Vulnerability and resistance in the spatial heterogeneity of soil microbial communities under resource additions.

Spatial heterogeneity in composition and function enables ecosystems to supply diverse services. For soil microbes and the ecosystem functions they catalyze, whether such heterogeneity can be maintained in the face of altered resource inputs is uncertain. In a 50-ha northern California grassland with a mosaic of plant communities generated by different soil types, we tested how spatial variability in microbial composition and function changed in response to nutrient and water addition. Fungal composition lost some of its spatial variability in response to nutrient addition, driven by decreases in mutualistic fungi and increases in antagonistic fungi that were strongest on the least fertile soils, where mutualists were initially most frequent and antagonists initially least frequent. Bacterial and archaeal community composition showed little change in their spatial variability with resource addition. Microbial functions related to nitrogen cycling showed increased spatial variability under nutrient, and sometimes water, additions, driven in part by accelerated nitrification on the initially more-fertile soils. Under anthropogenic changes such as eutrophication and altered rainfall, these findings illustrate the potential for significant changes in ecosystem-level spatial heterogeneity of microbial functions and communities.

A New Framework for Evaluating Estimates of Symbiotic Nitrogen Fixation in Forests.

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.

Plant-soil feedbacks on free-living nitrogen fixation over geological time.

Free-living heterotrophic nitrogen fixation (FNF) is a widespread nitrogen input pathway in terrestrial ecosystems. However, questions remain over the relative influence of co-occurring controls on patterns of heterotrophic FNF activity, especially across generalized stages of primary succession, from biomass accumulation to retrogressive phases. Here, we experimentally test two alternative hypotheses regarding FNF rates during ecosystem development: (H1) site (i.e., changes in soil fertility during succession) is the primary driver of leaf-litter FNF rates, vs. (H2) leaf-litter chemistry is the primary determinant of FNF activity across a broad range of ecosystem conditions. We evaluated these hypotheses across a well-studied soil chronosequence in California (i.e., the Ecological Staircase), which spans ~1 million years of ecosystem development and displays extreme ranges in plant-soil nutrient conditions, culminating in the nutrient depleted and stunted Pygmy forest. Across this successional gradient, we implemented a reciprocal leaf-litter transplant and a common garden litter bag decomposition experiment with senesced needles of Pinus muricata. Our results support H1: rates of FNF were similar for all leaf-litter types decomposed at the same site regardless of initial leaf-litter C and nutrient contents. FNF rates sharply declined from the maximal to retrogressive stage of succession. Trends in P dynamics during decomposition suggest an important role of P in regulating FNF. For example, P. muricata litter collected from the infertile Pygmy site displayed substantially higher FNF rates when decomposed at the fertile site, in part by immobilizing significant quantities of P from the soil at the fertile site. Conversely, P. muricata litter collected from the fertile site decomposed more slowly at the Pygmy site, with concomitant declines in FNF rates that matched those of Pygmy site litter decomposed in situ. These results are consistent with the idea that, over millennia, long-term declines in P availability feedback to constrain FNF rates, in part explaining the emergence of extremely nutrient-poor and retrograded ecosystems.

Nitrogen cycling during secondary succession in Atlantic Forest of Bahia, Brazil.

Carbon accumulation in tropical secondary forests may be limited in part by nitrogen (N) availability, but changes in N during tropical forest succession have rarely been quantified. We explored N cycle dynamics across a chronosequence of secondary tropical forests in the Mata Atlântica of Bahia, Brazil in order to understand how quickly the N cycle recuperates. We hypothesized that N fixation would decline over the course of succession as N availability and N gaseous losses increased. We measured N fixation, KCl-extractable N, net mineralization and nitrification, resin-strip sorbed N, gaseous N emissions and the soil δ15N in stands that were 20, 35, 50, and > 50 years old. Contrary to our initial hypothesis, we found no significant differences between stand ages in any measured variable. Our findings suggest that secondary forests in this region of the Atlantic forest reached pre-disturbance N cycling dynamics after just 20 years of succession. This result contrasts with previous study in the Amazon, where the N cycle recovered slowly after abandonment from pasture reaching pre-disturbance N cycling levels after ~50 years of succession. Our results suggest the pace of the N cycle, and perhaps tropical secondary forest, recovery, may vary regionally.

Iron controls over di-nitrogen fixation in karst tropical forest.

Limestone tropical forests represent a meaningful fraction of the land area in Central America (25%) and Southeast Asia (40%). These ecosystems are marked by high biological diversity, CO2 uptake capacity, and high pH soils, the latter making them fundamentally different from the majority of lowland tropical forest areas in the Amazon and Congo basins. Here, we examine the role of bedrock geology in determining biological nitrogen fixation (BNF) rates in volcanic (low pH) vs. limestone (high pH) tropical forests located in the Maya Mountains of Belize. We experimentally test how BNF in the leaf-litter responds to nitrogen, phosphorus, molybdenum, and iron additions across different parent materials. We find evidence for iron limitation of BNF rates in limestone forests during the wet but not dry season (response ratio 3.2 ± 0.2; P = 0.03). In contrast, BNF in low pH volcanic forest soil was stimulated by the trace-metal molybdenum during the dry season. The parent-material induced patterns of limitation track changes in siderophore activity and iron bioavailability among parent materials. These findings point to a new role for iron in regulating BNF in karst tropical soils, consistent with observations for other high pH systems such as the open ocean and calcareous agricultural ecosystems.