Tropical forests play a dominant role in the global carbon (C) cycle, and models predict increases in tropical net primary productivity (NPP) and C storage in response to rising atmospheric carbon ...dioxide (CO2) concentrations. The extent to which increasing CO2 will enhance NPP depends in part on the availability of nitrogen (N) and phosphorus (P) to support growth. Some tropical trees can potentially overcome nutrient limitation by acquiring N via symbiotic dinitrogen (N2) fixation, which may provide a benefit in acquiring P via investment in N-rich phosphatase enzymes or arbuscular mycorrhizal (AM) fungi. We conducted a seedling experiment to investigate the effects of elevated CO2 and soil nutrient availability on the growth of two N2-fixing and two non-N2-fixing tropical tree species. We hypothesized that under elevated CO2 and at low nutrient availability (i.e., low N and P), N2 fixers would have higher growth rates than non-N2 fixers because N2 fixers have a greater capacity to acquire both N and P. We also hypothesized that differences in growth rates between N2 fixers and non-N2 fixers would decline as nutrient availability increases because N2 fixers no longer have an advantage in nutrient acquisition. We found that the N2 fixers had higher growth rates than the non-N2 fixers under elevated CO2 and at low nutrient availability, and that the difference in growth rates between the N2 and non-N2 fixers declined as nutrient availability increased, irrespective of CO2. Overall, N2 fixation, root phosphatase activity, and AM colonization decreased with increasing nutrient availability, and increased under elevated CO2 at low nutrient availability. Further, AM colonization was positively related to the growth of the non-N2 fixers, whereas both N2 fixation and root phosphatase activity were positively related to the growth of the N2 fixers. Though our results indicate all four tree species have the capacity to up- or down-regulate nutrient acquisition to meet their stoichiometric demands, the greater capacity for the N2 fixers to acquire both N and P may enable them to overcome nutritional constraints to NPP under elevated CO2, with implications for the response of tropical forests to future environmental change.
Biological nitrogen fixation (BNF) is the largest natural source of exogenous nitrogen (N) to unmanaged ecosystems and also the primary baseline against which anthropogenic changes to the N cycle are ...measured. Rates of BNF in tropical rainforest are thought to be among the highest on Earth, but they are notoriously difficult to quantify and are based on little empirical data. We adapted a sampling strategy from community ecology to generate spatial estimates of symbiotic and free-living BNF in secondary and primary forest sites that span a typical range of tropical forest legume abundance. Although total BNF was higher in secondary than primary forest, overall rates were roughly five times lower than previous estimates for the tropical forest biome. We found strong correlations between symbiotic BNF and legume abundance, but we also show that spatially free-living BNF often exceeds symbiotic inputs. Our results suggest that BNF in tropical forest has been overestimated, and our data are consistent with a recent top-down estimate of global BNF that implied but did not measure low tropical BNF rates. Finally, comparing tropical BNF within the historical area of tropical rainforest with current anthropogenic N inputs indicates that humans have already at least doubled reactive N inputs to the tropical forest biome, a far greater change than previously thought. Because N inputs are increasing faster in the tropics than anywhere on Earth, both the proportion and the effects of human N enrichment are likely to grow in the future.
We hypothesized that dinitrogen (N2)- and non-N2-fixing tropical trees would have distinct phosphorus (P) acquisition strategies allowing them to exploit different P sources, reducing competition.
We ...measured root phosphatase activity and arbuscular mycorrhizal (AM) colonization among two N2- and two non-N2-fixing seedlings, and grew them alone and in competition with different inorganic and organic P forms to assess potential P partitioning.
We found an inverse relationship between root phosphatase activity and AM colonization in field-collected seedlings, indicative of a trade-off in P acquisition strategies. This correlated with the predominantly exploited P sources in the seedling experiment: the N2 fixer with high N2 fixation and root phosphatase activity grew best on organic P, whereas the poor N2 fixer and the two non-N2 fixers with high AM colonization grew best on inorganic P. When grown in competition, however, AM colonization, root phosphatase activity and N2 fixation increased in the N2 fixers, allowing them to outcompete the non-N2 fixers regardless of P source.
