Plant responses to fertilization experiments in lowland, species-rich, tropical forests.

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.

Arbuscular mycorrhizal fungal community composition is altered by long-term litter removal but not litter addition in a lowland tropical forest.

Tropical forest productivity is sustained by the cycling of nutrients through decomposing organic matter. Arbuscular mycorrhizal (AM) fungi play a key role in the nutrition of tropical trees, yet there has been little experimental investigation into the role of AM fungi in nutrient cycling via decomposing organic material in tropical forests. We evaluated the responses of AM fungi in a long-term leaf litter addition and removal experiment in a tropical forest in Panama. We described AM fungal communities using 454-pyrosequencing, quantified the proportion of root length colonised by AM fungi using microscopy, and estimated AM fungal biomass using a lipid biomarker. AM fungal community composition was altered by litter removal but not litter addition. Root colonisation was substantially greater in the superficial organic layer compared with the mineral soil. Overall colonisation was lower in the litter removal treatment, which lacked an organic layer. There was no effect of litter manipulation on the concentration of the AM fungal lipid biomarker in the mineral soil. We hypothesise that reductions in organic matter brought about by litter removal may lead to AM fungi obtaining nutrients from recalcitrant organic or mineral sources in the soil, besides increasing fungal competition for progressively limited resources.

Geographical variation in species' population responses to changes in temperature and precipitation.

Despite increasing concerns about the vulnerability of species' populations to climate change, there has been little overall synthesis of how individual population responses to variation in climate differ between taxa, with trophic level or geographically. To address this, we extracted data from 132 long-term (greater than or equal to 20 years) studies of population responses to temperature and precipitation covering 236 animal and plant species across terrestrial and freshwater habitats. Our results identify likely geographical differences in the effects of climate change on populations and communities in line with macroecological theory. Temperature tended to have a greater overall impact on populations than precipitation, although the effects of increased precipitation varied strongly with latitude, being most positive at low latitudes. Population responses to increased temperature were generally positive, but did not vary significantly with latitude. Studies reporting significant climatic trends through time tended to show more negative effects of temperature and more positive effects of precipitation upon populations than other studies, indicating climate change has already impacted many populations. Most studies of climate change impacts on biodiversity have focused on temperature and are from middle to high northern latitudes. Our results suggest their findings may be less applicable to low latitudes.

Mechanisms underpinning climatic impacts on natural populations: altered species interactions are more important than direct effects.

Shifts in species' distribution and abundance in response to climate change have been well documented, but the underpinning processes are still poorly understood. We present the results of a systematic literature review and meta-analysis investigating the frequency and importance of different mechanisms by which climate has impacted natural populations. Most studies were from temperate latitudes of North America and Europe; almost half investigated bird populations. We found significantly greater support for indirect, biotic mechanisms than direct, abiotic mechanisms as mediators of the impact of climate on populations. In addition, biotic effects tended to have greater support than abiotic factors in studies of species from higher trophic levels. For primary consumers, the impact of climate was equally mediated by biotic and abiotic mechanisms, whereas for higher level consumers the mechanisms were most frequently biotic, such as predation or food availability. Biotic mechanisms were more frequently supported in studies that reported a directional trend in climate than in studies with no such climatic change, although sample sizes for this comparison were small. We call for more mechanistic studies of climate change impacts on populations, particularly in tropical systems.

Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis.

Tropical rain forests play a dominant role in global biosphere-atmosphere CO(2) exchange. Although climate and nutrient availability regulate net primary production (NPP) and decomposition in all terrestrial ecosystems, the nature and extent of such controls in tropical forests remain poorly resolved. We conducted a meta-analysis of carbon-nutrient-climate relationships in 113 sites across the tropical forest biome. Our analyses showed that mean annual temperature was the strongest predictor of aboveground NPP (ANPP) across all tropical forests, but this relationship was driven by distinct temperature differences between upland and lowland forests. Within lowland forests (< 1000 m), a regression tree analysis revealed that foliar and soil-based measurements of phosphorus (P) were the only variables that explained a significant proportion of the variation in ANPP, although the relationships were weak. However, foliar P, foliar nitrogen (N), litter decomposition rate (k), soil N and soil respiration were all directly related with total surface (0-10 cm) soil P concentrations. Our analysis provides some evidence that P availability regulates NPP and other ecosystem processes in lowland tropical forests, but more importantly, underscores the need for a series of large-scale nutrient manipulations - especially in lowland forests - to elucidate the most important nutrient interactions and controls.

Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a 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 x 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.

Arbuscular mycorrhizal mycelial respiration in a moist tropical forest.

*Arbuscular mycorrhizal fungi (AMF) are widespread in tropical forests and represent a major sink of photosynthate, yet their contribution to soil respiration in such ecosystems remains unknown. *Using in-growth mesocosms we measured AMF mycelial respiration in two separate experiments: (1) an experiment in a semi-evergreen moist tropical forest, and (2) an experiment with 6-m-tall Pseudobombax septenatum in 4.5-m(3) containers, for which we also determined the dependence of AMF mycelial respiration on the supply of carbon from the plant using girdling and root-cutting treatments. *In the forest, AMF mycelia respired carbon at a rate of 1.4 t ha(-1) yr(-1), which accounted for 14 +/- 6% of total soil respiration and 26 +/- 12% of root-derived respiration. For P. septenatum, 40 +/- 6% of root-derived respiration originated from AMF mycelia and carbon was respired < 4 h after its supply from roots. *We conclude that arbuscular mycorrhizal mycelial respiration can be substantial in lowland tropical forests. As it is highly dependent on the recent supply of carbon from roots, a function of aboveground fixation, AMF mycelial respiration is therefore an important pathway of carbon flux from tropical forest trees to the atmosphere.

Climate change could threaten cocoa production: Effects of 2015-16 El Niño-related drought on cocoa agroforests in Bahia, Brazil.

Climate models predict a possible increase in the frequency of strong climate events such as El Niño-Southern Oscillation (ENSO), which in parts of the tropics are the cause of exceptional droughts, these threaten global food production. Agroforestry systems are often suggested as promising diversification options to increase farmers' resilience to extreme climatic events. In the Northeastern state of Bahia, where most Brazilian cocoa is grown in wildlife-friendly agroforests, ENSOs cause severe droughts which negatively affect forest and agriculture. Cocoa (Theobroma cacao) is described as being sensitive to drought but there are no field-studies of the effect of ENSO-related drought on adult cocoa trees in the America's; there is one study of an experimentally-imposed drought in Indonesia which resulted in 10 to 46% yield loss. In our study, in randomly chosen farms in Bahia, Brazil, we measured the effect of the 2015-16 severe ENSO, which caused an unprecedented drought in cocoa agroforests. We show that drought caused high cocoa tree mortality (15%) and severely decreased cocoa yield (89%); the drought also increased infection rate of the chronic fungal disease witches' broom (Moniliophthora perniciosa). Ours findings showed that Brazilian cocoa agroforests are at risk and that increasing frequency of strong droughts are likely to cause decreased cocoa yields in the coming decades. Furthermore, because cocoa, like many crops, is grown somewhat beyond its climatic limits, it and other crops could be the 'canaries in the coalmine' warning of forthcoming major drought effects on semi-natural and natural vegetation.

Responses of arbuscular mycorrhizal fungi to long-term inorganic and organic nutrient addition in a lowland tropical forest.

Improved understanding of the nutritional ecology of arbuscular mycorrhizal (AM) fungi is important in understanding how tropical forests maintain high productivity on low-fertility soils. Relatively little is known about how AM fungi will respond to changes in nutrient inputs in tropical forests, which hampers our ability to assess how forest productivity will be influenced by anthropogenic change. Here we assessed the influence of long-term inorganic and organic nutrient additions and nutrient depletion on AM fungi, using two adjacent experiments in a lowland tropical forest in Panama. We characterised AM fungal communities in soil and roots using 454-pyrosequencing, and quantified AM fungal abundance using microscopy and a lipid biomarker. Phosphorus and nitrogen addition reduced the abundance of AM fungi to a similar extent, but affected community composition in different ways. Nutrient depletion (removal of leaf litter) had a pronounced effect on AM fungal community composition, affecting nearly as many OTUs as phosphorus addition. The addition of nutrients in organic form (leaf litter) had little effect on any AM fungal parameter. Soil AM fungal communities responded more strongly to changes in nutrient availability than communities in roots. This suggests that the 'dual niches' of AM fungi in soil versus roots are structured to different degrees by abiotic environmental filters, and biotic filters imposed by the plant host. Our findings indicate that AM fungal communities are fine-tuned to nutrient regimes, and support future studies aiming to link AM fungal community dynamics with ecosystem function.

