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Keywords:

  • arbuscular mycorrhizal (AM) fungi;
  • fine root mass;
  • fine root length;
  • soil nutrients;
  • tropical forest

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Supplementary material
  9. References
  10. Supporting Information
  • • 
    It is commonly hypothesized that stand-level fine root biomass increases as soil fertility decreases both within and among tropical forests, but few data exist to test this prediction across broad geographic scales. This study investigated the relationships among fine roots, arbuscular mycorrhizal (AM) fungi and soil nutrients in four lowland, neotropical rainforests.
  • • 
    Within each forest, samples were collected from plots that differed in fertility and above-ground biomass, and fine roots, AM hyphae and total soil nutrients were measured.
  • • 
    Among sites, total fine root mass varied by a factor of three, from 237 ± 19 g m−2 in Costa Rica to 800 ± 116 g m−2 in Brazil (0–40 cm depth). Both root mass and length were negatively correlated to soil nitrogen and phosphorus, but AM hyphae were not related to nutrients, root properties or above-ground biomass.
  • • 
    These results suggest that understanding how soil fertility affects fine roots is an additional factor that may improve the representation of root functions in global biogeochemical models or biome-wide averages of root properties in tropical forests.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Supplementary material
  9. References
  10. Supporting Information

Forest soils in the tropics encompass a large range of mineral nutrient availability, and above-ground primary productivity may be limited by atmospherically derived nutrients such as nitrogen (N) or rock-derived nutrients such as phosphorus (P) (Chadwick et al., 1999). Similarly, below-ground biomass including fine roots (≤ 2 mm diameter), which are critical for nutrient and water uptake, may be strongly influenced by soil nutrient availability. Plants respond to limited soil nutrients by increasing biomass allocation to fine roots, by altering root morphology, or increasing fine root lifespan (Bloom et al., 1985; Eissenstat & Yanai, 1997). The demonstrated plasticity in fine root properties (Reynolds & D’Antonio, 1996; Forde & Lorenzo, 2001; Hodge, 2004) leads to the prediction that stand-level fine root biomass will increase as soil fertility decreases both within (Gower, 1987) and among tropical forests (Leigh, 1999, p. 133; Maycock & Congdon, 2000), but few data exist to test this prediction across broad geographic scales. Similarly, plants are expected to maintain a larger standing crop of arbuscular mycorrhizal (AM) fungi where soil nutrients are limiting (Mosse, 1973; Read, 1991; Treseder, 2004). However, data on the abundance of arbuscular mycorrhizal (AM) fungi in tropical systems are scarce (Allen et al., 1995).

Because fine roots are a dynamic component of the carbon cycle and may affect how forests respond to global changes such as increased atmospheric carbon dioxide, rising temperatures and nitrogen deposition, there is much interest in measuring and modeling root properties at continental and global scales (Norby & Jackson, 2000). A number of reviews have examined global patterns in fine root biomass/length, dynamics, and total depth (Vogt et al., 1996; Cairns et al., 1997; Jackson et al., 1997; Gill & Jackson, 2000; Schenk & Jackson, 2002). These reviews often group data by the biome in which they were collected, which does not account for variations within biomes that may result from differences in soil fertility, texture, rainfall seasonality and gap disturbances (Gower, 1987; Sanford, 1989; Ostertag, 1998; Silver et al., 2000). Moreover, it can be difficult to draw generalizations from the literature because data come from studies that have used different definitions of fine roots and different methods for measuring fine root properties (Vogt et al., 1996). Understanding the patterns of fine root distributions and their fungal symbionts within and among tropical forests and whether they vary with soil fertility is an important step to improving biome-wide fine root budgets and biogeochemical models.

This study tested the relationships among stand-level fine root distributions, AM fungi and soil nutrients at a broad geographic scale in four well studied lowland, Neotropical rain forests: La Selva (Costa Rica), Barro Colorado Island (Panama), Cocha Cashu (Peru), and Km 41 near Manaus (Brazil). Although many studies have examined variation within the forests, none have used common methods to document the patterns of soil chemical properties among the four forests (but see Vitousek & Matson, 1988). At each of the four forests we measured the stand-level distributions of fine root mass and length in three plots that differed in below-ground resource availability and above-ground biomass. Arbuscular mycorrhizal fungal hyphae, which are the dominant mycorrhizae in tropical forests (Smith & Read, 1997), were measured in three of the forests. We predicted that fine root mass (FRM), fine root length density (FRL) and lengths of AM hyphae would be greater on infertile soils, both within and among forests. We further hypothesized that the availability of rock-derived nutrients (P and cations) would be more important in determining root properties than N because many studies suggest that N does not limit net primary productivity in the forests that we studied (Denslow et al., 1987; Chadwick et al., 1999). Tree species composition varies among the forests (Gentry, 1990), thus, any patterns we find may include both phylogenetic and ecological causes (Nicotra et al., 2002).

