Publisher Correction: Pervasive phosphorus limitation of tree species but not communities in tropical forests.

In this Letter, the y axis of the right-hand panel of Fig. 2a was mislabelled 'Phosphomonoesterase' instead of 'Phosphodiesterase'. This error has been corrected online.

Pervasive phosphorus limitation of tree species but not communities in tropical forests.

Phosphorus availability is widely assumed to limit primary productivity in tropical forests, but support for this paradigm is equivocal. Although biogeochemical theory predicts that phosphorus limitation should be prevalent on old, strongly weathered soils, experimental manipulations have failed to detect a consistent response to phosphorus addition in species-rich lowland tropical forests. Here we show, by quantifying the growth of 541 tropical tree species across a steep natural phosphorus gradient in Panama, that phosphorus limitation is widespread at the level of individual species and strengthens markedly below a threshold of two parts per million exchangeable soil phosphate. However, this pervasive species-specific phosphorus limitation does not translate into a community-wide response, because some species grow rapidly on infertile soils despite extremely low phosphorus availability. These results redefine our understanding of nutrient limitation in diverse plant communities and have important implications for attempts to predict the response of tropical forests to environmental change.

Dynamics of two multi-stemmed understory shrubs in two temperate forests.

A multi-stemmed growth form may be an important trait enabling the persistence of individual shrubs in the forest understory. With the aim of evaluating the role of multiple stems, neighbor competition and soil nutrients in shrub performance, we study the dynamics of two temperate multi-stemmed shrub species. We modeled stem growth and survival of Corylus mandshurica and Acer barbinerve in two temperate forests with differing structure in northeastern China. One forest was an old growth broad-leaved Korean pine (Pinus koraiensis) mixed forest; the other was a secondary poplar-birch forest. Growth of the two species and survival of C. mandshurica increased with stem number in the old growth forest, but not the secondary forest, suggesting the benefits of a multi-stemmed growth form are facultative. C. mandshurica also suffered more from overstory neighbor competition in the old growth forest, which may suggest that this species is less shade-tolerant than A. barbinerve. Moreover, the performance of the two species were clearly influenced by understory neighbors and soil variables in the old growth forest relative to the secondary forest, which may be due to different forest structure. We conclude that multiple stems are not always important for the persistence of shrub species. Even within the same species, the multi-stemmed benefits might be facultative, differing among forests and neighborhood compositions.

Leaf damage and density-dependent effects on six Inga species in a neotropical forest

Many models have been proposed to explain the possible role of pests in the coexistence of a high diversity of plant species in tropical forests. Prominent among them is the Janzen-Connell model. This model suggests that specialized herbivores and pathogens limit tree recruitment as a function of their density or proximity to conspecifics. A large number of studies have tested the predictions of this model with respect to patterns of recruitment and mortality at different life stages, yet only a few have directly linked those density or distance-dependent effects to pest attack. If pest-attack is an important factor in density or distance-dependent mortality, there should be spatial heterogeneity in pest pressure. I studied the spatial distribution of leaf damage in saplings of six common Inga species (Fabaceae: Mimosoideae) in the 50ha forest dynamic plot of Barro Colorado Island, Panama. The percent leaf damage of Inga saplings was not heterogeneous in space, and the density of conspecific, congener or confamilial neighbors was uncorrelated with the observed damage levels in focal plants. One of the focal species did suffer density-dependent mortality, suggesting that spatial variation in plant performance in these species is not directly driven by leaf damaging agents. While multiple studies suggest that density-dependent effects on performance are common in tropical plant communities, our understanding of the mechanisms that drive those effects is still incomplete and the underlying assumption that these patterns result from differential herbivore attack deserves more scrutiny.

Se han propuesto muchos modelos para explicar la coexistencia de una alta diversidad de especies de árboles en bosques tropicales. Prominente, entre estos modelos es el de Janzen-Connell, que sugiere que los herbívoros especialistas limitan la colonización de árboles en función de la densidad o proximidad de con-específicos. Si este efecto es en realidad el resultado de ataque por herbívoros, debiera haber heterogeneidad espacial en la herbivoría. Aquí se evalúa esta hipótesis estudiando la distribución espacial de la herbivoría en juveniles de seis especies comunes de Inga (Fabaceae: Mimosoideae) en la parcela de 50ha de la Isla de Barro Colorado, en Panamá. Análisis de autocorrelación espacial no mostraron heterogeneidad en la herbivoría de estas especies, y la densidad local de con-específicos, congéneres o confamiliares no se correlacionó con la herbivoría de las plantas estudiadas. Solo una de las especies de estudio sufrió mortalidad densidad-dependiente en 20 años de censos. Aunque muchos estudios han demostrado que los efectos densidad-dependientes en la mortalidad de las plantas son comunes en bosques tropicales, nuestro entendimiento de los mecanismos que causan esos efectos es aún limitado, y la suposición de que estos resultan de heterogeneidad espacial en el ataque de herbívoros merece más escrutinio.

Leaf damage and density-dependent effects on six Inga species in a neotropical forest.