Root and arbuscular mycorrhizal mycelial interactions with soil microorganisms in lowland tropical forest.

Tropical forests have high rates of soil carbon cycling, but little information is available on how roots, arbuscular mycorrhizal fungi (AMF), and free-living microorganisms interact and influence organic matter mineralization in these ecosystems. We used mesh ingrowth cores and isotopic tracers in phospholipid fatty acid biomarkers to investigate the effects of roots and AMF mycelia on (1) microbial community composition, microbial carbon utilization, and hydrolytic enzyme activities for large, potted tropical trees and (2) enzyme activities and litter mass loss in a lowland tropical forest. Under the tropical tree, plant-derived carbon was incorporated predominantly into bacterial groups in both rhizosphere and AMF-only soils. Gram-positive bacteria incorporated additional soil-derived carbon in rhizosphere soils, which also contained the highest microbial biomass. For hydrolytic enzymes, ß-glucosidase and N-acetyl ß-glucosaminidase activities were highest in rhizosphere soils, while phosphomonoesterase activity was highest in AMF-only soil. In the forest, leaf litter mass loss was increased by the presence of roots, but not by the presence of AMF mycelia only. Root-microbial interactions influenced organic matter cycling, with evidence for rhizosphere priming and accelerated leaf litter decomposition in the presence of roots. Although AMF mycelia alone did not stimulate organic matter mineralization, they were a conduit of carbon to other soil microorganisms.

Evaluation of forest recovery over time and space using permanent plots monitored over 30 years in a Jamaican montane rain forest.

Conservation of tropical forest biodiversity increasingly depends on its recovery following severe human disturbance. Our ability to measure recovery using current similarity indices suffers from two limitations: different sized individuals are treated as equal, and the indices are proportionate (a community with twice the individuals of every species as compared with the reference community would be assessed as identical). We define an alternative recovery index for trees - the Tanner index, as the mean of the quantitative Bray-Curtis similarity indices of species composition for stem density and for basal area. We used the new index to compare the original (pre-gap) and post-gap composition of five experimental gap plots (each 90-100 m(2)) and four control plots over 24-35 years in the Blue Mountains of Jamaica. After 24-35 years, these small gaps surrounded by undisturbed forest had recovered 68% of the sum of per species stem density and 29% of the sum of per species basal area, a recovery index of 47%. Four endemic species were especially reduced in density and basal area. With the incorporation of basal area and stem density, our index reduces over-estimations of forest recovery obtained using existing similarity indices (by 24%-41%), and thus yields more accurate estimates of forest conservation status. Finally, our study indicates that the two kinds of comparisons: 1) over time between pre-gap and post-gap composition and 2) over space between gap plots and spatial controls (space-for-time substitution) yield broadly similar results, which supports the value of using space-for-time substitutions in studying forest recovery, at least in this tropical montane forest.

Increased litterfall in tropical forests boosts the transfer of soil CO2 to the atmosphere.

Aboveground litter production in forests is likely to increase as a consequence of elevated atmospheric carbon dioxide (CO(2)) concentrations, rising temperatures, and shifting rainfall patterns. As litterfall represents a major flux of carbon from vegetation to soil, changes in litter inputs are likely to have wide-reaching consequences for soil carbon dynamics. Such disturbances to the carbon balance may be particularly important in the tropics because tropical forests store almost 30% of the global soil carbon, making them a critical component of the global carbon cycle; nevertheless, the effects of increasing aboveground litter production on belowground carbon dynamics are poorly understood. We used long-term, large-scale monthly litter removal and addition treatments in a lowland tropical forest to assess the consequences of increased litterfall on belowground CO(2) production. Over the second to the fifth year of treatments, litter addition increased soil respiration more than litter removal decreased it; soil respiration was on average 20% lower in the litter removal and 43% higher in the litter addition treatment compared to the controls but litter addition did not change microbial biomass. We predicted a 9% increase in soil respiration in the litter addition plots, based on the 20% decrease in the litter removal plots and an 11% reduction due to lower fine root biomass in the litter addition plots. The 43% measured increase in soil respiration was therefore 34% higher than predicted and it is possible that this 'extra' CO(2) was a result of priming effects, i.e. stimulation of the decomposition of older soil organic matter by the addition of fresh organic matter. Our results show that increases in aboveground litter production as a result of global change have the potential to cause considerable losses of soil carbon to the atmosphere in tropical forests.