson et al. 2004; Yavitt and
Wright 2008). Indeed, our results are particularly surprising
given the relatively low values of soil extractable P present
at our site (Rangel-Vasconcelos et al. 2005).
Exploring the limited effects of resource limitation on k
Our results beget the question of why there were no strong
and unidirectional effects on demography and kin our two
focal species. First, it is possible that despite our large
experimental manipulations of water and nutrients, the
treatments did not result in significant changes in water and
nutrient availability. However, recent studies strongly
suggest that this is not the case. Past studies from our site
have linked changes in water availability to several eco-
system and individual-level responses, including increased
above-ground net primary productivity (ANPP; Fortini
et al. 2003; Vasconcelos et al. 2004,2007; Vasconcelos
2006; Veluci-Marlow 2007). Veluci-Marlow (2007) has
also demonstrated that our litter-removal treatment resulted
in decreased N mineralization, phosphatase activity, and
NH
4?
availability, as well as increased availability of
NO
3-
. Furthermore, Vasconcelos et al. (2008) found a
Fig. 4 Statistically significant time 9treatment effects on vital rates
of aL. pubescens,bM. sylvatica.Up arrow Increase in vital rate,
down arrow decrease in vital rate. sSurvival; ggrowth; rregression
(vital rate numbers indicate size class, e.g., g3 growth rate of size
class 3); Isignificant irrigation effect; Rsignificant litter-removal
effect
930 Oecologia (2010) 162:923–934
123
significant decrease in litterfall N content, indicative of
responses to nutrient limitation by individual trees at our
litter-removal plots. Although there are no results from this
system quantifying the increased magnitude of nutrient
limitation resulting from litter removal, the fact that the
removal of 4–5 times the initial P stocks in above-ground
fine litter over a 5-year period did not appreciably influence
the demography of our study species at such a nutrient-
poor site is surprising and merits further investigation.
Second, it is important to consider the possibility that
species with different life history strategies could be more
susceptible to changes in water and nutrient availability
than our focal taxa (McCook 1994). Past research con-
ducted at our study site suggest that other species may be
more responsive to changes in water availability than our
two focal species. A study of changes in whole-stand ANPP
in response to water availability found that whole-stand
diameter increment was linked to changes in water avail-
ability resulting from irrigation and previous dry sea-
son rainfall (Vasconcelos 2006). Although the growth of
L. pubescens individuals in size class 3 tracked the change
in ANPP for the whole stand, no other vital did. Further-
more, shifts in the size distribution of the two focal species
resulted in a drastic decrease in their population numbers,
and suggest the dynamics of these two species may be
different from others in the stand (Fig. 5). Nevertheless, it is
important to recognize that L. pubescens and M. sylvatica
represent very distinct species in the community of suc-
cessional trees found in our study site, and are the dominant
successional species in the region’s secondary forests
(L. Fortini, unpublished data). Hence, their response to our
experimental manipulations—or lack thereof—will have
important implications for the trajectory of succession.
Third,it is important to remember that the demographic
responses of a species to changes in abiotic constraints will
be influenced by how other species—which can be either
competitors or facilitators—respond to the same changes
(Goldberg 1996; Choler et al. 2001; Liancourt et al. 2005;
Suter et al. 2007). In secondary forests this is further
complicated by changes in the strength and direction of
competitive interactions over the course of a stand’s suc-
cessional trajectory (McCook 1994; Kobe et al. 1995; Mal
et al. 1997). The relative importance of different limiting
factors can also change as succession proceeds, further
shifting the competitive balance between species. As such,
the response of focal species to the same changes in abiotic
constraints may have differed if we had conducted these
experiments at earlier or later successional stages. At our
study stand, the shifts in diameter distribution for all spe-
cies present in the stand during the study period indicate an
ongoing dynamic development of the forest (Arau
´jo et al.
2005). Further support for this conclusion is that despite
continued fruiting by the two study species (L. Fortini,
personal observation), seedling recruitment by the end of
the study period was appreciably lower; this suggests that
the possibility of a delayed recruitment response to either
treatment is unlikely. This dynamism, and the myriad other
factors that also influence demography, work in a complex
fashion to influence a species’ interactions with competi-
tors; this competitive balance in turn alters population and
stand structure, leading to feedback changes in light
availability and other abiotic constraints.
