Caribbean Journal of Science, Vol. 44, No. 1, 36-42, 2008
Copyright 2008 College of Arts and Sciences
University of Puerto Rico, Mayagüez
Root Proliferation and Nutrient Limitations in a Nicaraguan
Rain Forest
BRENT C. BLAIR1 AND IVETTE PERFECTO
School of Natural Resources and Environment, University of Michigan, 430 East University,
Ann Arbor, MI 48105 USA
1
Corresponding author; current address: Department of Biology, Xavier University, 3800 Victory Parkway, Cincinnati,
OH 45207-4331, USA; E-mail: blairb@xavier.edu
ABSTRACT.—Knowledge of plant nutrient limitations within natural and agricultural ecosystems is important for a full understanding of the ecology of plant populations and communities. While broad generalizations have been made for wet tropical forests there are few studies that directly address the question of
nutrient limitations. The lack of research, in part, is due to the time and expense of traditional long-term
fertilization experiments that examine ecosystem productivity under different nutrient regimes. To identify
nutrient limitations within a lowland tropical rainforest we utilized an alternative method, the root ingrowth-core technique, which uses nutrient enriched substrates implanted into the forest soil. Over time root
growth into the enriched substrates is greatest in those containing limiting nutrients. In addition, we analyzed intact soil cores from the forest floor for nutrients and root length density to see if natural nutrient
variations were sufficient to elicit changes in root proliferation. We found that root ingrowth cores as well
as soil cores showed greater root length in cores richer in phosphorus and nitrogen. Comparisons between
root ingrowth core treatments revealed no differences in root width. However, overall root width was greater
in the ingrowth cores than in the forest soil. While most authors suggest that phosphorus and nutrient cations
(e.g., K, Mg, and Ca) tend to be limiting in lowland tropical forests, our study suggests that both phosphorus
and nitrogen but not potassium are in limited supply within the forest studied.
KEYWORDS.—ingrowth core; Nicaragua; root allocation; root foraging; root plasticity; soil; tropical lowland
forest
ent is necessarily limiting if plants in the
area are not restricted in their ability to
grow and reproduce (Gleeson & Good
2003).
More than 60 percent of tropical soils are
ultisols and oxisols, which are characterized by the presence of highly weathered
clays and low nutrient availabilities (Vitousek & Sanford 1986). In wet tropical
lowland forests phosphorus and nutrient
cations (e.g., K, Mg and Ca) are frequently
cited as being limiting (Vitousek & Sanford
1986, Cuevas & Medina 1988, Burslem et al.
1994, Gehring et al. 1999). Previous soil
analysis in the forest of the present study
supports this contention and while available P and K are at low levels (P = 2.89 ±
0.14 ␮g/g, K = 0.27 ± 0.004 cmol+/kg), total
N (5.40 ± 0.04 mg/g) is relatively more
abundant (Blair 2005).
Nutrient limitations can be at least partly
addressed through fertilizer experiments
that include measurements of long-term
INTRODUCTION
The relationship between nutrient limitation and plant growth is central to our understanding of both plant and ecosystem
function. Traditionally, absolute levels of
nutrients are assessed and the least available is deemed the limiting nutrient for the
ecosystem in question (Gleeson & Tilman
1992). This simplistic view causes problems
when used across ecosystems. For example,
a relatively rich tropical ultisol is likely nutrient poor when compared to an average
temperate alfasol. Currently, the concept of
nutrient limitations has shifted to the idea
that resource limitations are not so much
dependant on absolute levels, but on the
adaptation of plants growing in a particular
environment (Tilman 1982, Gleeson & Tilman 1992). While tropical rainforest soils
are generally quite low in nutrients compared to their temperate counterparts this
does not mean that all or the lowest nutri36
NUTRIENT LIMITATION IN A NICARAGUAN RAIN FOREST
plant growth responses. Although occasionally performed, time, expense and in
some areas legal limitations to manipulative experiments (e.g., national parks) make
this type of study difficult (Raich et al.
1994). An alternative method utilizes the
propensity of plants to proliferate roots in
areas with high levels of limiting nutrients.