Our results indicate that some tropical trees have the capacity to partition soil P, but this does not eliminate interspecific competition. Rather, enhanced P and N acquisition strategies may increase the competitive ability of N2 fixers relative to non-N2 fixers.
Paradoxically, symbiotic dinitrogen (N₂) fixers are abundant in nitrogen (N)‐rich, phosphorus (P)‐poor lowland tropical rain forests. One hypothesis to explain this pattern states that N₂ fixers have ...an advantage in acquiring soil P by producing more N‐rich enzymes (phosphatases) that mineralise organic P than non‐N₂ fixers. We assessed soil and root phosphatase activity between fixers and non‐fixers in two lowland tropical rain forest sites, but also addressed the hypothesis that arbuscular mycorrhizal (AM) colonisation (another P acquisition strategy) is greater on fixers than non‐fixers. Root phosphatase activity and AM colonisation were higher for fixers than non‐fixers, and strong correlations between AM colonisation and N₂ fixation at both sites suggest that the N–P interactions mediated by fixers may generally apply across tropical forests. We suggest that phosphatase enzymes and AM fungi enhance the capacity of N₂ fixers to acquire soil P, thus contributing to their high abundance in tropical forests.
Grassland ecosystems invaded by exotic plant species often exhibit substantially higher above‐ground productivity and soil nitrogen (N) than the native communities they replace. These shifts are ...likely associated with altered microbial carbon (C) and N cycling, but we know surprisingly little about how these processes change with plant invasion.
Targeting four invasive plant species common in the Rocky Mountain West, we collected soils from invaded and adjacent uninvaded grassland field plots, as well as from an experimental garden. We used a laboratory incubation of soils with 13C‐ and 15N‐labelled substrates to examine how microbial C respiration, C assimilation and N cycling differed among plant communities. To assess how these rates corresponded with plant productivity and microbial communities, we measured above‐ground plant biomass and characterized bacterial and fungal communities using Illumina sequencing.
In the paired observational plots, soil microbial communities associated with invaders generally had higher respiration rates and lower growth rates than those associated with the native plant communities, leading to a lower microbial carbon‐use efficiency (CUE). Overall, soil substrate with a lower C:N was related to decreased CUE, and lower CUE was related to increased gross and net N mineralization. In turn, faster gross N mineralization was related to greater above‐ground biomass. These patterns coincided with significant differences in fungal communities, whereas bacterial communities varied by site. Invasive plants also altered microbial communities in the experimental plots, but this was not associated with shifts in microbial CUE, which was low overall.
Synthesis. Our results provide evidence that invasive plants alter bacterial and fungal communities. These shifts were not associated with changes in microbial CUE and, thus, the often‐assumed link between compositional and functional shifts was not apparent in this study. However, lower CUE was associated with elevated rates of N cycling and productivity, which, in low‐productivity systems, could help explain the increased growth and success of exotic plant invaders.
The invasive plants we studied in a Rocky Mountain semi‐arid grassland harboured soil microbial communities with a lower carbon‐use efficiency than their neighbouring native plant assemblages. The low CUE of invasive plants was associated with elevated rates of N cycling and productivity, which, in low‐productivity systems, could help to explain the increased growth and success of exotic plant invaders.
The mechanistic links between nitrogen (N) availability and investment in plant phosphorus (P) acquisition have important implications for plant growth, species distributions, and responses to CO2 ...fertilization under global change, especially in P‐poor tropical ecosystems. Currently, it is unclear whether investment in strategies that enhance plant P acquisition (arbuscular mycorrhizal, AM; colonization or root phosphatase activity, RPA) are determined primarily by phylogeny, or whether these strategies differ among N2‐fixing legumes and nonfixing plants as a result of differing N availability.
We hypothesized that plant N status, which can vary widely independent of N fixation, correlates with investment in P acquisition, because: (a) N and P concentrations scale in plant tissue indicative of coupled demand and (b) plants with more N may have more resources available to allocate to acquisition strategies.