Materials and Methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Supplementary material
  9. References
  10. Supporting Information

Study sites

Fine roots and soils were sampled from mature forests at the La Selva Biological Station (Costa Rica: 10°26′ N, 83°59′ W), Barro Colorado Island (Panama: 9°09′ N, 79°51′ W), Cocha Cashu Biological Station in Manu National Park (Peru: 11°54′ S, 71°22′ W), and the Kilometer 41 field camp of the Biological Dynamics of Forest Fragmentation Project (Brazil: 2°30′ S, 60°0′ W). Throughout the text we abbreviate these sites as LS, BCI, CC and KM41, respectively. Mean annual temperature among the forests ranges from 24 to 27°C (Powers, 2004). Mean annual precipitation (MAP) and dry season lengths (defined as the number of months with rainfall < 100 mm) show greater differences and range from: LS MAP = 4000 mm and dry season = 0; BCI MAP = 2600 mm and dry season = 4; CC MAP = 2165 mm and dry season = 3; and KM41 MAP = 2650 mm and dry season = 0 (Laurance, 2001; Leigh, 1999, p. 46; Sanford et al., 1994). Even in tropical forests where average monthly precipitation exceeds 100 mm every month, there is usually some annual periodicity of rainfall. Both LS and BCI soils were sampled towards the end of the wet season (September through October 2001), CC was sampled at the end of the dry season (October 2001), and KM41 was sampled at the beginning of the wet season (November 2001).

There are large differences in soil properties among and within the forests which reflect variations in soil-forming factors (e.g. climate, parent material, topography and soil age) and the dominant soil-forming processes (e.g. in situ weathering, erosion, podzolization, etc.) (Chauvel et al., 1987; Riley, 1994; Sollins et al., 1994; Yavitt, 2000). Each site has at least two different soil orders (under US Soil Taxonomy), on which soil fertility presumably differs (Vitousek & Sanford, 1986). Detailed overviews of the sites can be found elsewhere (Powers, 2004).

Vegetation is classified as tropical wet or moist forest in all of the sites, and none of our plots have been disturbed by humans within the last 300 yr. The information on vegetation structure and composition that we have comes from concurrent studies in the same plots that we sampled (DeWalt & Chave, 2004; Harms et al., 2004; J. Chave, unpublished). Density of stems = 10 cm diameter at breast height (d.b.h) and above-ground biomass (AGBM) was higher in the South American forests (CC and KM41) compared with the Central American forests (LS and BCI) (Table 1). Species richness of trees ≥ 30 cm d.b.h. in six 1400 m2 plots within each forest was as follows: LS (23) < BCI (35) < CC (51) < KM41 (84) (J. Chave, unpublished). Of the 166 tree species identified in these plots, 30 are from the Leguminosae. These legumes are of note because they may support nitrogen-fixing bacteria that contribute total stocks of N in the forests. Abundance of individuals ≥ 30 cm d.b.h. from the legume genera reported to nodulate in Corby (1988) was highest at LS where Pentaclethra macroloba dominates forest composition (37 trees per 8400 m2), intermediate at KM41 (12 trees per 8400 m2), and low at CC (eight trees per 8400 m2) and BCI (two trees per 8400 m2).

Table 1.  Soil order and forest structure in plots from four Neotropical forests in Costa Rica, Panama, Peru and Brazil
ForestPlot numberSoil orderStem density ha−1 (= 10 cm d.b.h)aAbove-ground biomass, Mg ha−1 (= 10 cm d.b.h)aSmall sapling density (individual m−2)b (10–50 cm height)
  • Sites: LS, La Selva Biological Station, Costa Rica; BCI, Barro Colorado Island, Panama; CC, Cocha Cashu Biological Station, Manu National Park, Peru; KM41, Kilometer 41 field camp of the Biological Dynamics of Forest Fragmentation Project, Brazil.

  • a
  • b
LS 1Ultisol420138 0.9
 2Ultisol600264 1.3
 3Inceptisol460171 0.7
BCI 4Oxisol360210 6.0
 5Oxisol420131 6.8
 6Alfisol440 87 6.3
CC 7Oxisol70023415.9
 8Oxisol840261 3.7
 9Entisol500464 5.2
KM4110Spodosol740320 8.7
11Oxisol820248 4.5
12Oxisol600294 5.2

Field sampling

At each of the forests, we established three 10 × 50 m plots on different soil orders that we expected to vary in fertility based upon previous work by Vitousek and Sanford (1986). They categorized Inceptisols, Alfisols, and Entisols as fertile orders and Ultisols, Oxisols and Spodosols as infertile. At LS, BCI and CC, one plot was on the more fertile soil type (Alfisols, Entisols or Inceptisols) and two plots were on the less fertile soil type (Oxisols or Ultisols), which comprised a larger per cent of the total area of each field station (Table 1). At KM41, two plots were located on Oxisols and one plot was on a Spodosol. All plots were on level terrain in mature forests, avoiding treefall gaps.

Soil and root coring and processing

Each 50 × 10 m plot was subdivided into five 10 × 10 m subplots, and one sample point was placed at random within each subplot. At each sampling point, we excavated volumetric root samples from the mineral soil at four fixed depths (0–10, 10–20, 20–30 and 30–40 cm) for a total of 20 samples per plot. Several of the sample points at CC and KM41 had above-ground roots mats, which are highly efficient at retaining nutrients (Stark & Jordan, 1978). These roots were included in the samples of mineral soil from 0 to 10 cm. Although some tropical trees may have very deep roots (Nepstad et al., 1994), Schenk and Jackson (2002) have estimated that 50–95% of roots in tropical evergreen forests are found in the top 15–91 cm of mineral soil. Thus, our sampling depth (0–40 cm) includes a variable but large fraction of total fine roots.