One method uses root ingrowth cores
made from mesh bags or porous plastic
tubes which are filled with a rooting substrate and implanted into the forest floor
(Lund et al. 1970, Steen 1991). Although
originally intended to measure agricultural
root productivity, Cuevas & Medina (1988)
used ingrowth cores enriched with different nutrients to identify nutrient limitations
for fine root growth in several Amazonian
forest habitats. Raich et al. (1994) demonstrated that this technique could also indicate forest nutrient limitations by comparing root proliferation in ingrowth cores to
previous long-term fertilization studies.
More recent studies have verified this
method’s accuracy and utilized it to indicate limiting nutrients in a variety of ecosystems (Stewart 2000, McGrath et al. 2001,
Gleeson & Good 2003).
Root foraging is a widely recognized aspect of plant ecology. However, plant species foraging effectiveness varies greatly
overall and for specific nutrients (see Robinson 1994 for review). Roots are able to
enhance nutrient uptake, either through
morphological or physiological mechanisms. Foraging physiologically involves
absorbing more of a nutrient per unit root
length. Morphological foraging involves
changing the size or form of a root system
to maximize root absorption. This study focuses on morphological mechanisms.
Specifically, we examined the ability of
plants to alter root length and width in response to increased nutrient availability.
Increased root length is the most commonly studied aspect of root foraging and
is usually determined either by measuring
root length directly or by obtaining root
weight (Hutchings 1988, Pregitzer et al.
1993, Cain 1994, Einsmann et al. 1999,
Johnson & Biondini 2001, Blair & Perfecto
2004). In general root weight is a less desirable measure of root proliferation due to
37
changes in root width. On a per gram basis
fine roots have a greater surface area, and a
higher potential for nutrient absorption,
than coarse roots. Further, studies show
that fine roots are responsible for the bulk
of plant nutrient uptake while larger roots
are structural and used as jumping off
points for their thinner counterparts (Nye
& Tinker 1977, Caldwell & Richards 1983).
Within this study we used a mesh bag
technique to examine morphological foraging within a wet tropical forest in Nicaragua. In a previous study we showed that
roots preferentially grow into patches of
leaf litter than in the forest’s clayey soil
(Blair & Perfecto 2001). Presumably this
was because the leaf litter contained significantly greater quantities of nutrients. In
this study we use a similar technique to
determine if roots will grow more prolifically into substrates with elevated amounts
of specific nutrients (N, P and K) using a
similar ingrowth core technique. Because
previous work in this forest has shown that
P and K are the nutrients in lowest supply
(Blair 2005), we hypothesized that roots
would forage significantly more into substrates that are high in P and K than in the
N enriched substrate.
Methods
Study site.—The study was conducted on
a 30 × 40 m plot within a wet tropical forest
on the Caribbean coast of Nicaragua
(11°53N’, 83°58’W, 20 m altitude) ca. 15-km
northwest of the city of Bluefields. Characterized by a patchwork of forest and farmland, this region on Nicaragua’s agricultural frontier was struck in 1988 by a
category four storm (hurricane Joan) that
severely damaged the forest (Yih et al.
1991). The forest (>60 tree species per 0.1 ha
plot) is dominated by species characteristic
of wet tropical, primary rainforests (Vandermeer et al. 2000). The area’s mean
monthly temperature is 27°C, and receives
an average annual precipitation of 4800
mm. The forest’s soils are Ultisols with a
thin organic horizon (<3 cm) and a moderately thick A horizon (15-20 cm). The soils
are acidic with pH ranging between 3.94.7 (Picone 2000). The wet season lasts for
38
BRENT C. BLAIR AND IVETTE PERFECTO
ten months of the year with a short dry
season from February through March. Experiments were conducted between July
and October of 1999.
