[Show abstract][Hide abstract] ABSTRACT: 1. Classic theory in plant-insect interactions has linked herbivore pressure with diversification in plant species. We hypothesize that herbivores may exert divergent selection on defenses, such that closely related plant species will be more different in defensive than in non-defensive traits.2. We evaluated this hypothesis by investigating two clades of closely related plant species coexisting at a single site in the Peruvian Amazon: Inga capitata Desv., and Inga heterophylla Willd. species complexes. We compared how these lineages differ in the suite of chemical, biotic, phenological and developmental defenses as compared to non-defensive traits that are related to habitat use and resource acquisition. We also collected insect herbivores feeding on the plants.3. Our data show that sister lineages within both species complexes are more divergent in anti-herbivore defenses than in other non-defensive, functional traits. Moreover, the assemblages of herbivore communities are dissimilar between the populations of coexisting I. capitata lineages.4. Synthesis Our results are consistent with the idea that for the I. capitata and I. heterophylla species complexes, interactions with their natural enemies may have played a significant role in their phenotypic divergence and potentially in their diversification and coexistence. It also suggests that defensive traits are evolutionary labile.This article is protected by copyright. All rights reserved.
Journal of Ecology 06/2015; DOI:10.1111/1365-2745.12431 · 5.69 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Tree species in seasonally dry tropical forests likely vary in their drought-survival mechanisms. Drought-deciduousness, which reduces water loss, and low wood density, which may permit dependence on stored water, are considered key traits. For saplings of six species at two distinct sites, we studied these and two associated traits: the seasonal amount of water released per stem volume (“water released”) and the hydraulic capacitance of the stem (C). Two deciduous species with low stem density, Cavanillesia platanifolia and Bursera
simaruba, had high C and high dry-season stem water potential (Ψ
stem), but differed in dry-season water released. C. platanifolia did not use stored water during the dry season whereas B. simaruba, in a drier forest, released stored water. In both, water released was highest while flushing leaves, suggesting that stored water supports leaf flushing. In contrast, two deciduous species with intermediate stem density, Annona hayesii and Genipa americana, had intermediate C, low dry-season Ψ
stem, and high seasonal change in water released. Meanwhile, two evergreen species with intermediate stem density, Cojoba rufescens and Astronium graveolens, had relatively low C, low dry-season Ψ
stem, and intermediate seasonal change in water released. Thus, at least three, distinct stored-water-use strategies were observed. Additionally, bark relative water content (RWC) decreased along with Ψ
stem during the dry season while xylem RWC did not change, suggesting that bark-stored water buffers Ψ
stem seasonally. Together these results suggest that seasonal use of stored water and change in Ψ
stem are associated with functional groups that are characterized by combinations of deciduousness and stem density.
[Show abstract][Hide abstract] ABSTRACT: Understanding variation in resource specialization is important for progress on issues that include coevolution, community assembly, ecosystem processes, and the latitudinal gradient of species richness. Herbivorous insects are useful models for studying resource specialization, and the interaction between plants and herbivorous insects is one of the most common and consequential ecological associations on the planet. However, uncertainty persists regarding fundamental features of herbivore diet breadth, including its relationship to latitude and plant species richness. Here, we use a global dataset to investigate host range for over 7,500 insect herbivore species covering a wide taxonomic breadth and interact- ing with more than 2,000 species of plants in 165 families. We ask whether relatively specialized and generalized herbivores represent a dichotomy rather than a continuum from few to many host families and species attacked and whether diet breadth changes with increasing plant species richness toward the tropics. Across geographic regions and taxonomic subsets of the data, we find that the distribution of diet breadth is fit well by a discrete, truncated Pareto power law characterized by the predominance of specialized herbivores and a long, thin tail of more generalized species. Both the taxonomic and phylogenetic distributions of diet breadth shift globally with latitude, consistent with a higher frequency of specialized insects in tropical regions. We also find that more diverse lineages of plants support assemblages of relatively more specialized herbivores and that the global distribution of plant diversity contributes to but does not fully explain the latitudinal gradient in insect herbivore specialization.