For most of the sites, soil samples were extracted with a 9.6 × 2.0 cm rectangular turf grass sampler inserted into the soil at 10 cm increments. This method worked well at all sites except BCI, where high densities of coarse roots throughout upper soil profiles prevented sampling with the turf grass sampler at many points. Therefore, for some BCI samples, we used a punch tube soil probe (inserted into the soil in 10 cm increments). For these samples, we composited seven samples extracted from a c. 20 × 30 cm2 area. Estimates of fine roots made using both the methods were highly correlated (r2 > 0.97, n = 16). Therefore regression equations were used to convert the FRM and FRL values for BCI root samples extracted with the soil probe to ‘turf sampler values’, and these converted values are reported to allow for direct comparison with all other data.

In the field laboratories, soil clods were broken up, each sample was well mixed in a separate plastic bag and a root-free subsample was removed from each soil sample. The root-free soil subsamples were composited by depth interval within each plot, oven-dried at approx. 60°C, and analysed for soil chemical properties as described later. From each main sample, roots were separated from soil by washing in a 0.5 mm sieve. Root length (FRL) was determined on wet roots (≤ 2 mm diameter) using the line intercept method (Newman, 1966; Tennant, 1975). Because of time constraints, no effort was made to separate live roots from dead roots, although we estimate that < 15% of any sample consisted of dead roots (J. S. Powers, personal observation). At BCI, the most seasonal forest we sampled, dead fine roots are reported to be < 8% of total FRM, even during the dry season (Yavitt & Wright, 2001). Roots were oven-dried for > 24 h at c. 60–70°C, and then weighed (± 0.001 g) for FRM.

Mycorrhizal hyphae

Soils from LS, BCI and CC were exported to the USA for analyses of mycorrhizal hyphae and total nutrients. Lengths of AM hyphae were determined using a modified procedure from Sylvia (1992) described in detail in Treseder and Allen (2002). Briefly, soils were dispersed in sodium metaphosphate solution (39.5 g l−1), passed through a series of sieves and hyphae recovered on a 45 µm sieve. The hyphae were then collected on filters, which were examined at ×200 magnification using a Zeiss phase-contrast microscope (Carl Zeiss, Inc., Thornwood, NY, USA). Hyphae from AM fungi were distinguished from those of non-AM fungi by examining morphology. Arbuscular mycorrhizal hyphae lack septa, tend to branch angularly and have irregular walls (Bonfante-Fasolo, 1986). Nevertheless, we note that distinctions between AM and non-AM fungi can be challenging, and this difficulty may be a source of error in our estimates. A reticule was used to measure the length of each AM hypha encountered, and total lengths of AM hyphae were expressed as mm hyphae g−1 soil.

Soil chemical properties

Chemical properties of soils from LS, BCI and CC were analysed using common methods. Soil pH was measured in a 1 : 2.5 soil solution ratio of deionized water using a ‘Corning pH 20’ meter (Corning Electrochemistry Products, Woburn, MA, USA). We compared two measurements of P and cations: total and extractable concentrations. For total nutrients, soils were digested with concentrated HNO3 in a microwave and total P and nutrient base cations – calcium (Ca), magnesium (Mg), potassium (K) and sodium (Na) – were quantified via inductively coupled plasma electron spectroscopy at the Research Analytical Laboratory at the University of Minnesota. ‘Labile’ nutrients were extracted in the Mehlich III dilute acid solution and measured as above (Mehlich, 1984).

Total carbon (C) and total N were measured on finely ground soil samples following dry combustion on a Carlo Erba Elemental Analyser (Thermo Electron Corp., Milan, Italy). All nutrient concentrations are reported on an oven-dry weight basis. Because it was not possible to export soils from Brazil, samples from KM41 were analysed using standard protocols for pH in water, total C and N at EMBRAPA in Manaus (Fearnside & Filho, 2001).

Statistical analyses

We calculated pairwise Pearson correlation coefficients to explore correlations among soil chemical properties (pH, total P, sum of base cations, percentage C (%C), percentage N (%N)), fine roots (length and mass), AM hyphae length and above-ground biomass using plots as experimental units. Stepwise multiple regression was used relate FRM and FRL (from 0 to 10 cm depth) to percentage N, total P and cations, using AGBM as a covariate. Residual plots confirmed that the response variables did not require data transformations. All analyses were performed with s-plus 2000 (Mathsoft, Inc., Seattle, WA, USA).

