Paul-Camilo Zalamea

Continental-scale patterns of Cecropia reproductive phenology: evidence from herbarium specimens

Plant phenology is concerned with the timing of recurring biological events. Though phenology has traditionally been studied using intensive surveys of a local flora, results from such surveys are difficult to generalize to broader spatial scales. In this study, contrastingly, we assembled a continental-scale dataset of herbarium specimens for the emblematic genus of Neotropical pioneer trees, Cecropia, and applied Fourier spectral and cospectral analyses to investigate the reproductive phenology of 35 species. We detected significant annual, sub-annual and continuous patterns, and discuss the variation in patterns within and among climatic regions. Although previous studies have suggested that pioneer species generally produce flowers continually throughout the year, we found that at least one third of Cecropia species are characterized by clear annual flowering behaviour. We further investigated the relationships between phenology and climate seasonality, showing strong associations between phenology and seasonal variations in precipitation and temperature. We also verified our results against field survey data gathered from the literature. Our findings indicate that herbarium material is a reliable resource for use in the investigation of large-scale patterns in plant phenology, offering a promising complement to local intensive field studies.

Growth pattern and age determination for Cecropia sciadophylla (Urticaceae)

Cecropia species, ranging from Mexico to northern Argentina and the West Indies, are pioneer trees that colonize cleared areas with high light. To determine their ages to help pinpoint the date of the areas disturbance, we need to understand their developmental and architectural changes over time. The simple architecture of Cecropia conforms to the model of Rauh; that is, it has orthotropic axes with lateral flowering and rhythmic branching. The axes are made of a succession of nodes and internodes whose length and associated lateral productions remain measurable for years. Thus, by describing the tree trunk node by node, we can depict the sequence of events involved in tree development. For 25 trees of C. sciadophylla, from two stations in French Guiana and Colombia, we recorded internode length and any presence of branches, and flowers for each node. Using autocorrelation coefficients, we found a high periodicity in flowering and branching, with inflorescences at every 25 nodes, stages of branches spaced by a multiple of 25 nodes, and alternation of long and short nodes every 25 nodes. Considering that flowering is annual for many Cecropia species, the main conclusion of this work is that C. sciadophylla has strong annual growth, branching, and flowering rhythms. In addition, the age of the tree can be estimated retrospectively by observing its adult morphology.

Seedling growth responses to phosphorus reflect adult distribution patterns of tropical trees

Soils influence tropical forest composition at regional scales. In Panama, data on tree communities and underlying soils indicate that species frequently show distributional associations to soil phosphorus. To understand how these associations arise, we combined a pot experiment to measure seedling responses of 15 pioneer species to phosphorus addition with an analysis of the phylogenetic structure of phosphorus associations of the entire tree community. Growth responses of pioneers to phosphorus addition revealed a clear tradeoff: species from high-phosphorus sites grew fastest in the phosphorus-addition treatment, while species from low-phosphorus sites grew fastest in the low-phosphorus treatment. Traits associated with growth performance remain unclear: biomass allocation, phosphatase activity and phosphorus-use efficiency did not correlate with phosphorus associations; however, phosphatase activity was most strongly down-regulated in response to phosphorus addition in species from high-phosphorus sites. Phylogenetic analysis indicated that pioneers occur more frequently in clades where phosphorus associations are overdispersed as compared with the overall tree community, suggesting that selection on phosphorus acquisition and use may be strongest for pioneer species with high phosphorus demand. Our results show that phosphorus-dependent growth rates provide an additional explanation for the regional distribution of tree species in Panama, and possibly elsewhere.

Diversity, Specificity, and Phylogenetic Relationships of Endohyphal Bacteria in Fungi That Inhabit Tropical Seeds and Leaves