While understory light availability did not vary with
respect to experimental treatment (L. Fortini, unpublished
data), there is evidence suggesting light plays an important
role in the demography of our focal species as seen else-
where (Kobe et al. 1995; Graham et al. 2003). Although
neither study species was suffering from high overstory
mortality or low reproductive output (L. Fortini, unpub-
lished data), both species showed clear bottlenecks in their
understory size classes. Almost no L. pubescens individuals
recruited in spite of ample fruiting, including in litter-
removal plots where the elimination of the litter layer
should have resulted in increased understory recruitment
(Facelli and Pickett 1991). Furthermore, there was also an
understory bottleneck in M. sylvatica—despite ample
understory recruitment, nearly no individuals survived to
reach the smaller reproductive size classes. Given the
previously documented impacts of water and nutrient
availability on stand- and individual-level processes at our
study site and elsewhere, we expected controls over forest
succession were potentially more complex than overriding
autogenic control through light availability (Huston and
Fig. 5 Changes in the diameter distribution of aL. pubescens,bM.
sylvatica and call other species from control plots at the 14-year-old
secondary forest in Apeu
´, Para
´, Brazil. Irrigation and litter-removal
plots exhibited similar distributional shifts
Oecologia (2010) 162:923–934 931
123
Smith 1987). Our results suggest that, for some species and
at certain successional stages, light availability may still
overshadow prolonged alterations of other ecosystem
properties posited critical for forest function.
Our results suggest a set of research directions and
related experiments that merit further exploration. First, it
is necessary to explore the role of autogenic successional
factors (e.g., light availability, root competition) in medi-
ating population response to exogenous abiotic constraints.
This could be done by monitoring of seedlings to adults
from a number of species of contrasting life history traits in
similar manipulative experiments, therefore ensuring a
better representation of species under varied strengths of
autogenic control from stand structure. Alternatively, one
could explore the effects of experimental manipulations of
abiotic factors along a chronosequence representing dif-
ferent stages of succession. Second, applied treatments
should ideally include multidirectional manipulations (e.g.,
irrigation and exclusion) to properly evaluate limitations to
typical and atypical stress conditions. Finally, such exper-
iments should monitor how treatments impact competitive
ability/relative fitness of individuals over time to begin
understanding the potentially complex response of popu-
lations in a diverse community setting. Such experimental
approaches, coupled with recent theoretical advances
(Caswell 2007), could help investigate the potentially
important role of transient population dynamics.
Lastly, it is also worth noting how the contrasting
demographic patterns for the two focal species clearly
reflect their distinct successional roles. L. pubescens
establishes stand dominance early on, but soon declines in
abundance. We found no consistent temporal patterns in
L. pubescens demographic rates, suggesting the patterns of
demography we observed reflect ecological influences
that preceded our monitoring of the stand. In contrast,
M. sylvatica’s inverse-J population structure, high survival
of smaller size classes, and initially high understory
recruitment are consistent with the observation that its
dominance in the successional community lags behind
that of L. pubescens. Nevertheless, the near absence of
recruitment into M. sylvatica’s understory stages and the
smallest overstory size class implies the long-term persis-
tence of M. sylvatica is unlikely. If so, this gives rise to
increased dominance of other species in the successional
progression of these stands, although it does not exclude
the possibility of M. sylvatica’s return from the seed bank
or from younger neighboring stands following disturbance.
Conclusion
With the growing interest in the mitigation of anthropo-
genic disturbance and changes in global C dynamics,
research on processes and factors constraining tropical
forest regrowth is flourishing (Vester and Cleef 1998;
Coomes et al. 2000; Johnson et al. 2000; Moran et al. 2000;
de Jong et al. 2001; Guariguata and Ostertag 2001; Capers
et al. 2005; Vasconcelos 2006). While our results suggest
the population growth rates of secondary forest tree
species are resilient to altered precipitation regimes or
land-use-induced nutrient limitation, the complex mecha-
nisms underlying this response clearly indicate a need for
work in other systems and with a broad diversity of species.
