Questions remain as to which soil nutrients limit primary production in tropical forests. Phosphorus (P) has long been considered the primary limiting element in lowland forests, but recent evidence ...demonstrates substantial heterogeneity in response to nutrient addition, highlighting a need to understand and diagnose nutrient limitation across diverse forests. Fine‐root characteristics including their abundance, functional traits, and mycorrhizal symbionts can be highly responsive to changes in soil nutrients and may help to diagnose nutrient limitation. Here, we document the response of fine roots to long‐term nitrogen (N), P, and potassium (K) fertilization in a lowland forest in Panama. Because this experiment has demonstrated that N and K together limit tree growth and P limits fine litter production, we hypothesized that fine roots would also respond to nutrient addition. Specifically we hypothesized that N, P, and K addition would reduce the biomass, diameter, tissue density, and mycorrhizal colonization of fine roots, and increase nutrient concentration in root tissue. Most morphological root traits responded to the single addition of K and the paired addition of N and P, with the greatest response to all three nutrients combined. The addition of N, P, and K together reduced fine‐root biomass, length, and tissue density, and increased specific root length, whereas root diameter remained unchanged. Nitrogen addition did not alter root N concentration, but P and K addition increased root P and K concentration, respectively. Mycorrhizal colonization of fine roots declined with N, increased with P, and was unresponsive to K addition. Although plant species composition remains unchanged after 14 years of fertilization, fine‐root characteristics responded to N, P, and K addition, providing some of the strongest stand‐level responses in this experiment. Multiple soil nutrients regulate fine‐root abundance, morphological and chemical traits, and their association with mycorrhizal fungi in a species‐rich lowland tropical forest.
We maintained a factorial nitrogen (N), phosphorus (P), and potassium (K) addition experiment for 11 years in a humid lowland forest growing on a relatively fertile soil in Panama to evaluate ...potential nutrient limitation of tree growth rates, fine-litter production, and fine-root biomass. We replicated the eight factorial treatments four times using 32 plots of 40 ×× 40 m each. The addition of K was associated with significant decreases in stand-level fine-root biomass and, in a companion study of seedlings, decreases in allocation to roots and increases in height growth rates. The addition of K and N together was associated with significant increases in growth rates of saplings and poles (1-–10 cm in diameter at breast height) and a further marginally significant decrease in stand-level fine-root biomass. The addition of P was associated with a marginally significant (
P
== 0.058) increase in fine-litter production that was consistent across all litter fractions. Our experiment provides evidence that N, P, and K all limit forest plants growing on a relatively fertile soil in the lowland tropics, with the strongest evidence for limitation by K among seedlings, saplings, and poles.
Foliar nitrogen to phosphorus (N:P) ratios are widely used to indicate soil nutrient availability and limitation, but the foliar ratios of woody plants have proven more complicated to interpret than ...ratios from whole biomass of herbaceous species. This may be related to tissues in woody species acting as nutrient reservoirs during active growth, allowing maintenance of optimal N:P ratios in recently produced, fully expanded leaves (i.e., "new" leaves, the most commonly sampled tissue). Here we address the hypothesis that N:P ratios of newly expanded leaves are less sensitive indicators of soil nutrient availability than are other tissue types in woody plants. Seedlings of five naturally established tree species were harvested from plots receiving two years of fertilizer treatments in a lowland tropical forest in the Republic of Panama. Nutrient concentrations were determined in new leaves, old leaves, stems, and roots. For stems and roots, N:P ratios increased after N addition and decreased after P addition, and trends were consistent across all five species. Older leaves also showed strong responses to N and P addition, and trends were consistent for four of five species. In comparison, overall N:P ratio responses in new leaves were more variable across species. These results indicate that the N:P ratios of stems, roots, and older leaves are more responsive indicators of soil nutrient availability than are those of new leaves. Testing the generality of this result could improve the use of tissue nutrient ratios as indices of soil nutrient availability in woody plants.