Interactions between fungi and tropical trees help shape some of the most biodiverse communities on earth. These interactions occur in the presence of additional microbes that can modify fungal phenotypes, such as endohyphal bacteria (EHB). Here we examine the occurrence, diversity, and taxonomic composition of EHB in fungi that colonize seeds and leaves of plants in tropical forests. We use PCR and fluorescence microscopy to detect EHB in fungi, and a phylogenetic approach to explore evolutionary relationships among seed- and leaf-inhabiting fungi and their bacterial partners. Analyses focusing on two prevalent orders of fungi (Hypocreales and Xylariales) revealed that seed- and leaf-inhabiting fungi have a shared evolutionary history, yet differ in the prevalence, richness, and composition of their endohyphal symbionts. Phylogenetic analyses detected that the endohyphal habit is widespread, here encompassing members of seven phyla of bacteria (including three classes of Proteobacteria). Occurring in seed- vs. leaf-associated fungi has not resulted in detectable structure in the evolution of EHB, and no congruence was observed in the phylogenetic relationships of these apparently facultative, horizontally transmitted symbionts and their fungal hosts. Our results are consistent with multiple origins of fungus-bacterium associations and argue for evaluating focal pairs to determine how particular EHB affect the establishment or maintenance of fungal symbioses in seeds and leaves.

The Genus Cecropia: A Biological Clock to Estimate the Age of Recently Disturbed Areas in the Neotropics

Forest successional processes following disturbance take decades to play out, even in tropical forests. Nonetheless, records of vegetation change in this ecosystem are scarce, increasing the importance of the chronosequence approach to study forest recovery. However, this approach requires accurate dating of secondary forests, which until now was a difficult and/or expensive task. Cecropia is a widespread and abundant pioneer tree genus of the Neotropics. Here we propose and validate a rapid and straightforward method to estimate the age of secondary forest patches based on morphological observations of Cecropia trees. We found that Cecropia-inferred ages were highly correlated with known ages of the forest. We also demonstrate that Cecropia can be used to accurately date disturbances and propose twenty-one species distributed all over the geographical range of the genus as potential secondary forest chronometer species. Our method is limited in applicability by the maximal longevity of Cecropia individuals. Although the oldest chronosequence used in this study was 20 years old, we argue that at least for the first four decades after disturbance, the method described in this study provides very accurate estimations of secondary forest ages. The age of pioneer trees provides not only information needed to calculate the recovery of carbon stocks that would help to improve forest management, but also provides information needed to characterize the initial floristic composition and the rates of species remigration into secondary forest. Our contribution shows how successional studies can be reliably and inexpensively extended without the need to obtain forest ages based on expensive or potentially inaccurate data across the Neotropics.

Soilborne fungi have host affinity and host-specific effects on seed germination and survival in a lowland tropical forest.

Significance The remarkable diversity of trees in tropical forests is thought to be maintained by natural enemies such as fungal pathogens, which must exhibit sufficient host specificity to differentially impact survival of co-occurring host species. Little is known about the specificity of fungi that infect seeds of tropical trees. Here we show that communities of seed-associated fungi are structured more by plant species than by soil type, forest characteristics, or time in soil. These fungi have host-specific impacts on seed viability and germination. In this way, highly diverse communities of soilborne fungi directly impact a critical component of reproduction in tropical trees—seeds—with the potential to contribute to maintaining diversity in some of the richest terrestrial communities on Earth. The Janzen–Connell (JC) hypothesis provides a conceptual framework for explaining the maintenance of tree diversity in tropical forests. Its central tenet—that recruits experience high mortality near conspecifics and at high densities—assumes a degree of host specialization in interactions between plants and natural enemies. Studies confirming JC effects have focused primarily on spatial distributions of seedlings and saplings, leaving major knowledge gaps regarding the fate of seeds in soil and the specificity of the soilborne fungi that are their most important antagonists. Here we use a common garden experiment in a lowland tropical forest in Panama to show that communities of seed-infecting fungi are structured predominantly by plant species, with only minor influences of factors such as local soil type, forest characteristics, or time in soil (1–12 months). Inoculation experiments confirmed that fungi affected seed viability and germination in a host-specific manner and that effects on seed viability preceded seedling emergence. Seeds are critical components of reproduction for tropical trees, and the factors influencing their persistence, survival, and germination shape the populations of seedlings and saplings on which current perspectives regarding forest dynamics are based. Together these findings bring seed dynamics to light in the context of the JC hypothesis, implicating them directly in the processes that have emerged as critical for diversity maintenance in species-rich tropical forests.