We grew seedlings of eight tropical tree species from three families (including three N2‐fixing and one nonfixing legume) under greenhouse conditions in native forest soil for four months. Species represented almost the full range of foliar N observed in tropical trees.
Neither foliar N nor P concentrations correlated with investment in P acquisition. Across all species, we found an inverse relationship between investment in AM colonization and RPA, but this trade‐off was unrelated to foliar N or P and did not differ between functional types (i.e., N2 fixers vs. nonfixers).
Within legumes (family Fabaceae), two strategies were evident that were unrelated to fixation status. High‐fixing Inga and nonfixing Dialium displayed high foliar N and P concentrations and greater proportional investment in RPA versus AM, while lower fixing Ormosia species were characterized by lower foliar nutrient concentrations and proportionally more investment in AM.
Synthesis.Investment in P acquisition strategies in tropical trees is not dependent on foliar N or functional group, but instead may be controlled in part by resource trade‐offs. High diversity in nutrient strategies between related species cautions again the use of simple functional groupings to draw conclusions about nutrient acquisition in tropical trees.
Although nitrogen and phosphorus are stoichiometrically coupled in foliage, we found no evidence that investment in phosphorus‐acquisition mechanisms is related to either foliar nitrogen or to the presence of nitrogen fixation in tropical tree seedlings. Instead, species show trade‐offs between P acquisition mechanisms (arbuscular mycorrhizal colonization and root phosphatase enzymes), and display diverse nutrient strategies, even within plant families.
Tropical forests play a dominant role in the global carbon (C) cycle, and models predict increases in tropical net primary productivity (NPP) and C storage in response to rising atmospheric carbon ...dioxide (CO
) concentrations. The extent to which increasing CO
will enhance NPP depends in part on the availability of nitrogen (N) and phosphorus (P) to support growth. Some tropical trees can potentially overcome nutrient limitation by acquiring N via symbiotic dinitrogen (N
) fixation, which may provide a benefit in acquiring P via investment in N-rich phosphatase enzymes or arbuscular mycorrhizal (AM) fungi. We conducted a seedling experiment to investigate the effects of elevated CO
and soil nutrient availability on the growth of two N
-fixing and two non-N
-fixing tropical tree species. We hypothesized that under elevated CO
and at low nutrient availability (i.e., low N and P), N
fixers would have higher growth rates than non-N
fixers because N
fixers have a greater capacity to acquire both N and P. We also hypothesized that differences in growth rates between N
fixers and non-N
fixers would decline as nutrient availability increases because N
fixers no longer have an advantage in nutrient acquisition. We found that the N
fixers had higher growth rates than the non-N
fixers under elevated CO
and at low nutrient availability, and that the difference in growth rates between the N
and non-N
fixers declined as nutrient availability increased, irrespective of CO
. Overall, N
fixation, root phosphatase activity, and AM colonization decreased with increasing nutrient availability, and increased under elevated CO
at low nutrient availability. Further, AM colonization was positively related to the growth of the non-N
fixers, whereas both N
fixation and root phosphatase activity were positively related to the growth of the N
fixers. Though our results indicate all four tree species have the capacity to up- or down-regulate nutrient acquisition to meet their stoichiometric demands, the greater capacity for the N
fixers to acquire both N and P may enable them to overcome nutritional constraints to NPP under elevated CO
, with implications for the response of tropical forests to future environmental change.
The role of lowland tropical forest tree communities in shaping soil nutrient cycling has been challenging to elucidate in the face of high species diversity. Previously, we showed that differences ...in tree species composition and canopy foliar nitrogen (N) concentrations correlated with differences in soil N availability in a mature Costa Rican rainforest. Here, we investigate potential mechanisms explaining this correlation. We used imaging spectroscopy to identify study plots containing 10–20 canopy trees with either high or low mean canopy N relative to the landscape mean. Plots were restricted to an uplifted terrace with relatively uniform parent material and climate. In order to assess whether canopy and soil N could be linked by litterfall inputs, we tracked litter production in the plots and measured rates of litter decay and the carbon and N content of leaf litter and leaf litter leachate. We also compared the abundance of putative N fixing trees and rates of free-living N fixation as well as soil pH, texture, cation exchange capacity, and topographic curvature to assess whether biological N fixation and/or soil properties could account for differences in soil N that were, in turn, imprinted on the canopy. We found no evidence of differences in legume communities, free-living N fixation, or abiotic properties. However, soils beneath high canopy N assemblages received ~ 60% more N via leaf litterfall due to variability in litter N content between plot types. The correlation of N in canopy leaves, leaf litter, and soil suggests that, under similar abiotic conditions, litterfall-mediated feedbacks can help maintain soil N differences among tropical tree assemblages in this diverse tropical forest.