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Supplementary material
  9. References
  10. Supporting Information

Patterns of soil nutrients

As expected, Mehlich-III extractable P and cations were a smaller fraction of total nutrients (Fig. 1). However, extractable P was not well correlated with total P (Fig. 1a), although cations were positively related to one another (Fig. 1b). The poor correlation between extractable and total P may be an artifact of soil drying. Therefore, we made the assumption that total nutrient pools provide a better time-integrated index of relative nutrient availability among sites than extractable pools, and do not discuss extractable nutrients further.

image

Figure 1. Relationships between total and Mehlich-III extractable soil P (a) and soil cations (b). Triangles, LS (La Selva Biological Station, Costa Rica); circles, BCI (Barro Colorado Island, Panama); diamonds, CC (Cocha Cashu Biological Station, Manu National Park, Peru).

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There were large differences in total nutrients, pH and %C among sites (Table 2). In particular, base cation concentrations were extremely variable, ranging from 2- to 76-fold differences among plots for the 0–10 cm sampling depth. Not surprisingly, among sites both cations and pH were significantly correlated, as were total C and N (Table 3). Total P was positively correlated with total C and N, with Pearson correlation coefficients of 0.77 (P < 0.012) and 0.78 (P < 0.012), respectively (Table 3). The soils from La Selva are comparatively high in P, but low in total base cations. By contrast, soils from BCI appear to be high in Ca but low in P, a pattern also found in the nearby Gigante Peninsula (Cavelier, 1992). Soils at CC showed a different pattern. The alluvial Entisol formed from recently deposited sediment from the Andes had intermediate P, very high base cation concentrations and near-neutral pH, in contrast to the extremely weathered, terra firme Oxisols. It is interesting to note that the soils from Brazil had higher %C and %N than the Peruvian Oxisols (Table 2). See the supplementary material Tables S1–S4 for soil chemical data from other soil depths.

Table 2.  Soil chemical properties in plots on different soil orders in four neotropical forests
ForestPlot numberpHwaterC (%)N (%)P (µg g−1)Ca (cmol (+) kg−1)K (cmol (+) kg−1)Mg (cmol (+) kg−1)Na (cmol (+) kg−1)
  1. Sites: LS, La Selva Biological Station, Costa Rica; BCI, Barro Colorado Island, Panama; CC, Cocha Cashu Biological Station, Manu National Park, Peru; KM41, Kilometer 41 field camp of the Biological Dynamics of Forest Fragmentation Project, Brazil.

  2. All data are for the 0–10 cm depth intervals. Nutrient data are total concentrations.

LS 14.05.770.49 873 0.961.30 7.760.43
 24.14.700.421129 1.190.31 2.040.11
 33.94.770.451552 1.661.31 5.340.28
BCI 45.64.250.42 93110.290.59 3.500.22
 55.33.930.401025 6.250.58 5.860.15
 65.53.650.36 36123.590.5922.160.30
CC 74.50.830.09 221 1.391.90 2.120.06
 83.80.300.03 167 0.535.31 5.090.40
 96.74.450.43 77740.358.3632.970.35
KM41104.31.940.11     
114.13.920.26     
124.43.680.24     
Table 3.  Pearson's correlation coefficients between soil chemical variables, fine root mass (FRM), fine root length (FRL), arbuscular mycorrhizal (AM) hyphae and above-ground biomass (AGBM) in four neotropical forests
 CationspH%C%NFRMFRLAM hyphaeAGBM
  1. P-values are in parentheses. Soil and root properties were measured in 0–10 cm soil depth. Degrees of freedom are 7 for comparisons involving hyphae, cations and/or P, and 10 otherwise. Correlations with P-values < 0.05 are in bold type.

Total P−0.17 (0.65)−0.08 (0.83)0.77 (0.014)0.78 (0.012)−0.77 (0.015)−0.77 (0.014)−0.25 (0.52)−0.08 (0.85)
Cations 0.83 (0.006)0.17 (0.66)0.22 (0.58) 0.21 (0.59)−0.08 (0.85) 0.30 (0.43) 0.54 (0.13)
pH  0.20 (0.54)0.35 (0.27)−0.23 (0.48)−0.18 (0.58) 0.11 (0.78) 0.29 (0.36)
%C   0.95 (< 0.0001)−0.35 (0.27)−0.79 (0.003) 0.17 (0.66)−0.18 (0.57)
%N    −0.57 (0.054)−0.85 (0.0004) 0.12 (0.75)−0.26 (0.42)
FRM     0.71 (0.010)−0.03 (0.93) 0.38 (0.23)
FRL      −0.22 (0.57) 0.35 (0.26)
AM hyphae        0.20 (0.60)

Fine roots and AM hyphae in relation to soil nutrients

Average fine root mass and fine root length density declined consistently with depth in the soil profile at all sites (Fig. 2), but did not reach zero. This suggests that fine roots exist in all forests below 40 cm depth, but also that our surface sampling of roots stocks is a relatively constant proportion of total roots in each plot, allowing for comparisons among sites. There was over a threefold variation in cumulative FRM (g m−2) in the top 40 cm of soil among sites (± 1 SE, n = 3): LS = 237 ± 19, BCI = 278 ± 20, CC = 497 ± 45 and KM41 = 800 ± 116. As expected, FRM and FRL were positively correlated to one another, but these estimates of surface root biomass (0–10 cm) were not correlated with above-ground biomass (Table 3). Both FRM and FRL were strongly, negatively related to total soil P and %N (Table 3, Fig. 3). However, the strength of these correlations differed for root mass and length. The FRM was better correlated to soil P than %N (Pearson's correlation coefficient of −0.77 vs −0.57, respectively). By contrast, FRL was better correlated to soil N (Pearson's correlation coefficient = −0.85) than soil P (−0.77). Multiple regression analyses did not include the sites from Brazil because of the lack of data for cations and P. In this restricted data set, %N was the only variable that explained variation in FRM (F1,7 = 25.19, r2 = 0.78, P = 0.002) and FRL (F1,7 = 35.37, r2 = 0.83, P = 0.0006); cations, P and AGBM were not retained in the regression models.