Proceedings of the National Academy of Sciences 12/2014; 112(2). DOI:10.1073/pnas.1423042112 · 9.81 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Organisms are adapted to particular habitats; consequently, community composition changes across environmental gradients, enhancing regional diversity. In Panama, a rainfall gradient correlates with the spatial turnover of tree species. While strong evidence suggests that tree species common in the wetter forests are excluded from the drier forests by seasonal drought, the factor(s) excluding drought-tolerant species, common in the drier forests, from the wetter forests remain ambiguous.Here, we show that seedlings were significantly more likely to suffer pathogen-caused damage and mortality in the wetter forest. While seedlings of dry- and wet-forest species were equally likely to suffer pathogen attack, seedlings of dry-forest species were significantly more likely to die when attacked and tended to suffer more pathogen-caused mortality overall. Furthermore, seedlings of dry-forest species suffered pathogen-caused mortality in the forest in which they do not naturally occur and in which conspecific and/or congeneric adults are absent or rare, indicating that some pathogens are relatively widespread and/or are capable of damaging multiple host species.Synthesis. Elevated risk of pathogen-caused damage and mortality in the wetter forests and a greater impact to host fitness from pathogen attack for seedlings of dry-forest species suggest that pathogens may enhance regional forest diversity by contributing to changes in tree species composition via the exclusion of dry-forest tree species from the wetter forests. This study highlights a potentially widespread and under explored mechanism by which pathogens shape plant communities at the landscape scale. An understanding of how species’ distributions are shaped by the interplay between abiotic and biotic factors is essential for conservation biology.
Journal of Ecology 11/2014; 103(1). DOI:10.1111/1365-2745.12339 · 5.69 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Plant-symbiotic fungi influence the structure and function of all terrestrial ecosystems, but factors shaping their distributions in time and space are rarely well understood. Grasses (Poaceae), which first arose and diversified in tropical forests, harbor diverse but little-studied endophytes in the lowland forests of Panama. We used sequence data for 402 isolates from two sampling years, 11 host species, and 55 microsites at Barro Colorado Island, Panama to investigate the influence of host and habitat (soil type, forest age) in shaping endophyte diversity and composition. In contrast to previous studies, we found no evidence for host- or habitat specificity. Instead, endophytes demonstrated strong spatial structure consistent with dispersal limitation, with community similarity decaying markedly over a scale of hundreds of meters. Spatial structure that is independent of host species and habitat reveals remarkable heterogeneity of endophyte–host associations at small geographic scales and adds an important spatial component to extrapolative estimates of fungal diversity.
[Show abstract][Hide abstract] ABSTRACT: Fungal endophytes - fungi that grow within plant tissues without causing immediate signs of disease - are abundant and diverse producers of bioactive secondary metabolites. Endophytes associated with leaves of tropical plants are an especially exciting and relatively untapped source of novel compounds. However, one major challenge in drug discovery lies in developing strategies to efficiently recover highly bioactive strains. As part of a 15-year drug discovery project, foliar endophytes were isolated from 3198 plant samples (51 orders, 105 families and at least 232 genera of angiosperms and ferns) collected in nine geographically distinct regions of Panama. Extracts from culture supernatants of >2700 isolates were tested for bioactivity (in vitro percent inhibition of growth, % IG) against a human breast cancer cell line (MCF-7) and the causative agents of malaria, leishmaniasis, and Chagas' disease. Overall, 32.7% of endophyte isolates were highly active in at least one bioassay, including representatives of diverse fungal lineages, host lineages, and collection sites. Up to 17% of isolates tested per assay were highly active. Most bioactive strains were active in only one assay. Fungal lineages differed in the incidence and degree of bioactivity, as did fungi from particular plant taxa, and greater bioactivity was observed in endophytes isolated from plants in cloud forests vs. lowland forests. Our results suggest that using host taxonomy and forest type to tailor plant collections, and selecting endophytes from specific orders or families for cultivation, will markedly increase the efficiency and efficacy of discovering bioactive metabolites for particular pharmaceutical targets.
PLoS ONE 09/2013; 8(9):e73192. DOI:10.1371/journal.pone.0073192 · 3.23 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Two novel reddish-orange alkaloids, mycoleptodiscin A (1) and mycoleptodiscin B (2), were isolated from liquid cultures of the endophytic fungus Mycoleptodiscus sp. that had been isolated from Desmotes incomparabilis in Panama. Elucidation of their structures was accomplished using 1D and 2D NMR spectroscopy in combination with IR spectroscopic and MS data. These compounds are indole-terpenes with a new skeleton uncommon in nature. Mycoleptodiscin B (2) was active in inhibiting the growth of cancer cell lines with IC50 values in the range 0.60-0.78 μM.