We present a meta-analysis of plant responses to fertilization experiments conducted in lowland, species-rich, tropical forests. We also update a key result and present the first species-level ...analyses of tree growth rates for a 15-yr factorial nitrogen (N), phosphorus (P), and potassium (K) experiment conducted in central Panama. The update concerns community-level tree growth rates, which responded significantly to the addition of N and K together after 10 yr of fertilization but not after 15 yr. Our experimental soils are infertile for the region, and species whose regional distributions are strongly associated with low soil P availability dominate the local tree flora. Under these circumstances, we expect muted responses to fertilization, and we predicted species associated with low-P soils would respond most slowly. The data did not support this prediction, species-level tree growth responses to P addition were unrelated to species-level soil P associations. The meta-analysis demonstrated that nutrient limitation is widespread in lowland tropical forests and evaluated two directional hypotheses concerning plant responses to N addition and to P addition. The meta-analysis supported the hypothesis that tree (or biomass) growth rate responses to fertilization are weaker in old growth forests and stronger in secondary forests, where rapid biomass accumulation provides a nutrient sink. The meta-analysis found no support for the long-standing hypothesis that plant responses are stronger for P addition and weaker for N addition. We do not advocate discarding the latter hypothesis. There are only 14 fertilization experiments from lowland, species-rich, tropical forests, 13 of the 14 experiments added nutrients for five or fewer years, and responses vary widely among experiments. Potential fertilization responses should be muted when the species present are well adapted to nutrient-poor soils, as is the case in our experiment, and when pest pressure increases with fertilization, as it does in our experiment. The statistical power and especially the duration of fertilization experiments conducted in old growth, tropical forests might be insufficient to detect the slow, modest growth responses that are to be expected.
Seed dispersal by animals is key for restoration of tropical forests because it maintains plant diversity and accelerates community turnover. Therefore, changes in seed dispersal during forest ...restoration can indicate the recovery of species interactions, and yet these changes are rarely considered in forest restoration planning. In this study, we examined shifts in the importance of different seed dispersal modes during passive restoration in a tropical chronosequence spanning more than 100 years, by modelling the proportion of trees dispersed by bats, small birds, large birds, flightless mammals and abiotic means as a function of forest age. Contrary to expectations, tree species dispersed by flightless mammals dominated after 20 years of regeneration, and tree richness and abundance dispersed by each mode mostly recovered to old growth levels between 40 and 70 years post-abandonment. Seed dispersal by small birds declined over time during regeneration, while bat dispersal played a minor role throughout all stages of succession. Results suggest that proximity to old growth forests, coupled with low hunting, explained the prevalence of seed dispersal by animals, especially by flightless mammals at this site. We suggest that aspects of seed dispersal should be monitored when restoring forest ecosystems to evaluate the reestablishment of species interactions. This article is part of the theme issue 'Understanding forest landscape restoration: reinforcing scientific foundations for the UN Decade on Ecosystem Restoration'.
Treefall gaps are the "engines of regeneration" in tropical forests and are loci of high tree recruitment, growth, and carbon accumulation. Gaps, however, are also sites of intense competition ...between lianas and trees, whereby lianas can dramatically reduce tree carbon uptake and accumulation. Because lianas have relatively low biomass, they may displace far more biomass than they contribute, a hypothesis that has never been tested with the appropriate experiments. We tested this hypothesis with an 8-yr liana removal experiment in central Panama. After 8 years, mean tree biomass accumulation was 180% greater in liana-free treefall gaps compared to control gaps. Lianas themselves contributed only 24% of the tree biomass accumulation they displaced. Scaling to the forest level revealed that lianas in gaps reduced net forest woody biomass accumulation by 8.9% to nearly 18%. Consequently, lianas reduce whole-forest carbon uptake despite their relatively low biomass. This is the first study to demonstrate experimentally that plant-plant competition can result in ecosystem-wide losses in forest carbon, and it has critical implications for recently observed increases in liana density and biomass on tropical forest carbon dynamics.
Ecology Letters (2010) 13: 849-857 Treefall gaps are hypothesized to maintain diversity by creating resource-rich, heterogeneous habitats necessary for species coexistence. This hypothesis, however, ...is not supported empirically for shade-tolerant trees, the dominant plant group in tropical forests. The failure of gaps to maintain shade-tolerant trees remains puzzling, and the hypothesis implicated to date is dispersal limitation. In central Panama, we tested an alternative 'biotic interference' hypothesis: that competition between growth forms (lianas vs. trees) constrains shade-tolerant tree recruitment, survival and diversity in gaps. We experimentally removed lianas from eight gaps and monitored them for 8 years, while also monitoring nine un-manipulated control gaps. Removing lianas increased tree growth, recruitment and richness by 55, 46 and 65%, respectively. Lianas were particularly harmful to shade-tolerant species, but not pioneers. Our findings demonstrate that competition between plant growth forms constrains diversity in a species-rich tropical forest. Because lianas are abundant in many tropical systems, our findings may apply broadly.
