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1.
Ecology ; 100(4): e02641, 2019 04.
Article in English | MEDLINE | ID: mdl-30712256

ABSTRACT

High rates of land conversion and land use change have vastly increased the proportion of secondary forest in the lowland tropics relative to mature forest. As secondary forests recover following abandonment, nitrogen (N) and phosphorus (P) must be present in sufficient quantities to sustain high rates of net primary production and to replenish the nutrients lost during land use prior to secondary forest establishment. Biogeochemical theory and results from individual studies suggest that N can recuperate during secondary forest recovery, especially relative to P. Here, we synthesized 23 metrics of N and P in soil and plants from 45 secondary forest chronosequences located in the wet tropics to empirically explore (1) whether there is a consistent change in nutrients and nutrient cycling processes during secondary succession in the biome; (2) which metrics of N and P in soil and plants recuperate most consistently; (3) if the recuperation of nutrients during succession approaches similar nutrient concentrations and fluxes as those in mature forest in ~100 yr following the initiation of succession; and (4) whether site characteristics, including disturbance history, climate, and soil order are significantly related to nutrient recuperation. During secondary forest succession, nine metrics of N and/or P cycling changed consistently and substantially. In most sites, N concentrations and fluxes in both plants and soil increased during secondary succession, and total P concentrations increased in surface soil. Changes in nutrient concentrations and nutrient cycling processes during secondary succession were similar whether mature forest was included or excluded from the analysis, indicating that nutrient recuperation in secondary forest leads to biogeochemical conditions that are similar to those of mature forest. Further, of the N and P metrics that recuperated, only soil total P and foliar δ15 N were strongly influenced by site characteristics like climate, soils, or disturbance history. Predictable nutrient recuperation across a diverse and productive ecosystem may support future forest growth and could provide a means to quantify successful restoration of ecosystem function in secondary tropical forest beyond biomass or species composition.


Subject(s)
Ecosystem , Trees , Forests , Nitrogen , Phosphorus , Soil , Tropical Climate
2.
Ecology ; 100(4): e02646, 2019 04.
Article in English | MEDLINE | ID: mdl-30714149

ABSTRACT

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.


Subject(s)
Soil , Trees , Carbon Dioxide , Nitrogen , Nitrogen Fixation , Nutrients
3.
Am Nat ; 192(5): 618-629, 2018 11.
Article in English | MEDLINE | ID: mdl-30332582

ABSTRACT

Symbiotic nitrogen fixation (SNF) makes atmospheric nitrogen biologically available and regulates carbon storage in many terrestrial ecosystems. Despite its global importance, estimates of SNF rates are highly uncertain, particularly in tropical forests where rates are assumed to be high. Here we provide a framework for evaluating the uncertainty of sample-based SNF estimates and discuss its implications for quantifying SNF and thus understanding of forest function. We apply this framework to field data sets from six lowland tropical rainforests (mature and secondary) in Brazil and Costa Rica. We use this data set to estimate parameters influencing SNF estimation error, notably the root nodule abundance and variation in SNF rates among soil cores containing root nodules. We then use simulations to gauge the relationship between sampling effort and SNF estimation accuracy for a combination of parameters. Field data illuminate a highly right-skewed lognormal distribution of SNF rates among soil cores containing root nodules that were rare and spanned five orders of magnitude. Consequently, simulations demonstrated that sample sizes of hundreds to even thousands of soil cores are needed to obtain estimates of SNF that are within, for example, a factor of 2 of the actual rate with 75% probability. This represents sample sizes that are larger than most studies to date. As a result of this previously undescribed uncertainty, we suggest that current estimates of SNF in tropical forests are not sufficiently constrained to elucidate forest stand-level controls of SNF, which hinders our understanding of the impact of SNF on tropical forest ecosystem processes.