Many models have been proposed to explain the possible role of pests in the coexistence of a high diversity of plant species in tropical forests. Prominent among them is the Janzen-Connell model. This model suggests that specialized herbivores and pathogens limit tree recruitment as a function of their density or proximity to conspecifics. A large number of studies have tested the predictions of this model with respect to patterns of recruitment and mortality at different life stages, yet only a few have directly linked those density- or distance-dependent effects to pest attack. If pest-attack is an important factor in density- or distance-dependent mortality, there should be spatial heterogeneity in pest pressure. I studied the spatial distribution of leaf damage in saplings of six common Inga species (Fabaceae: Mimosoideae) in the 50ha forest dynamic plot of Barro Colorado Island, Panama. The percent leaf damage of Inga saplings was not heterogeneous in space, and the density of conspecific, congener or confamilial neighbors was uncorrelated with the observed damage levels in focal plants. One of the focal species did suffer density-dependent mortality, suggesting that spatial variation in plant performance in these species is not directly driven by leaf damaging agents. While multiple studies suggest that density-dependent effects on performance are common in tropical plant communities, our understanding of the mechanisms that drive those effects is still incomplete and the underlying assumption that these patterns result from differential herbivore attack deserves more scrutiny.

Pests vs. drought as determinants of plant distribution along a tropical rainfall gradient.

Understanding the mechanisms that shape the distribution of organisms can help explain patterns of local and regional biodiversity and predict the susceptibility of communities to environmental change. In the species-rich tropics, a gradient in rainfall between wet evergreen and dry seasonal forests correlates with turnover of plant species. The strength of the dry season has previously been shown to correlate with species composition. Herbivores and pathogens (pests) have also been hypothesized to be important drivers of plant distribution, although empirical evidence is lacking. In this study we experimentally tested the existence of a gradient in pest pressure across a rainfall gradient in the Isthmus of Panama and measured the influence of pests relative to drought on species turnover. We established two common gardens on the dry and wet sides of the Isthmus using seedlings from 24 plant species with contrasting distributions along the Isthmus. By experimentally manipulating water availability and insect herbivore access, we showed that pests are not as strong a determinant of plant distributions as is seasonal drought. Seasonal drought in the dry site excluded wet-distribution species by significantly increasing their seedling mortality. Pathogen mortality and insect herbivore damage were both higher in the wet site, supporting the existence of a gradient in pest pressure. However, contrary to predictions, we found little evidence that dry-distribution species suffered significantly more pest attack than wet-distribution species. Instead, we hypothesize that dry-distribution species are limited from colonizing wetter forests by their inherently slower growth rates imposed by drought adaptations. We conclude that mechanisms limiting the recruitment of dry-distribution species in wet forests are not nearly as strong as those limiting wet-distribution species from dry forests.

Contrasting mechanisms of secondary metabolite accumulation during leaf development in two tropical tree species with different leaf expansion strategies.

Young leaves of most species experience remarkably higher herbivore attack rates than mature leaves. Considerable theoretical effort has focused on predicting optimal defense and tradeoffs in defense allocation during leaf expansion. Among others, allocation to secondary chemistry may be dependent on growth constraints. We studied flavanoid production during leaf development in two species of Inga (Fabaceae: Mimosoideae) with different expansion strategies: Inga goldmanii, a species with slowly expanding young leaves, and Inga umbellifera, a species with fast-expanding young leaves. In these two species, the most abundant and toxic class of defensive compounds is flavanoids (which include tannins). We measured their concentration by leaf dry weight, their total content per leaf, their HPLC chemical profile and their toxicity to a generalist herbivore at different expansion levels. Although in both species the flavanoid concentration decreased with increasing leaf expansion, that decrease was twice as pronounced for I. umbellifera as it was for I. goldmanii. I. umbellifera leaves produced flavanoids only during the first half of their development while I. goldmanii leaves continued production throughout. The changes in flavanoid HPLC profiles and toxicity were also more dramatic for I. umbellifera, which had different flavanoids in young than in mature leaves. Relative to I. umbellifera, I. goldmanii showed smaller changes in both flavanoid composition and toxicity in the transition from young to mature leaves. These results indicate that, even though young leaves suffer higher rates of attack and are predicted to have better chemical defenses than mature leaves, growth constraints may modulate defense allocation and thus, evolution of defense strategies.

Allelochemic function for a primary metabolite: the case of l-tyrosine hyper-production in Inga umbellifera (Fabaceae).

Young leaves of tropical forest trees experience far higher herbivory pressure than mature leaves of the same species. Selection on young leaves has led to diverse forms of defense chemical expression. Though most allelochemicals are secondary metabolites, allelochemic function for a primary metabolite remains a possibility. We recently observed this phenomenon in the young leaves of Inga umbellifera, which accumulate the protein amino acid l-tyrosine to very high levels. We isolated l-tyrosine from young leaves of trees in Panama and characterized it using spectroscopic and chemical means. We chromatographically quantified leaf l-tyrosine levels across a range of developmental stages, showing that it was present in the youngest leaves and that its concentration increased throughout the period of expansion, reaching an average maximum of ca 10% of leaf dry mass in late-stage young leaves. This chemical phenotype was seen to be highly leaf-age specific: Free tyrosine was only present in mature leaves at very low levels. In bioassays with larvae of the noctuid moth H. virescens, l-tyrosine proved to be a potent growth inhibitor when added to artificial diet at 10% of dry mass. This suggests that a rarely observed defense strategy occurs in young I. umbellifera leaves, a hyper-produced primary metabolite functioning as an allelochemical.