[Show abstract][Hide abstract] ABSTRACT: 1. Understanding the factors that limit species distributions along environmental gradients is a central question of ecology. Here, we evaluate the hypothesis that the traits that result in performance trade-offs between habitats contribute to the turnover of woody species along a rainfall gradient in the Isthmus of Panama. 2. We studied 24 plant species with contrasting distributions along this rainfall gradient. We measured 18 morphological and physiological traits, and three performance variables in seedlings planted in common garden experiments in two contrasting sites across the Isthmus. 3. We found evidence for a trade-off suggesting that better survival during the dry season corresponded to a lower growth rate in the forest understorey. This trade-off correlated well with the distribution of the species along the rainfall gradient and was explained mostly by variation in photosynthetic capacity. 4. While not all species fit into this trade-off, most dry-distribution species, which we had previously reported to have higher drought survival, were associated with higher stem hydraulic conductance and higher capacity for CO 2 assimilation. Our interpretation is that this combination of traits may be associated mostly with desiccation avoidance (deep roots) or desiccation delay (deciduousness) rather than desiccation tolerance. Despite their higher photosynthetic capacity, these species had lower growth in the low-light understorey, probably because of higher maintenance costs (dark respiration rates). 5. Wet-distribution species, on the other hand, had lower photosynthetic capacity and higher leaf area ratio. This strategy is typical of shade-tolerant species and may explain their higher growth rates in the low-light understorey. 6. In conclusion, our results suggest that habitat associations along the rainfall gradient in the Isthmus of Panama may result in part from a trade-off between traits that are favourable to species that avoid or delay desiccation but that otherwise limit shade tolerance. This trade-off may limit the capacity of some dry-distribution species to colonize wet forests.
[Show abstract][Hide abstract] ABSTRACT: Treefall gaps in tropical forests have a profound effect on plants growing in the understory, primarily due to increased light availability. In higher light, mature leaves typically have increased anti-herbivore defenses. However, since the majority of herbivory occurs while leaves are expanding, it is important to determine whether defense expression during the short period of leaf expansion is canalized (invariant) or plastic in response to variation in light. Therefore, we examined young leaves of Inga paraensis (Fabaceae) saplings growing along a light gradient in a terra-firme forest in Central Amazonia. We quantified leaf production and expansion time, dry mass of phenolics, saponins, and nitrogen, ants attracted to extrafloral nectaries, and leaf consumption. Over the entire light gradient, the number of leaves produced per flush increased by 50 % and the mass of phenolic compounds by 20 %, but no other traits changed. On average, 39 % of leaf area was consumed with no difference across the light gradient. Alone, none of the leaf traits was a significant predictor of leaf consumption, except for phenolics, which showed a positive relationship. Multiple regressions showed that leaf consumption was positively related to more leaves per flush and a higher concentration of phenolics in leaves. Unlike studies of mature leaves, young leaves of I. paraensis show low plasticity in defense traits across a light gradient, suggesting that leaf development is canalized.
[Show abstract][Hide abstract] ABSTRACT: Among thirty four endophytic fungal strains screened for in vitro antagonism, the endophytic fungus Cordyceps dipterigena was found to strongly inhibit mycelial growth of the plant pathogenic fungus Gibberella fujikuroi. Two new depsidone metabolites, cordycepsidone A (1) and cordycepsidone B (2), were isolated from the PDA culture extract of C. dipterigena and identified as being responsible for the antifungal activity. Elucidation of their chemical structures was carried out using 1D and 2D NMR spectroscopy in combination with IR and MS spectroscopic data. Cordycepsidone A displayed strong and dose-dependent antifungal activity against the plant pathogenic fungus Gibberella fujikuroi. The isolates were inactive in bioassays for malaria (Plasmodium falciparum), leishmaniasis (Leishmania donovani), Chagas's disease (Trypanosoma cruzi), and cytotoxicity at 10 μg/mL. The compounds were also found to be inactive against several bacterial strains at 50 μg/mL.
[Show abstract][Hide abstract] ABSTRACT: Three new terpenoids of mixed biosynthetic origin were isolated from the culture filtrate of the endophytic fungus Pycnoporus sanguineus. Their structures were determined by extensive spectroscopic analyses. We have named these tricyclic and tetracyclic metabolites ‘coibanoles A–C’ in reference to Coiba Island and Coiba National Park, Panamá, from which the plant and endophyte were collected. The extract was inactive to the human parasites Trypanosoma cruzi, Leishmania donovani, and Plasmodium falciparum at a test concentration of 10 μg/mL.