If climate change results in increases in precipitation for
the region (Marengo 2004), our results suggest that the
demography and population dynamics of some species will
be minimally affected by increases in the frequency of dry
season rainfall. However, if climate change results in more
intense dry seasons (Harris et al. 2008), rainfall-exclusion
experiments are more likely to take plants into water stress
levels beyond those commonly experienced in typical dry
seasons and thus may be valuable complements to our
present study (Nepstad et al. 2007). In effect, while
addressing the consequences of climate change on
tree populations in the Amazon, both irrigation and rain-
fall-exclusion experiments only offer partial answers.
Similarly, nutrient limitation comparable to that in our
experimental manipulations would also be predicted to
have limited effects on demography.
Acknowledgments We thank Osorio Oliveira, Glebson Sousa, and
Evandro da Silva for their assistance in the field, and Raimundo
Nonato da Silva (UFRA) and De
´bora Araga
˜o for logistical support.
This research was conducted under cooperative agreements between
the University of Florida, Universidade Federal Rural da Amazonia
and Embrapa Amazo
ˆnia Oriental and supported by a grant from the
Andrew Mellon Foundation to D. J. Z., a grant from Conselho
Nacional de Desenvolvimento Cientı
´fico e Tecnolo
´gico—CNPQ to
I. S. M. and an EPA STAR fellowship to L. B. F. All conducted
experiments comply with current Brazilian laws.
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    • Using M. paraensis (the most abundant species) as an example, the integration of demographic effects of logging using life table response experiments (LTRE) shows that demographic rates most affected by logging may not be the most important for determining post-harvest tree population dynamics. These conclusions are important because harvest evaluations commonly consider growth, survival, and recruitment effects separately, and may misrepresent changes in population dynamics resulting from observed demographic effects [36]. Without the use of an integrated population approach, however, it would not be possible to detect the larger contribution that smaller juvenile growth increases offer to the persistence of the species in the stand.
    [Show abstract] [Hide abstract] ABSTRACT: At the Amazon estuary, the oldest logging frontier in the Amazon, no studies have comprehensively explored the potential long-term population and yield consequences of multiple timber harvests over time. Matrix population modeling is one way to simulate long-term impacts of tree harvests, but this approach has often ignored common impacts of tree harvests including incidental damage, changes in post-harvest demography, shifts in the distribution of merchantable trees, and shifts in stand composition. We designed a matrix-based forest management model that incorporates these harvest-related impacts so resulting simulations reflect forest stand dynamics under repeated timber harvests as well as the realities of local smallholder timber management systems. Using a wide range of values for management criteria (e.g., length of cutting cycle, minimum cut diameter), we projected the long-term population dynamics and yields of hundreds of timber management regimes in the Amazon estuary, where small-scale, unmechanized logging is an important economic activity. These results were then compared to find optimal stand-level and species-specific sustainable timber management (STM) regimes using a set of timber yield and population growth indicators. Prospects for STM in Amazonian tidal floodplain forests are better than for many other tropical forests. However, generally high stock recovery rates between harvests are due to the comparatively high projected mean annualized yields from fast-growing species that effectively counterbalance the projected yield declines from other species. For Amazonian tidal floodplain forests, national management guidelines provide neither the highest yields nor the highest sustained population growth for species under management. Our research shows that management guidelines specific to a region's ecological settings can be further refined to consider differences in species demographic responses to repeated harvests. In principle, such fine-tuned management guidelines could make management more attractive, thus bridging the currently prevalent gap between tropical timber management practice and regulation.