Experimental design.—Root ingrowth
cores (Lund et al. 1970, Steen 1991) were
filled with nutrient enriched vermiculite, a
nutrient-free substrate. Vermiculite was
soaked for 24 h in either purified water or
0.1 M solution of NH4Cl, NaHPO4, or KCl.
We used vermiculite soaked in purified
water as the control. The enriched substrate
of each of the four treatments was then
packaged in cylindrical mesh bags (9 cm
diameter × 20 cm length, 5 mm mesh diameter) constructed from synthetic minnow
seine (North American Sports Products,
Detroit, Michigan). Bags were filled to
equal volumes to minimize differences in
surface area of each treatment. After packaging, the tops of the bags were tied shut
with color-coded nylon string. Each treatment was replicated 20 times for a total of
80 ingrowth cores.
A sampling grid was created over the 30
× 40 m plot, with grid points at 10 m intervals. A complete block design was applied
with blocks of four cores, one from each
treatment. The grid points served as center
points for mesh bag placement. At each
point, a block of cores was implanted in the
soil with cores planted 0.5 m north, south,
east, and west of the center point. This resulted in blocks with one bag from each
treatment being distributed in a square
where adjacent bags were ca. 0.7 m apart.
Between blocks bags were at least 9 m
apart. At each site used for ingrowth core
placement, the surface leaf litter was removed and a shallow hole (10 × 15 cm
depth) was created using a circular steel
coring tube. An ingrowth core was placed
in each hole and surrounding soil was
firmly pressed down to fill gaps and ensure
contact between the soil and the substrate
in each bag. Finally, the protruding top of
the ingrowth core was marked with fluorescent spray-paint for future identification
and the previously removed leaf litter was
replaced over the treatment area.
To compare natural rooting densities of
the forest to that of the implanted ingrowth
cores, in both September and October of
1999 ten soil cores (15 × 20 cm depth) were
obtained at random points within an adjacent 50 × 50 m forest plot (20 cores total). In
addition to providing rooting information
on undisturbed soil, these soil cores were
analyzed for nutrient availability.
Analysis.—The ingrowth core experiment
was run for 4 months before harvest to allow sufficient time for roots to encounter
and potentially proliferate into the substrates. At the end of the designated periods, cores were harvested using a small
machete to cut roots from around the bags.
Once removed, protruding roots were
trimmed using scissors. After harvest, all
roots were carefully separated from the
substrates using a combination of wet sieving (2 mm mesh diam.) and visual inspection. Roots were stored in a 30 percent alcohol solution until analysis. Dead roots,
though rare, were included in all analyses
when present. Roots from soil cores collected in September and October were similarly separated and stored.
Roots were scanned using a desktop
scanner and light bank system to obtain binary root images (Richner et al. 2000).
These images were then examined using
the program ROOTEDGE (Kasper & Ewing
1997), which estimates root length and diameter using the edge chord algorithm
(Ewing & Kasper 1995).
Variability of total root length within
treatments was measured by the coefficient
of variation (CV = s/x̄). Differences in root
length density (RLD, cm/cm3) among the
substrates were tested by one-way analysis
of variance (ANOVA), using log-transformed data to meet assumptions of normality and equal variances. Root length
density of soil cores was also examined using correlation analysis to see if roots grew
preferentially into soil of naturally elevated
nutrient availabilities.
Nutrient analysis was performed on five
replicates of each ingrowth core treatment
that were subsampled and mixed thoroughly. The resulting pooled subsamples
were tested for total nitrogen, available
phosphorus and available potassium, as indicators of their nutrient content. Soil cores
were individually analyzed for total nitrogen, available phosphorus and available
NUTRIENT LIMITATION IN A NICARAGUAN RAIN FOREST
potassium. All analyses were done on airdried substrate and soil.
Total nitrogen was determined by oxidizing 30-mg subsamples of ground soil/
substrate in a C-H-N analyzer (NC2500, CE
Instruments, Milan, Italy). Soil phosphorus
was determined using 2-g subsamples extracted with 10ml Olsen’s solution (Olsen &
Sommers 1982) and automated colorometry (ALPKEM RFA 300, ALPKEM Corporation, Wilsonville, Oregon). Available potassium was determined through 1g
subsamples extracted with 10 ml 1M
NH4Cl (Olsen & Sommers 1982) and flame
spectrophotometry (Perkin Elmer 403, Perkin Elmer Corporation, Norwalk, CN).