[Show abstract][Hide abstract] ABSTRACT: Chemical investigation of a new endophytic fungus, Mycosphaerella sp. nov. strain F2140, associated with the foliage of the plant Psychotria horizontalis (Rubiaceae) in Panama, resulted in the isolation of cercosporin (1) and a new cercosporin analog (3) as the major components. The structures of minor compounds in the extract were elucidated by detailed spectroscopic analysis as 2-(2-butyl)-6-ethyl-3-hydroxy-6-methylcyclohex-2-ene-1,5-dione (4), 3-(2-butyl)-6-ethyl-5-hydroxy-2-methoxy-6-methyl-cyclohex-2-enone (5), and an isomer of 5 (6). To study the influence of the hydroxy groups on the anti-parasitic activity of cercosporin, compound 1 was acetylated to obtain derivative 2. The isolated compounds 1- 6 were tested in vitro to determine their anti-parasitic activity against the causal agents of malaria (Plasmodium falciparum), leishmaniasis (Leishmania donovani), and Chagas disease (Trypanosoma cruzi). Cytotoxicity and potential anticancer activity of these compounds were evaluated using mammalian Vero cells and MCF7 cancer cell lines, respectively. Compounds 1 and 2 displayed high potency against L. donovani (IC50 0.46 and 0.64 microM), T. cruzi (IC50 1.08 and 0.78 microM), P. falciparum (IC50 1.03 and 2.99 microM), and MCF7 cancer cell lines (IC50 4.68 and 3.56 microM). Compounds 3-6 were not active in these assays at a concentration of 10 microg/mL.
[Show abstract][Hide abstract] ABSTRACT: Many plants use induced defenses to reduce the costs of antiherbivore defense. These plants invest energy in growth when herbivores are absent but shunt energy to defense when herbivores are present. In contrast, constitutive defenses are expressed continuously regardless of herbivore presence. Induction has been widely documented in temperate plants but has not been reported from tropical plants. Most tropical plants have higher, more constant herbivore pressure than temperate plants. In this situation, it is hypothesized that constitutive defenses rather than induced defense would be favored. Using natural herbivores of four species of Inga saplings on Barro Colorado Island, Panama, herbivore presence was crossed with ant presence to determine their effects on extrafloral nectar production. Analysis of nectar samples revealed that Inga species do not induce nectar production in response to herbivores. This result is not due to an inability of the plants to respond, as the plants in this study increased nectar production in response to light and ant presence. Contrary to most induction experiments with temperate ecosystem plants, these results demonstrate that tropical plants do not induce one type of defense, and they suggest that the most adaptive defense strategies are different for the two ecosystems.
[Show abstract][Hide abstract] ABSTRACT: In tropical forests, regional differences in annual rainfall correlate with differences in plant species composition. Although water availability is clearly one factor determining species distribution, other environmental variables that covary with rainfall may contribute to distributions. One such variable is light availability in the understory, which decreases towards wetter forests due to differences in canopy density and phenology. We established common garden experiments in three sites along a rainfall gradient across the Isthmus of Panama in order to measure the differences in understory light availability, and to evaluate their influence on the performance of 24 shade-tolerant species with contrasting distributions. Within sites, the effect of understory light availability on species performance depended strongly on water availability. When water was not limiting, either naturally in the wetter site or through water supplementation in drier sites, seedling performance improved at higher light. In contrast, when water was limiting at the drier sites, seedling performance was reduced at higher light, presumably due to an increase in water stress that affected mostly wet-distribution species. Although wetter forest understories were on average darker, wet-distribution species were not more shade-tolerant than dry-distribution species. Instead, wet-distribution species had higher absolute growth rates and, when water was not limiting, were better able to take advantage of small increases in light than dry-distribution species. Our results suggest that in wet forests the ability to grow fast during temporary increases in light may be a key trait for successful recruitment. The slower growth rates of the dry-distribution species, possibly due to trade-offs associated with greater drought tolerance, may exclude these species from wetter forests.
Electronic supplementary material
The online version of this article (doi:10.1007/s00442-010-1832-9) contains supplementary material, which is available to authorized users.
[Show abstract][Hide abstract] ABSTRACT: Most studies examining endophytic fungi associated with grasses (Poaceae) have focused on agronomically important species in managed ecosystems or on wild grasses in subtropical, temperate and boreal grasslands. However grasses first arose in tropical forests, where they remain a significant and diverse component of understory and forest-edge communities. To provide a broader context for understanding grass-endophyte associations we characterized fungal endophyte communities inhabiting foliage of 11 species of phylogenetically diverse C(3) grasses in the understory of a lowland tropical forest at Barro Colorado Island, Panama. Our sample included members of early-arising subfamilies of Poaceae that are endemic to forests, as well as more recently arising subfamilies that transitioned to open environments. Isolation on culture media and direct PCR and cloning revealed that these grasses harbor species-rich and phylogenetically diverse communities that lack the endophytic Clavicipitaceae known from diverse woodland and pasture grasses in the temperate zone. Both the incidence and diversity of endophytes was consistent among grass species regardless of subfamily, clade affiliation or ancestral habitat use. Genotype and phylogenetic analyses suggest that these endophytic fungi are predominantly host generalists, shared not only among distinctive lineages of Poaceae but also with non-grass plants at the same site.