The spatial habitat heterogeneity hypothesis posits that habitat complexity increases the abundance and diversity of species. In tropical forests, lianas add substantial habitat heterogeneity and ...complexity throughout the vertical forest profile, which may maintain animal abundance and diversity. The effects of lianas on tropical animal communities, however, remain poorly understood. We propose that lianas have a positive effect on animals by enhancing habitat complexity. Lianas may have a particularly strong influence on the forest bird community, providing nesting substrate, protection from predators, and nutrition (food). Understory insectivorous birds, which forage for insects that specialize on lianas, may particularly benefit. Alternatively, it is possible that lianas have a negative effect on forest birds by increasing predator abundances and providing arboreal predators with travel routes with easy access to bird nests. We tested the spatial habitat heterogeneity hypothesis on bird abundance and diversity by removing lianas, thus reducing forest complexity, using a large-scale experimental approach in a lowland tropical forest in the Republic of Panama. We found that removing lianas decreased total bird abundance by 78.4% and diversity by 77.4% after 8 months, and by 40.0% and 51.7%, respectively, after 20 months. Insectivorous bird abundance and diversity 8 months after liana removal were 91.8% and 89.5% lower, respectively, indicating that lianas positively influence insectivorous birds. The effects of liana removal persisted longer for insectivorous birds than other birds, with 77.3% lower abundance and 76.2% lower diversity after 20 months. Liana removal also altered bird community composition, creating two distinct communities in the control and removal plots, with disproportionate effects on insectivores. Our findings demonstrate that lianas have a strong positive influence on the bird community, particularly for insectivorous birds in the forest understory. Lianas may maintain bird abundance and diversity by increasing habitat complexity, habitat heterogeneity, and resource availability.
Over the past two decades, liana density and basal area have been increasing in many tropical forests, which has profound consequences for forest diversity and functioning. One hypothesis to explain ...increasing lianas is elevated nutrient deposition in tropical forests resulting from fossil fuels, agricultural fertilizer, and biomass burning. We tested this hypothesis by surveying all lianas ≥1 cm in diameter (n = 3,967) in 32 plots in a fully factorial nitrogen (N), phosphorus (P), and potassium (K) addition experiment in a mature tropical forest in central Panama. We conducted the nutrient-addition experiment from 1998 until present and we first censused lianas in 2013 and then again in 2018. After 20 yr of nutrient addition (1998–2018), liana density, basal area, and rarefied species richness did not differ significantly among any of the nutrient-addition and control treatments. Moreover, nutrient addition in the most recent 5 yr of the experiment did not affect liana relative growth, recruitment, or mortality rates. From 2013 until 2018, liana density, basal area, and species richness increased annually by 1.6%, 1.4%, and 2.4%, respectively. Nutrient addition did not influence these increases. Our findings indicate that nutrient deposition does not explain increasing lianas in this tropical forest. Instead, increases in tree mortality and disturbance, atmospheric carbon dioxide, drought frequency and severity, and hunting pressure may be more likely explanations for the increase in lianas in tropical forests.
Lianas are a prominent growth form in tropical forests, and there is compelling evidence that they are increasing in abundance throughout the Neotropics. While recent evidence shows that soil ...resources limit tree growth even in deep shade, the degree to which soil resources limit lianas in forest understories, where they coexist with trees for decades, remains unknown. Regardless, the physiological underpinnings of soil resource limitation in deeply shaded tropical habitats remain largely unexplored for either trees or lianas. Theory predicts that lianas should be more limited by soil resources than trees because they occupy the quick-return end of the "leaf economic spectrum," characterized by high rates of photosynthesis, high specific leaf area, short leaf life span, affinity to high-nutrient sites, and greater foliar nutrient concentrations. To address these issues, we asked whether soil resources (nitrogen, phosphorus, and potassium), alone or in combination, applied experimentally for more than a decade would cause significant changes in the morphology or physiology of tree and liana seedlings in a lowland tropical forest. We found evidence for the first time that phosphorus limits the photosynthetic performance of both trees and lianas in deeply shaded understory habitats. More importantly, lianas always showed significantly greater photosynthetic capacity, quenching, and saturating light levels compared to trees across all treatments. We found little evidence for nutrient × growth form interactions, indicating that lianas were not disproportionately favored in nutrient-rich habitats. Tree and liana seedlings differed markedly for six key morphological traits, demonstrating that architectural differences occurred very early in ontogeny prior to lianas finding a trellis (all seedlings were self-supporting). Overall, our results do not support nutrient loading as a mechanism of increasing liana abundance in the Neotropics. Rather, our finding that lianas always outperform trees, in terms of photosynthetic processes and under contrasting rates of resource supply of macronutrients, will allow lianas to increase in abundance if disturbance and tree turnover rates are increasing in Neotropical forests as has been suggested.
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