image

Figure 2. (a) Average fine root mass, and (b) fine root length density by depth in four Neotropical forests (error bars are 1 SE of the mean), n = 15 per site and depth. Open columns, La Selva Biological Station, Costa Rica; tinted columns, Barro Colorado Island, Panama; closed columns, Cocha Cashu Biological Station, Manu National Park, Peru; hatched columns, Kilometer 41 field camp of the Biological Dynamics of Forest Fragmentation Project, Brazil.

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image

Figure 3. Fine root mass and fine root length density (0–10 cm) in relation to total soil nitrogen (N) (a,b) and total phosphorus (P) (c,d). Triangles, LS (La Selva Biological Station, Costa Rica); circles, Barro Colorado Island, Panama; diamonds, Cocha Cashu Biological Station, Manu National Park, Peru; squares, Kilometer 41 field camp of the Biological Dynamics of Forest Fragmentation Project, Brazil.

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Mean AM fungal hyphae lengths (0–10 cm) were highly variable within each forest: LS = 156 ± 62, BCI = 149 ± 73, and CC = 153 ± 67 (mm g−1 soil ± 1 SE, n = 3 plots per forest). The AM hyphal lengths were generally higher in the upper soil layers (see the supplementary material Tables S1, S2 and S3), and were lowest at BCI in soil depths from 10 to 40 cm. There were no significant correlations between AM hyphae lengths and soil chemical properties, root traits or AGBM (Table 3).

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Supplementary material
  9. References
  10. Supporting Information

From Central America to Central Amazonia, we found a threefold range of variation in fine root stocks in our single sampling period and a strong negative correlation between fine roots and soil nitrogen and phosphorous concentrations. We found little evidence, however, for either fine roots or soil nutrients to be correlated with AGBM or AM fungal hyphae. The large interforest variation and relationship between roots and soil nutrients have important implications for understanding the controls over fine roots, for estimating below-ground carbon distribution in tropical soils and for predicting the consequences of environmental changes on root stocks and dynamics.

Jackson et al. (1997) compiled a global database of fine root biomass for different biomes, including 12 observations for tropical evergreen forests. Our values of FRM bracket Jackson's tropical evergreen forest average of 570 ± 69 (SEM) g m−2 FRM in the top 30 cm soil, but show considerably more variability. Some of this variability is negatively correlated with variation in soil nutrient concentrations (Fig. 3). These results are consistent with other tropical and temperate studies of FRM along natural fertility gradients (Gower, 1987; Ostertag, 1998; Maycock & Congdon, 2000) and under fertilization (Gower & Vitousek, 1989).

The four forests differ clearly with respect to soil nutrients, however, there are other important differences in climate and species composition among sites that may also affect root properties. Although our data do not allow us to partition the variation in root stocks among forests into these components, it is interesting to note that LS and BCI vary greatly in mean annual precipitation and dry season length, but have relatively fewer differences in soil nutrients (Fig. 3). They also stand out as the forests with the lowest root stocks. By contrast, LS and KM41 are both relatively aseasonal (both have no months with rainfall < 10 cm), but have large differences in total nutrients and a threefold difference in fine root stocks. Taken together these pairwise comparisons suggest a large influence of soil nutrients on root stocks in these forests.

We found several unexpected results when examining the correlations between root traits and individual nutrients. First, total soil N and P were positively correlated with one another, but not with total nutrient cations. Although both N and P change over the course of soil development, they are not expected to covary, as they have different ultimate sources and biogeochemical controls (Walker & Syers, 1976). Second, soil N was as good a predictor of root traits as P. While total soil N may not be the best measure of N availability, there is direct evidence that N availability declines from La Selva soils to those near Manaus, Brazil (Vitousek & Matson, 1988). Because many tropical forests are located on highly weathered landforms, it is often assumed that rock-derived nutrients such as P and Ca are more important controls on above-ground primary productivity than N. Our results provide strong support that N is a key control on fine root distributions in tropical rain forests across large spatial scales and underscore that there remains much to be learned about the relationships between soil nutrients and ecosystem processes in tropical forests.