Subject(s)
Nitrogen Fixation , Rainforest , Root Nodules, Plant/metabolism , Bacteria , Brazil , Computer Simulation , Costa Rica , Soil/chemistry , Symbiosis/physiology , Tropical Climate
4.
Ecology ; 99(9): 2080-2089, 2018 09.
Article in English | MEDLINE | ID: mdl-29931744

ABSTRACT

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 (N2 O), 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 N2 O 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 N2 O fluxes monthly for 1 yr and found that high canopy N species assemblages had on average three-fold higher total mean N2 O 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 N2 O 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 N2 O emissions in heterogeneous landscapes.


Subject(s)
Nitrogen/analysis , Nitrous Oxide , Ecosystem , Rainforest , Soil/chemistry
5.
New Phytol ; 214(4): 1506-1517, 2017 Jun.
Article in English | MEDLINE | ID: mdl-28262951

ABSTRACT

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.


Subject(s)
Phosphorus/metabolism , Rainforest , Soil/chemistry , Trees/physiology , Costa Rica , Fabaceae/physiology , Moraceae/physiology , Mycorrhizae , Nitrogen Fixation , Phosphoric Monoester Hydrolases/metabolism , Plant Roots/metabolism , Plant Roots/microbiology , Seedlings/physiology , Species Specificity , Tropical Climate
6.
Ecol Appl ; 26(8): 2449-2462, 2016 Dec.
Article in English | MEDLINE | ID: mdl-27874999

ABSTRACT

Distributions of foliar nutrients across forest canopies can give insight into their plant functional diversity and improve our understanding of biogeochemical cycling. We used airborne remote sensing and partial least squares regression to quantify canopy foliar nitrogen (foliar N) across ~164 km2 of wet lowland tropical forest in the Osa Peninsula, Costa Rica. We determined the relative influence of climate and topography on the observed patterns of foliar N using a gradient boosting model technique. At a local scale, where climate and substrate were constant, we explored the influence of slope position on foliar N by quantifying foliar N on remnant terraces, their adjacent slopes, and knife-edged ridges. In addition, we climbed and sampled 540 trees and analyzed foliar N in order to quantify the role of species identity (phylogeny) and environmental factors in predicting foliar N. Observed foliar N heterogeneity reflected environmental factors working at multiple spatial scales. Across the larger landscape, elevation and precipitation had the highest relative influence on predicting foliar N (30% and 24%), followed by soils (15%), site exposure (9%), compound topographic index (8%), substrate (6%), and landscape dissection (6%). Phylogeny explained ~75% of the variation in the field collected foliar N data, suggesting that phylogeny largely underpins the response to the environmental factors. Taken together, these data suggest that a large fraction of the variance in foliar N across the landscape is proximately driven by species composition, though ultimately this is likely a response to abiotic factors such as climate and topography. Future work should focus on the mechanisms and feedbacks involved, and how shifts in climate may translate to changes in forest function.


Subject(s)
Nitrogen , Plant Leaves , Costa Rica , Forests , Trees , Tropical Climate
7.
Ecol Lett ; 17(10): 1282-9, 2014 Oct.
Article in English | MEDLINE | ID: mdl-25070023

ABSTRACT

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.


Subject(s)
Forests , Mycorrhizae/physiology , Nitrogen Fixation , Phosphorus/metabolism , Plant Roots/enzymology , Soil/chemistry , Costa Rica , Phosphoric Monoester Hydrolases/metabolism , Plant Roots/microbiology , Rhizosphere , Tropical Climate
8.
Proc Natl Acad Sci U S A ; 111(22): 8101-6, 2014 Jun 03.
Article in English | MEDLINE | ID: mdl-24843146

ABSTRACT

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.


Subject(s)
Ecosystem , Fabaceae/metabolism , Nitrogen Cycle , Nitrogen Fixation , Trees , Agriculture , Biomass , Costa Rica , Environment , Human Activities , Humans , Models, Theoretical , Symbiosis , Tropical Climate
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