RESULTS
Nutrient levels.—At the end of the experiment, ingrowth cores enriched with N and
P still held these nutrients at elevated levels
compared to surrounding soil, while cores
not enriched had low background quantities (Table 1). Ingrowth cores dosed with K
had increased K availability when compared to other treatments. However, background levels of K in the P cores were
higher than the average level of K in the
forest soil (Table 1). This was an unexpected result likely due to natural nutrient
variation of K in the area and vermiculite’s
propensity to adsorb nutrients, due to its
high cation exchange capacity.
Root density and width.—The N and P ingrowth cores had significantly greater total
TABLE 1. Nutrient content of root ingrowth cores
and forest soil. Ingrowth core data represent pooled
samples. Soil data are means (±SE). Leaf litter and clay
data are from a separate experiment (Blair & Perfecto
2001).
Treatment
Nitrogen
Phosphorus
Potassium
Control
Forest soil
Leaf litter
Clay
Total N
(mg/g)
Available P
(␮g/g)
Available K
(cmol+/kg)*
11.9
<0.1
<0.1
1.0
5.03 ± 0.02
10.4
0.7
1.55
21.28
2.04
1.57
3.88 ± 0.37
6.68
<.10
0.42
0.66
1.86
0.37
0.44 ± <0.01
—
—
*Dashes indicate substrates not included in analysis.
39
root length densities than cores containing
either the K or the control substrate. The
forest soil cores had significantly lower root
length density than the P treatment but
higher densities than the K treatment
(Table 2). The forest soil had thicker roots
than the four ingrowth core treatments, but
no significant differences existed between
ingrowth core treatments (Table 2).
All ingrowth cores had roots present at
the time of harvest. Variability of root ingrowth between cores of each treatment
showed the control treatment to be highest
(CV = 67%) followed by K (CV = 56%), P
(CV = 50%), N (CV = 47%) and soil core
(CV = 35%) treatments. Within the forest
soil cores root length density was significantly correlated with both N (r = 0.45, P =
0.05) and P (r = 0.49, P = 0.03) but not with
K. Root width was uncorrelated with nutrient levels but N and P were highly correlated with each other (r = 0.902, P < 0.001).
DISCUSSION
Although preliminary, our study suggests that both N and P availability in this
forest ecosystem is less than optimal. This
is supported by both the ingrowth core
TABLE 2. Root length density and root diameter
means (±SE) found in root ingrowth cores by treatment and in forest soil. Soil data are from soil cores
(0–20 cm depth) taken in September and October 1999.
Leaf litter and clay data are from a separate experiment (Blair & Perfecto 2001).
Treatment
N
Root length
density
(cm/cm3)*
Nitrogen
Phosphorus
Potassium
Control
Forest soil
Leaf litter
Clay
20
20
20
20
20
20
20
1.096ab ± 0.123
1.533a ± 0.164
0.494d ± 0.062
0.565cd ± 0.083
0.844bc ± 0.066
2.428 ± .402
0.357 ± .062
Root
diameter (cm)*
0.050a ± 0.007
0.057a ± 0.012
0.051a ± 0.010
0.051a ± 0.014
0.066b ± 0.003
—
—
*Treatment differences were significant overall for
root length density (F = 13.52; df = 4,95; P < 0.001) and
for root diameter (F = 7.017; df = 4,95; P = 0.006).
Comparisons of treatment means based on Tukey’s
HSD multiple comparison tests. Treatments that do
not share a superscript letter have significantly different means (P < 0.05). Dashes indicate substrates not
included in the analysis.
40
BRENT C. BLAIR AND IVETTE PERFECTO
data and correlations between in situ soil
nutrient availability and root length density data. The propensity of roots to forage
for N was unexpected. Both generalizations
about nutrient limitations of lowland tropical forests on ultisols (Vitousek & Sanford
1986), and the high levels of total N found
in the forest soil (Table 1) suggested that N
limitation would be unlikely. However,
due to the complicated nature of N pathways (mineralization and nitrification) it is
difficult to extrapolate N availability from
total nitrogen pools or its available forms
(ammonium and nitrate) (Vitousek & Matson 1985, Denslow et al. 1987).