Tropical forests exhibit significant heterogeneity in plant functional and chemical traits that may contribute to spatial patterns of key soil biogeochemical processes, such as carbon storage and ...greenhouse gas emissions. Although tropical forests are the largest ecosystem source of nitrous oxide (N2O), drivers of spatial patterns within forests are poorly resolved. Here, we show that local variation in canopy foliar N, mapped by remote-sensing image spectroscopy, correlates with patterns of soil N2O emission from a lowland tropical rainforest. We identified ten 0.25 ha plots (assemblages of 40–70 individual trees) in which average remotely-sensed canopy N fell above or below the regional mean. The plots were located on a single minimally-dissected terrace (< 1 km²) where soil type, vegetation structure and climatic conditions were relatively constant. We measured N2O fluxes monthly for 1 yr and found that high canopy N species assemblages had on average three-fold higher total mean N2O fluxes than nearby lower canopy N areas. These differences are consistent with strong differences in litter stoichiometry, nitrification rates and soil nitrate concentrations. Canopy N status was also associated with microbial community characteristics: lower canopy N plots had two-fold greater soil fungal to bacterial ratios and a significantly lower abundance of ammonia-oxidizing archaea, although genes associated with denitrification (nirS, nirK, nosZ) showed no relationship with N2O flux. Overall, landscape emissions from this ecosystem are at the lowest end of the spectrum reported for tropical forests, consist with multiple metrics indicating that these highly productive forests retain N tightly and have low plant-available losses. These data point to connections between canopy and soil processes that have largely been overlooked as a driver of denitrification. Defining relationships between remotely-sensed plant traits and soil processes offers the chance to map these processes at large scales, potentially increasing our ability to predict N2O emissions in heterogeneous landscapes.
Nutrient availability varies substantially across lowland tropical forests and constrains their responses to global change. However, interactions among regional, landscape, and local controls of ...nutrient availability are poorly understood. In that context, we explored the effects of rainfall, topography, and canopy chemistry on nitrogen (N) cycling across the Osa Peninsula (Costa Rica). We sampled soils from catenas in regions receiving 3000 versus 5000 mm y⁻¹ rainfall. In both regions, we sampled catenas starting on narrow, knife-edged ridges, and in the less humid region we compared catenas starting on rapidly eroding knife-edged ridges to catenas with ridges consisting of slowly eroding terraces. On the stable terraces, we sampled soils from 0.25 ha plots with either high or low mean canopy N. In all sites, we measured metrics of long-(soil δ¹⁵N) and short-term (net nitrification, net N mineralization, and KCl-extractable N) N availability. Mean soil δ¹⁵N was elevated in the less humid region (3.8 ± 0.16 vs. 3.1 ± 0.14‰; P = 0.003). Within that region, mean δ¹⁵N was enriched by approximately 1‰ on stable terraces (5.3 ± 0.14‰) relative to nearby knife-edged ridges (4.0 ± 0.24‰; P < 0.001). Short-term N metrics did not vary with rainfall or topography (P > 0.05). By contrast, short-term soil N metrics differed under canopies with high versus low canopy N, but soil δ¹⁵N did not. These results illustrate the role of climate and topography as dominant drivers of long-term N cycling in the region, as well as the potential for canopy characteristics, which are likely determined by species composition in this system, to impose smallscale heterogeneity within those broader constraints. Overall, our work suggests the utility of a hierarchical framework for understanding how diverse drivers of nutrient status interact across space and time in tropical forests.
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