The negative relationship between soil nutrients and roots does not appear to reflect differences in investment to AM fungi; we found no evidence that AM hyphal lengths were correlated with either soil nutrients or root abundance. In addition, standing stocks were generally low compared with those of other tropical forests (Treseder & Allen, 2002), grasslands (Tisdall & Oades, 1979; McNaughton & Oesterheld, 1990), and greenhouse experiments (reviewed in Smith & Read, 1997), which typically contain one or more meters of hyphae per gram soil. In our study sites, plants may rely primarily on roots for nutrient uptake and might not cultivate AM fungi in response to nutrient limitation. Fungal symbionts in these systems may confer alternative benefits such as tolerance to high levels of aluminum (Lux & Cumming, 2001). The reduction in AM hyphal length at depths below 10 cm is consistent with patterns observed in other field studies (Cooke et al., 1993; Brown & Bledsoe, 1996; Ingleby et al., 1997). In our sites, the decline may be related to the reduction in root biomass with depth.

Many studies in other tropical forests have reported that both fine root stocks and production are higher during the wet season (Yavitt & Wright, 2001; Kummerow et al., 1990; Roy & Singh, 1995). A major limitation of our study is that we sampled only a single period because of logistical constraints. It is possible that our results are influenced by differences in the season in which we collected our data. However, seasonal differences in root production and decomposition at these sites would tend to minimize the differences in root stocks among these forests, i.e. the forests with lowest root stocks, LS and BCI, were sampled during the wet season when root stocks should be highest, while the forests with highest roots stocks, CC and KM41 were sampled at the end of the dry season and the beginning of the wet season, respectively, when root stocks should be lower.

In conclusion, our broad geographic sampling of fine roots, soil nutrients and AM hyphae in evergreen tropical forests revealed strong correlations between fine roots and soil N and P, but no patterns for AM hyphae. These intriguing results lead to further hypotheses about which nutrients are important for root processes in lowland tropical forests, the degree to which root stocks are uncoupled from above-ground biomass, the possibility that above- and below-ground plant process may be limited by different nutrients, and controls on the abundance of fungal symbionts in these forests. Together, these results suggest that understanding how soil fertility affects fine roots is an additional factor that may help to improve the representation of root functions in global biogeochemical models or biome-wide averages of root properties in tropical forests.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Supplementary material
  9. References
  10. Supporting Information

The data for this study were collected during a 10-wk course, ‘Comparative Neotropical Ecology’, run by the Organization for Tropical Studies and the Smithsonian Tropical Research Institute and funded by the Mellon Foundation. The OTS staff helped make this project possible. We thank Saara DeWalt and Jerome Chave for forest structure and composition data. Peter Groffman, Tom Gower, Peter Tiffin, Helene Muller-Landau, Saara DeWalt, Horacio Paz, Ken Feeley, Jeff Klemens and three anonymous reviewers provided many helpful comments on earlier drafts of the manuscript. J.S.P. thanks all of the course participants for interesting discussions and support. We also thank Carmen and Ken Feeley for helping to export soils from Peru. This work was made possible through funding from the Graduate Women in Science to J.S.P and the Mellon Foundation to M.T.L.

Supplementary material

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Supplementary material
  9. References
  10. Supporting Information

The following material is available as supplementary material at http://www.blackwellpublishing.com/products/journals/suppmat/NPH/NPH1279/NPH1279sm.htm

Table S1 Total soil nutrients, fine root mass (FRM), fine root length (FRL) and arbuscular mycorrhizal (AM) fungal hyphae by depth from three plots at La Selva, Costa Rica.

Table S2 Total soil nutrients, fine root mass (FRM), fine root length (FRL) and arbuscular mycorrhizal (AM) fungal hyphae by depth from three plots at Barro Colorado Island, Panama.

Table S3 Total soil nutrients, fine root mass (FRM), fine root length (FRL) and arbuscular mycorrhizal (AM) fungal hyphae by depth from three plots at Cocha Cashu, Peru.