Nonetheless, Gleeson & Good (2003) suggest plants in general may be more prone to
forage for N than for P. While N uptake is
primarily limited to root absorption, most
plants can significantly enhance P uptake
through the utilization of mycorrhizae (Fitter 1985, Koide & Elliott 1989). Thus, a mycorrhizal plant may avoid the considerable
carbon cost of additional fine root production if mycorrhizae can provide sufficient
quantities of P. In contrast N deficient
plants may be more dependent on proliferation of roots in N rich microsites.
Friend et al. (1990) demonstrated that
seedlings of Douglas fir in N-stressed conditions grew more roots into enriched soil
than when grown in an N-rich environment, suggesting root foraging is dependant on the nutrient stress of the whole
plant. Hetrick et al. (1991) found that the
ability of roots to forage is inhibited by inoculation with arbuscular mycorrhizae,
which reduced root branching and lateral
root extension. However, recent studies
show that this response is not universal and
when plants are grown in impoverished
soils mycorrhizal infection does not always
inhibit root proliferation (Farley & Fitter
1999, Wijesinghe et al. 2001). Soil nutrient
status was not specifically examined in
these studies but soil nutrient status is often
the deciding factor in whether plants are
infected by mycorrhizae (Allsopp & Stock
1994) and may influence whether infected
plants continue to forage for nutrients. Regardless of mycorrhizal status, in nutrient
poor environments root proliferation may
represent a plant’s only alternative to obtain a sufficient nutrient supply.
We found no significant treatment effects
on average root diameter in the ingrowth
cores or in situ comparisons between soil
nutrients and root width. These results
were consistent with a pot experiment that
found little variation in root diameter of
tropical trees in response to P patches (Blair
& Perfecto 2004). It was not consistent with
our previous ingrowth core study, which
found root diameter size-class related to
nutrient content in this forest (Blair & Perfecto 2001). However, this previous experiment used several substrates of varying nutrient quality (e.g., leaf litter and clayey
forest soil (20-40 cm depth)) and a substrate
effect on root width is possible. In the present study the only width differences were
between roots in the forest soil (0-20 cm
depth) and in the vermiculite ingrowth
core treatments (Table 2). Differences in
textural properties of the substrates are a
likely cause although we are not able to
dismiss root age as roots in the intact soil
were probably older on average than those
in the ingrowth-cores.
Background levels of K in the ingrowthcores were higher than expected. However,
concentration of available K in the control
(.37 cmol+/kg) and N (.42 cmol+/kg) treatments were still slightly lower than the average of the surrounding soil (.44 cmol+/
kg). The P treatment displayed increased
concentration of K (.66 cmol+/kg) compared to the control. When total root length
in the K treatment is compared to that of
the control (Table 2) or the clay treatment in
the substrate experiment (F = 2.38; df =
1,38; P = 0.132) there were no significant
differences in total root length densities.
This suggests that the elevated background
levels of K did not increase total root
lengths and supports the conclusion that in
this forest K does not increase root length
density.
Within the forest studied here, roots
grew preferentially into substrates high in
N and P. Following other root-ingrowth
core experiments in the wet tropics (St.
John 1983, Cuevas & Medina 1988, Raich et
al. 1994, Ostertag 1998), this study supports
the idea that plants take advantage of nu-
NUTRIENT LIMITATION IN A NICARAGUAN RAIN FOREST
trient patches by increasing total root
length. Most root foraging studies depend
on artificially elevated nutrient levels.
However, our study also showed that even
the natural variations in these tropical forest soils appear to elicit root proliferation.
While some initial work exists, further
study is needed to determine the ubiquitousness of the observed response among
plants of different successional status
(Johnson & Biondini 2001), growth form
(Einsmann et al. 1999), and ultimately the
importance of nutrient limitations to plant
competition (Gusewell & Bollens 2003).
Acknowledgments.—We would like to
thank J. Vandermeer for his input at the
beginning of this project and the Centro de
Investigaciones y Documentación de la
Costa Atlantica (CIDCA) for the use of their
facilities and logistical support. The manuscript was greatly improved by comments
from L. D. Potter and D. Plante. This study
was funded by a grant from the Fulbright
Foundation (to the author) and a grant
from the National Science Foundation
(DEB 9524061 to John Vandermeer).