[Show abstract][Hide abstract] ABSTRACT: Background/Question/Methods:
Tropical tree communities can have astounding alpha diversity, even within individual genera. For example, there are 45 species within the genus Inga (Fabaceae) alone in 25 ha of rainforest in Ecuador. Negative frequency dependence enforced by natural enemies is often cited as a process that facilitates the coexistence of tropical tree species. One of the central assumptions underlying this process is that coexisting species vary in their mechanism of defense against natural enemies, and further, we might predict that coexisting species diverge more in defense traits than in communities assembled at random. Testing these ideas requires quantifying defense traits across species. While many recent studies in tropical tree communities have focused on characterizing species for traits related to resource acquisition, few have focused on traits related to defense against natural enemies. We present one such study.
We focus on members of the diverse neotropical tree genus Inga (Fabaceae). We characterize species in French Guiana, Peru, and Panama for various traits that likely play a role in herbivore defense. We first construct a phylogeny for these species and assess how these various defense traits evolve. We than use plot inventory data to determine if coexisting species are more divergent for these defense traits than expected if communities are assembled at random.
We find evidence for a large diversity of defense syndromes within the genus. There seem to be three principal axes of defense, which are orthogonal to each other and across which species show great variation: chemical defenses, developmental defenses (e.g. rapid expansion), and ant defenses (through production of nectar at extrafloral nectaries). Furthermore, these different defense axes seem to be evolving rapidly and independently of each other. In analyses of plot data, we find that coexisting species diverge more in defense traits than expected if communities are assembled at random. This seems largely driven by differences in chemical defenses.
Our results suggest that negative frequency dependence, enforced by herbivores, may play a role in facilitating the coexistence of closely related plant species. Further work is aimed at characterizing other aspects of this process, such as whether natural enemies are indeed specializing on different species of Inga.
[Show abstract][Hide abstract] ABSTRACT: Background/Question/Methods
The arms race between herbivores and plants has lead to countless antiherbivore defenses. It is assumed that these defenses are costly and that plants have evolved to streamline their defenses so that only effective non-redundant defenses are retained. One example that has received much attention in temperate ecosystem plants is induced defense. These defenses are thought to be more adaptive because they allow plants to invest energy in growth when herbivores are absent but shunt energy to defense when herbivores are present. In contrast, constitutive defenses are expressed continuously regardless of herbivore presence. Induction has been widely document in temperate plants but has not been reported from tropical plants. The current hypothesis predicts that induction will be beneficial when herbivore pressure is intermittent with predictable cues. Most tropical plants, however, have high, constant herbivore pressure. Therefore it is predicted that plants under these circumstances should invest in constitutive defense rather than induced defense. This hypothesis was tested using the tropical tree genus Inga (Leguminosae) which utilizes chemicals and ant bodyguards to defend its leaves. Using natural herbivores of Inga saplings on Barro Colorado Island, Panama, herbivore and no-herbivore treatments were crossed with ant and no-ant treatments to determine their effects on leaf defense chemistry. Leaf samples were collected, fractionated, and quantified gravimetrically.
Chemical defenses were induced in the young leaves that experienced a range of low and high herbivore pressure, but, were constitutive in the young leaves that were constantly under higher herbivore pressure. Inga marginata induced phenolics when herbivores were present but did not induce in response to ant presence. Inga multijuga did not induce in response to any of the treatments. In the tropics, 70% of herbivory occurs on the young leaves because they are soft and full of nutrients. We suggest that because the young leaves of I. marginata expand so rapidly (less than a week) and spend such a short time in the young vulnerable state, they are unlikely to be discovered by herbivores and thus have a sufficiently low and variable herbivore pressure to make induction an adaptive strategy. In contrast, young leaves of I. multijuga are more susceptible to herbivore attack because they expand much slower (three weeks). Therefore, constitutive defenses are more adaptive for I. multijuga. These results are the first to demonstrate induced defenses in tropical trees and suggest that induced defenses are not necessarily more adaptive than constitutive defenses.