Table S4 Total soil nutrients, fine root mass (FRM) and fine root length (FRL) by depth from three plots at KM41, Brazil.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Supplementary material
  9. References
  10. Supporting Information
  • Allen EB, Allen MF, Helm DJ, Trappe JM, Molina R, Rincon E. 1995. Patterns and regulation of mycorrhizal plant and fungal diversity. Plant and Soil 170: 4762.
  • Bloom AJ, Chapin FS, Mooney HA. 1985. Resource limitation in plants – an economic analogy. Annual Review of Ecology and Systematics 16: 363392.
  • Bonfante-Fasolo P. 1986. Anatomy and morphology of VA mycorrhizae. In: PowellC, BagyarajD, eds. VA mycorrhiza. Boca Raton, FL, USA: CRC Press, 233.
  • Brown AM, Bledsoe C. 1996. Spatial and temporal dynamics of mycorrhizas in Jaumea carnosa, a tidal saltmarsh halophyte. Journal of Ecology 84: 703715.
  • Cairns MA, Brown S, Helmer EH, Baumgardner GA. 1997. Root biomass allocation in the world's upland forests. Oecologia 111: 111.
  • Cavelier J. 1992. Fine-root biomass and soil properties in a semideciduous and a lower montane rain forest in Panama. Plant and Soil 142: 187201.
  • Chadwick OA, Derry LA, Vitousek PM, Huebert BJ, Hedin LO. 1999. Changing sources of nutrients during four million years of ecosystem development. Nature 397: 491497.
  • Chauvel A, Lucas Y, Boulet R. 1987. On the genesis of the soil mantle of the region of Manaus, Central Amazonia, Brazil. Experientia 43: 234240.
  • Cooke JC, Butler RH, Madole G. 1993. Some observations on the vertical distribution of vesicular arbuscular mycorrhizae in roots of salt marsh grasses growing in saturated soils. Mycologia 85: 547550.
  • Corby HDL. 1988. Types of rhizobial nodules and their distribution among the Leguminosae. Kirkia 13: 53123.
  • Denslow JS, Vitousek PM, Schultz JC. 1987. Bioassays of nutrient limitation in a tropical rain forest soil. Oecologia 74: 370376.
  • DeWalt SJ, Chave J. 2004. Structure and biomass of four lowland Neotropical forests. Biotropica 36: 719.
  • Eissenstat DM, Yanai RD. 1997. The ecology of root lifespan. Advances in Ecological Research 27: 260.
  • Fearnside PM, Filho NL. 2001. Soil and development in Amazonia: lessons from the Biological Dynamics of Forest Fragmentation Project. In: BierregaardRO, GasconC, LovejoyTE, De SantosAA, eds. Lessons from Amazonia: the ecology and conservation of a fragmented forest. New Haven, MA, USA: Yale University Press, 291312.
  • Forde B, Lorenzo H. 2001. The nutritional control of root development. Plant and Soil 232: 5168.
  • Gentry AH, ed. 1990. Four neotropical rainforests. New Haven, MA, USA: Yale University Press.
  • Gill R, Jackson RB. 2000. Global patterns of root turnover for terrestrial ecosystems. New Phytologist 147: 1331.
  • Gower ST. 1987. Relations between mineral nutrient availability and fine root biomass in two Costa Rican tropical wet forests: a hypothesis. Biotropica 19: 171175.
  • Gower ST, Vitousek PM. 1989. Effects of nutrient amendment on fine root biomass in a primary successional forest in Hawai’i. Oecologia 81: 566568.
  • Harms KE, Powers JS, Montgomery RA. 2004. Variation in small sapling density, understory cover and resource availability in four Neotropical forests. Biotropica 36: 4051.
  • Hodge A. 2004. Tansley Review: The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytologist 162: 924.
  • Ingleby K, Diagne O, Deans JD, Lindley DK, Neyra M, Ducousso M. 1997. Distribution of roots, arbuscular mycorrhizal colonisation and spores around fast-growing tree species in Senegal. Forest Ecology and Management 90: 1927.
  • Jackson RB, Mooney HA, Schultze E-D. 1997. A global budget for fine root biomass, surface area, and nutrient concentrations. Proceedings of the National Academy of Sciences of the USA 94: 73627366.
  • Kummerow J, Castillanos J, Maas M, Lariguaderie A. 1990. Production of fine roots and the seasonality of their growth in a Mexican deciduous dry forest. Vegetatio 90: 7380.
  • Laurance WF. 2001. The hyper-diverse flora of the Central Amazon: an overview. In: BierregaardROJr, GasconC, LovejoyTE, MesquitaR, eds. Lessons from Amazonia: the ecology and conservation of a fragmented forest. New Haven, MA, USA: Yale University Press, 4753.
  • Leigh EG Jr . 1999. Tropical forest ecology: a view from Barro Colorado Island. New York, NY, USA: Oxford University Press.
  • Lux HB, Cumming JR. 2001. Mycorrhizae confer aluminum resistance to tulip-poplar seedlings. Canadian Journal of Forest Research 31: 694702.
  • Maycock CR, Congdon RA. 2000. Fine root biomass and soil N and P in North Queensland rain forests. Biotropica 32: 185190.
  • McNaughton SJ, Oesterheld M. 1990. Extramatrical mycorrhizal abundance and grass nutrition in a tropical grazing ecosystem, the Serengeti National Park, Tanzania. Oikos 59: 9296.
  • Mehlich A. 1984. Mehlich 3 soil test extractant: a modification of the Melich 2 extractant. Communications in Soil and Plant Analysis 15: 14091416.
  • Mosse B. 1973. Plant growth responses to vesicular–arbuscular mycorrhizae. IV. In soil given additional phosphate. New Phytologist 72: 127136.
  • Nepstad DC, De Carvalho CR, Davidson EA, Jipp PH, Lefebvre PA, Negreiros GH, Da Silva ED, Stone TA, Trumbore SE, Vieira S. 1994. The role of deep roots in the hydrological and carbon cycles of Amazonian forests and pastures. Nature 372: 666669.