LITERATURE CITED
Alsopp, N., and W. D. Stock. 1994. VA mycorrhizal
infection in relation to edaphic characteristics and
disturbance regime in three lowland plant communities in the south-western Cape, South Africa. J.
Ecol. 82: 271-279.
Blair, B. C. 2005. Fire effects on the spatial patterns of
soil resources in a Nicaraguan wet tropical forest. J.
Trop. Ecol. 21:435-444.
Blair, B. C., and I. Perfecto. 2001. Nutrient content and
substrate effect on fine root density and size distribution in a Nicaraguan rain forest. Biotropica 33:
697-701.
Blair, B. C., and I. Perfecto. 2004. Successional status
and root foraging for phosphorus in seven tropical
tree species. Can. J. For. Res. 34: 1128-1135.
Burslem, D. F. R. P., I. M. Turner, and P. J. Grubb.
1994. Nutrient status of coastal hill dipterocarp forest and adinandra belukar in Singapore: bioassays
of nutrient limitation. J. Trop. Ecol. 10: 579-599.
Cain, M. 1994. Consequences of foraging in clonal
plant species. Ecology 75: 933-944.
Caldwell, M. M., and J. Richards. 1983. Competing
root systems: morphology and models of absorption. In On the economy of plant form and function, ed.
T. Givnish, 251-273. New York: Cambridge University Press.
41
Cuevas, E., and E. Medina. 1988. Nutrient dynamics
within Amazonian forests II: fine root growth, nutrient availability and leaf litter decomposition.
Oecologia 76: 222-235.
Denslow, J. S., P. M. Vitousek, and J. C. Schultz. 1987.
Bioassays of nutrient limitation in a tropical rain
forest soil. Oecologia 74: 370-376.
Einsmann, J. C., R. H. Jones, P. Mou, and R. Mitchell.
1999. Nutrient foraging traits in 10 co-occurring
plant species of contrasting life forms. J. Ecol. 87:
609-619.
Ewing, R., and T. Kasper. 1995. Accurate perimeter
and length measurement using an edge chord algorithm. Journal of Computer Assisted Microscopy 7:
91-100.
Fitter, A. H. 1985. Functioning of vesicular-arbuscular
mycorrhizas under field conditions. New Phytol. 99:
257-265.
Farley, R. A., and A. H. Fitter. 1999. The responses of
seven co-occurring woodland herbaceous perennials to localized nutrient-rich patches. J. Ecol. 87:
849-859.
Friend, A. L., M. R. M. Eide, and T. M. Hinckley. 1990.
Nitrogen stress alters root proliferation in douglasfir seedlings. Can. J. For. Res. 20: 1524-1529.
Gehring, C., M. Denich, M. Kanashiro, and P. L. G.
Vlek. 1999. Response of secondary vegetation in
eastern Amazonia to relaxed nutrient availability
constraints. Biogeochem 45: 223-241.
Gleeson, S. K., and R. E. Good. 2003. Root allocation
and multiple nutrient limitation in the New Jersey
Pinelands. Ecol. Lett. 6: 220-227.
Gleeson, S. K., and D. Tilman. 1992. Plant allocation
and the multiple limitation hypothesis. Am. Nat.
139: 1322-1343.
Gusewell, S., and U. Bollens. 2003. Composition of
plant species mixtures grown at various N: P ratios
and levels of nutrient supply. Basic and Appl. Ecol.
4 (5): 453-466.
Hetrick, B. A. D., G. W. T. Wilson, and J. F. Leslie.
1991. Root architecture of warm- and cool-season
grasses: relationship to mycorrhizal dependence.
Can. J. Bot. 69: 112-118.
Hutchings, M. 1988. Differential foraging for resources
and structural plasticity in plants. Trends Ecol. and
Evol. 3: 200-204.
Johnson, H. A., and M. E. Biondini. 2001. Root morphological plasticity and nitrogen uptake of 59
plant species from the Great Plains grasslands
USA. Basic Appl. Ecol. 2: 127-143.