Asynchrony of Seasons: Genetic Differentiation Associated with Geographic Variation in Climatic Seasonality and Reproductive Phenology

Many organisms exhibit distinct breeding seasons tracking food availability. If conspecific populations inhabit areas that experience different temporal cycles in food availability spurred by variation in precipitation regimes, then they should display asynchronous breeding seasons. Thus, such populations might exhibit a temporal barrier to gene flow, which may potentially promote genetic differentiation. We test a central prediction of this hypothesis, namely, that individuals living in areas with more asynchronous precipitation regimes should be more genetically differentiated than individuals living in areas with more similar precipitation regimes. Using mitochondrial DNA sequences, climatic data, and geographical/ecological distances between individuals of 57 New World bird species mostly from the tropics, we examined the effect of asynchronous precipitation (a proxy for asynchronous resource availability) on genetic differentiation. We found evidence for a positive and significant cross-species effect of precipitation asynchrony on genetic distance after accounting for geographical/ecological distances, suggesting that current climatic conditions may play a role in population differentiation. Spatial asynchrony in climate may thus drive evolutionary divergence in the absence of overt geographic barriers to gene flow; this mechanism contrasts with those invoked by most models of biotic diversification emphasizing physical or ecological changes to the landscape as drivers of divergence.

Seed polyphenols in a diverse tropical plant community

Polyphenols are one of the most common groups of secondary metabolites in plants and thought to play a key role in enhancing plant fitness by protecting plants against enemies. Although enemy-inflicted mortality at the seed stage can be an important regulator of plant populations and a key determinant of community structure, few studies have assessed community-level patterns of polyphenol content in seeds. We describe the distribution of the main seed polyphenol groups across 196 tree and liana species on Barro Colorado Island (Panama) and community-level patterns in two aspects of their biological activity (protein precipitation and oxidative capacity). Taking advantage of substantial variation in morphological and ecological traits in the studied plant community, we test for correlations and trade-offs between seed polyphenols and nonchemical plant traits hypothesised to make plant species more or less likely to invest in polyphenol production. The majority of species have polyphenols in their seeds. The incidence and concentrations of polyphenols were related to a set of nonchemical plant traits. Polyphenols were most likely to be present (and where present, to be expressed in high concentrations) in species with large seeds, short seed dormancy times, low investment in mechanical seed defences, high wood density, high leaf mass per area, tough leaves and slow growth rates. Synthesis. Our study reveals a potential trade-off between chemical and mechanical seed defences and shows that plant species that invest in physical defences at later life stages (high wood density and tough leaves) tend not to invest in physical defences of seeds but instead produce secondary metabolites likely to act as seed defences. Overall, our results conform to predictions from the resource availability hypothesis, which states that species in resource-limited environments (such as slow-growing shade-tolerant tree species) will invest more in defences than fast-growing pioneer species. (Less)

Analysing the effects of local environment on the source-sink balance of Cecropia sciadophylla: a methodological approach based on model inversion

Abstract• ContextFunctional–structural models (FSM) of tree growth have great potential in forestry, but their development, calibration and validation are hampered by the difficulty of collecting experimental data at organ scale for adult trees. Due to their simple architecture and morphological properties, “model plants” such as Cecropia sciadophylla are of great interest to validate new models and methodologies, since exhaustive descriptions of their plant structure and mass partitioning can be gathered.• AimsOur objective was to develop a model-based approach to analysing the influence of environmental conditions on the dynamics of trophic competition within C. sciadophylla trees.• MethodsWe defined an integrated environmental factor that includes meteorological medium-frequency variations and a relative index representing the local site conditions for each plant. This index is estimated based on model inversion of the GreenLab FSM using data from 11 trees for model calibration and 7 trees for model evaluation.• ResultsThe resulting model explained the dynamics of biomass allocation to different organs during the plant growth, according to the environmental pressure they experienced.• PerspectivesBy linking the integrated environmental factor to a competition index, an extension of the model to the population level could be considered.

Analysis of Cecropia sciadophylla Morphogenesis Based on a Sink-Source Dynamic Model

Although there is an increasing number of models simulating the functional and structural development of trees at organ scale, few of them can be fully calibrated, evaluated and validated. A major obstacle resides in the intrinsic complexity of trees due to their high stature, large number of organs and long life span that limits the possibilities of experimental work and the access to measurement data. This is why ’model plants’ such as the neotropical genus Cecropia are of great interest. This genus has a simple architecture and some qualities that allow collecting exhaustive datasets at the organ scale. In this paper, we evaluate the GreenLab model on data recorded on 11 individuals measured in 2007 in French Guiana. The branching and flowering patterns are analyzed using an index of trophic competition.