  • Newman EI. 1966. A method of estimating the total length of root in a sample. Journal of Of Applied Ecology 3: 139145.
  • Nicotra AB, Babicka N, Westoby M. 2002. Seedling root anatomy and morphology: an examination of ecological differentiation with rainfall using phylogenetically independent contrasts. Oecologia 130: 136145.
  • Norby RJ, Jackson RB. 2000. Root dynamics and global change: seeking an ecosystem perspective. New Phytologist 147: 312.
  • Ostertag R. 1998. Belowground effects of canopy gaps in a tropical wet forest. Ecology 79: 12941304.
  • Powers JS. 2004. New perspectives in comparative ecology of Neotropical rain forests: reflections on past, present and future. Biotropica 36: 15.
  • Read DJ. 1991. Mycorrhizas in ecosystems – Nature's response to the ‘Law of the minimum’. In: HawksworthDL, ed. Frontiers in Mycology. Regensburg, Germany: CAB International, 101130.
  • Reynolds HL, D’Antonio C. 1996. The ecological significance of plasticity in root weight ratio in response to nitrogen. Plant and Soil 185: 7597.
  • Riley MP. 1994. Soil chemical changes accompanying a primary riparian succession in Manu National Park, Madre de Dios, Peru. Master's Thesis. Durham, NC, USA: Duke University.
  • Roy S, Singh JS. 1995. Seasonal and spatial dynamics of plant-available N and P pools and N-mineralization in relation to fine roots in a dry tropical forest. Soil Biology and Biochemistry 27: 3340.
  • Sanford RL Jr . 1989. Fine root biomass under a tropical forest light gap opening in Costa Rica. Journal of Tropical Ecology 5: 251256.
  • Sanford RL Jr, Paaby P, Luvall JC, Phillips E. 1994. Climate, geomorphology, and aquatic systems. In: McDadeL, BawaK, HespenheideH, HartshornGS, eds. La Selva: ecology and natural history of a neotropical rain forest. Chicago, IL, USA/London, UK: University of Chicago Press, 1933.
  • Schenk HJ, Jackson RB. 2002. The global biogeography of roots. Ecological Monographs 72: 311328.
  • Silver WL, Neff J, McGroddy M, Veldkamp E, Keller M, Cosme R. 2000. Effects of soil texture on belowground carbon and nutrient storage in a lowland Amazonian forest ecosystem. Ecosystems 3: 193209.
  • Smith SE, Read DJ. 1997. Mycorrhizal symbiosis, 2nd edn. San Diego, CA, USA: Academic Press.
  • Sollins P, Sancho MF, Mata Ch R, Sanford RL Jr . 1994. Soils and soil process research. In: McDadeL, BawaK, HespenheideH, HartshornGS, eds. La Selva: ecology and natural history of a neotropical rain forest. Chicago, IL, USA/London, UK: University of Chicago Press, 3453.
  • Stark NM, Jordan CF. 1978. Nutrient retention by the root mat of an Amazonian rain forest. Ecology 59: 434437.
  • Sylvia DM. 1992. Quantification of external hyphae of vesicular–arbuscular mycorrhizal fungi. In: NorrisJR, ReadD, VarmaAK, eds. Techniques for mycorrhizal research. London, UK: Academic Press, 513525.
  • Tennant D. 1975. A test of a modified line intercept method of estimating root length. Journal of Ecology 63: 9951001.
  • Tisdall JM, Oades JM. 1979. Stabilization of soil aggregates by the root systems of ryegrass. Australian Journal of Soil Research 17: 429441.
  • Treseder KK. 2004. A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytologist 164: 347355.
  • Treseder KK, Allen MF. 2002. Direct N and P limitation of arbuscular mycorrhizal fungi: a model and field test. New Phytologist 155: 507515.
  • Vitousek PM, Matson PA. 1988. Nitrogen transformations in a range of tropical forest soils. Soil Biology and Biochemistry 20: 361367.
  • Vitousek PM, Sanford RL, Jr. 1986. Nutrient cycling in moist tropical forests. Annals of Review of Evolution Systematic 17: 137167.
  • Vogt KA, Vogt DJ, Palmiotto PA, Boon P, O'Hara J, Asbjornsen H. 1996. Review of root dynamics in forest ecosystems grouped by climate, climatic forest type and species. Plant and Soil 187: 159219.
  • Walker TW, Syers JK. 1976. The fate of phosphorus during pedogenesis. Geoderma 15: 119.
  • Yavitt JB. 2000. Nutrient dynamics of soil derived from different parent material on Barro Colorado Island, Panama. Biotropica 32: 198207.
  • Yavitt JB, Wright SJ. 2001. Drought and irrigation effects on fine root dynamics in a tropical moist forest, Panama. Biotropica 33: 421434.

Supporting Information

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Supplementary material
  9. References
  10. Supporting Information

Table S1. Total soil nutrients, fine root mass (FRM), fine root length (FRL) and arbuscular mycorrhizal (AM) fungal hyphae by depth from three plots at La Selva, Costa Rica. Table S2. Total soil nutrients, fine root mass (FRM), fine root length (FRL) and arbuscular mycorrhizal (AM) fungal hyphae by depth from three plots at Barro Colorado Island, Panama. Table S3. Total soil nutrients, fine root mass (FRM), fine root length (FRL) and arbuscular mycorrhizal (AM) fungal hyphae by depth from three plots at Cocha Cashu, Peru. Table S4. Total soil nutrients, fine root mass (FRM) and fine root length (FRL) by depth from three plots at KM41, Brazil.

FilenameFormatSizeDescription
NPH_1279_sm_tableS1.doc44KSupporting info item
NPH_1279_sm_tableS2.doc44KSupporting info item
NPH_1279_sm_tableS3.doc44KSupporting info item
NPH_1279_sm_tableS4.doc39KSupporting info item