Kasper, T., and P. Ewing. 1997. ROOTEDGE: software
for measuring root length from desktop scanner
images. Agron. J. 89: 932-940.
Koide, R. T., G. Elliott. 1989. Cost, benefit and efficiency of the vesicular-arbuscular mycorrhizal
symbiosis. Func. Ecol. 3: 252-255.
Lund, Z., R. Pearson, and G. Buchanan. 1970. An implanted soil mass technique to study herbicide effects on root growth. Weed Sci. 18: 279-281.
McGrath, D. A., M. L. Druyea, and W. P. Cropper.
2001. Soil phosphorus availability and fine root
42
BRENT C. BLAIR AND IVETTE PERFECTO
proliferation in Amazonian agroforests 6 years following forest conversion. Agr. Ecosyst. and Environ.
83: 271-284.
Nye, P., and P. Tinker. 1977. Solute Movement in the
Soil-Root System. Berkeley, California: Univ. of
California Press.
Olsen, S., and L. Sommers. 1982. Phosphorus (Chap.
24). In Methods of soil analysis, Part 2. Chemical and
microbiological properties, eds. A. Page, R. Miller,
and D. Keeney, 403-430. Madison, Wisconsin:
American Society of Agronomy.
Ostertag, R. 1998. Belowground effects of canopy gaps
in a tropical wet forest. Ecology 79: 1294-1304.
Picone, C. 2000. Diversity and abundance of arbuscular-mycorrhizal fungus spores in tropical forest
and pasture. Biotropica 32: 734-750.
Pregitzer, K., R. Hendrick, and R. Fogel. 1993. The
demography of fine roots in response to patches of
water and nitrogen. New Phytol. 125: 575-580.
Raich, J., R. Riley, and P. Vitousek. 1994. Use of rootingrowth cores to assess nutrient limitations in forest ecosystems. Can. J. For. Res. 24: 2135-2138.
Richner, W., M. Liedgens, H. Bürgi, A. Soldati, and P.
Stamp. 2000. Root analysis and interpretation. In
Root methods: A handbook, eds. A. L. Smit, A. G.
Bengough, C. Engels, M. Van Noordwijk, S. Pellerin, and S. C. Van De Geijn, 305-341. Berlin:
Springer-Verlag.
Robinson, D. 1994. Tansley review no.73: The responses of plants to non-uniform supplies of nutrients. New Phytol. 127: 635-674.
Stewart, C.G. 2000. A test of nutrient limitation in two
tropical mountain forests using root ingrowth
cores. Biotropica 32: 369-373.
Steen, E. 1991. Usefulness of the mesh bag method in
quantitative root studies. In Plant Root Growth: an
ecological perspective, ed. D. Atkinson, 75-86. Oxford: Blackwell Scientific Publications.
St. John, T. 1983. Response of tree roots to decomposing organic matter in two lowland Amazonian rain
forests. Can. J. For. Res. 13: 346-349.
Tilman, D. 1982. Resource Competition and Community
Structure. Princeton, New Jersey: Princeton University Press,.
Vandermeer, J., I. Granzow de la Cerda, D. Boucher, I.
Perfecto, and J. Ruiz. 2000. Hurricane disturbance
and tropical tree species diversity. Science 290: 788791.
Vitousek, P. M., and P. A. Matson. 1985. Disturbance,
nitrogen availability, and nitrogen losses in an intensively managed loblolly pine plantation. Ecology
66: 1360-1376.
Vitousek, P. M., and R. L. Sanford. 1986. Nutrient cycling in moist tropical forests. Annual Review of
Ecol. Syst. 17: 137-167.
Wijesinghe, D. K., E. A. John, S. Beurskens, and M. J.
Hutchings. 2001. Root system size and precision in
nutrient foraging: responses to spatial pattern of
nutrient supply in six herbaceous species. J. Ecol.
89: 972-983.
Yih, K., D. Boucher, J. Vandermeer, N. Zamora. 1991.
Recovery of the rainforest of southwestern Nicaragua after destruction by Hurricane Joan. Biotropica
23: 106-113.