    Full-text · Article · Aug 2015
  • [Show abstract] [Hide abstract] ABSTRACT: Understanding the pattern of species diversity and soil factors can enhance our knowledge of the mechanism of vegetation recovery, however, there is still a gap in the knowledge of succession rate and trend for species diversity in relation to soil nutrients during the vegetation recovery process. Patterns of species diversity and soil nutrients during the tropical vegetation recovery as well as the correlation between species diversity and soil nutrients were explored in Hainan Island, located in southern China. Plots assigned as grassland stage (GS), shrub stage (SS), secondary forest stage (SFS), and primary forest stage (PFS) were established using a chronosequence approach. Results showed that species richness and evenness increased from GS to PFS. Species dominance/diversity curves were fitted using the lognormal distribution model (r 2 = 0.891–0.972). Species richness for the herb layer was maximal at SFS, whereas species richness for both the shrub layer and tree layer reached their maximum at PFS. Species turnover and soil total phosphorus decreased, whereas organic matter and total nitrogen increased from GS to PFS. Organic matter and total nitrogen were both positively correlated with species richness and total coverage, and total phosphorus was positively correlated with species turnover. The results clearly demonstrate that diversity asymptotically increases and positively correlates with increasing soil fertility, and the total phosphorus value is predicted to be an important soil factor that affects successional rate during tropical vegetation recovery processes.
    Article · May 2012
  • [Show abstract] [Hide abstract] ABSTRACT: Ecologically relevant restoration of secondary Atlantic forest on abandoned land offers a potential means to recover biodiversity and improve crucial ecosystem services, including carbon sequestration. Early secondary successional trajectories are determined by a range of environmental factors that influence plant community development. Context-specific understanding of forest vegetation communities, their dynamics, and underlying drivers is needed for future restoration strategies. In this study we examined relationships between soil (chemical and physical) and environmental (landscape and topographical) characteristics, plant community attributes, and carbon stocks during early secondary succession. Data were collected at two sites undergoing early secondary succession in seasonally-dry Atlantic Forest (Rio de Janeiro State, Brazil). Both sites were previously used for pasture and abandoned at similar times, but showed differing vegetation communities. We found tree biomass and diversity and ecosystem carbon storage to be strongly positively related to the amount of surrounding forest, less steep slopes and clay soils, and negatively to the abundance of the shrub Leandra aurea. Soil carbon pools significantly increased with aboveground tree biomass. The only factor significantly affecting the metric of overall successional development (combining tree biomass and diversity) was total surrounding forest cover. Our findings suggest recovery of secondary forest and below- and aboveground carbon storage is limited by the amount of adjacent forest, some soil properties and dense shrub establishment down-regulating the succession process. Overall we offer evidence of potential to improve recovery of Atlantic forest with ecologically relevant seeding/planting programmes and selective shrub removal that could benefit ecosystem carbon storage.
    Article · Aug 2015
Article
April 2007 · Biotropica · Impact Factor: 2.08
    Leaf-litter decomposition is a major component of carbon and nutrient dynamics in tropical forest ecosystems, and moisture availability is widely considered to be a major influence on decomposition rates. Here, we report the results of a study of leaf-litter decomposition of five tree species in response to dry-season irrigation in a tropical forest regrowth stand in the Brazilian Amazon;... [Show full abstract]
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    July 2003 · American Journal of Botany · Impact Factor: 2.60
      Analyses of the effects of drought stress on Amazonian regrowth stands are lacking. We measured leaf gas exchange and leaf water potential of Miconia ciliata (Melastomataceae) in a dry-season irrigation experiment in 14-yr-old regrowth. In the dry season, irrigated plants maintained significantly higher leaf water potentials, photosynthetic capacity at light saturation (A(max)), stomatal... [Show full abstract]
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      August 2010 · New Phytologist · Impact Factor: 7.67
        *Fine root dynamics is widely recognized as an important biogeochemical process, but there are few data on fine root growth and its response to soil resource availability, especially for tropical forests. *We evaluated the response of fine root dynamics to altered availability of soil water and nutrients in a 20-yr-old forest regrowth in eastern Amazonia. In one experiment the dry season... [Show full abstract]
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        April 2015 · Revista Brasileira de Ciência do Solo · Impact Factor: 0.76
          Soil microbial biomass (SMB) plays an important role in nutrient cycling in agroecosystems, and is limited by several factors, such as soil water availability. This study assessed the effects of soil water availability on microbial biomass and its variation over time in the Latossolo Amarelo concrecionário of a secondary forest in eastern Amazonia. The fumigation-extraction method was used to... [Show full abstract]
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