Deciphering the ecological roles of plant secondary metabolites requires integrative studies that assess both the allocation patterns of compounds and their bioactivity in ecological interactions. Secondary metabolites have been primarily studied in leaves, but many are unique to fruits and can have numerous potential roles in interactions with both mutualists (seed dispersers) and antagonists (pathogens and predators). We described 10 alkenylphenol compounds from the plant species Piper sancti-felicis (Piperaceae), quantified their patterns of intraplant allocation across tissues and fruit development, and examined their ecological role in fruit interactions. We found that unripe and ripe fruit pulp had the highest concentrations and diversity of alkenylphenols, followed by flowers; leaves and seeds had only a few compounds at detectable concentrations. We observed a nonlinear pattern of alkenylphenol allocation across fruit development, increasing as flowers developed into unripe pulp then decreasing as pulp ripened. This pattern is consistent with the hypothesis that alkenylphenols function to defend fruits from pre-dispersal antagonists and are allocated based on the contribution of the tissue to the plant's fitness, but could also be explained by non-adaptive constraints. To assess the impacts of alkenylphenols in interactions with antagonists and mutualists, we performed fungal bioassays, field observations, and vertebrate feeding experiments. In fungal bioassays, we found that alkenylphenols had a negative effect on the growth of most fungal taxa. In field observations, nocturnal dispersers (bats) removed the majority of infructescences, and diurnal dispersers (birds) removed a larger proportion of unripe infructescences. In feeding experiments, bats exhibited an aversion to alkenylphenols, but birds did not. This observed behavior in bats, combined with our results showing a decrease in alkenylphenols during ripening, suggests that alkenylphenols in fruits represent a trade-off (defending against pathogens but reducing disperser preference). These results provide insight into the ecological significance of a little studied class of secondary metabolites in seed dispersal and fruit defense. More generally, documenting intraplant spatiotemporal allocation patterns in angiosperms and examining mechanisms behind these patterns with ecological experiments is likely to further our understanding of the evolutionary ecology of plant chemical traits.
The maintenance of biodiversity in tropical forests is thought to be dependent on fine-scale mechanisms of niche partitioning that allow species to coexist. This study examined whether three species of short-tailed fruit bat that co-occur at a lowland tropical forest site in Costa Rica (Carollia castanea, C. perspicillata, C. sowelli) avoid inter- and intraspecific competition through dietary specialization on species in the genus Piper. First, dietary composition was examined using faecal samples (N = 210), which yielded three main findings: (1) bat species and sexes vary in overall reliance on fruits of Piper, with a higher percentage of seeds of Piper detected in the diets of C. castanea (98.2%) and females (91.5%); (2) adults and juveniles partition species of Piper by habitat, with a lower percentage of mid- to late-successional species of Piper detected in adults (20.8%); and (3) overall, there is a strong dietary overlap among and within the three species of Carollia. Second, controlled choice experiments were conducted with individual bats (N = 123) to examine preferences for different species of Piper. These results indicated few differences in Piper preference based on bat species, sex, age class or reproductive status, suggesting preference is not the primary mechanism shaping the observed differences in dietary composition. Overall, the dietary composition and preference similarities suggest there is strong competition both among and within the three species of Carollia for food resources.
Specialist herbivores are thought to often enhance or maintain plant diversity within ecosystems, because they prevent their host species from becoming competitively dominant. In contrast, specialist herbivores are not generally expected to have negative impacts on non-hosts. However, we describe a cascade of indirect interactions whereby a specialist sooty mold (Scorias spongiosa) colonizes the honeydew from a specialist beech aphid (Grylloprociphilus imbricator), ultimately decreasing the survival of seedlings beneath American beech trees (Fagus grandifolia). A common garden experiment indicated that this mortality resulted from moldy honeydew impairing leaf function rather than from chemical or microbial changes to the soil. In addition, aphids consistently and repeatedly colonized the same large beech trees, suggesting that seedling-depauperate islands may form beneath these trees. Thus this highly specialized three-way beech-aphid–fungus interaction has the potential to negatively impact local forest regeneration via a cascade of indirect effects.
Climate change is a mounting global issue, but its consequences will be variable across regions. Tropical species are hypothesized to have reduced climatic adaptability and plasticity. Yet, relative to temperate species, less is understood about how they will respond to climate change. Rising temperature and atmospheric CO 2 could impact plant-herbivore systems directly by altering species traits or abundances, or the effects could be indirect by altering the strength and direction of the relationships that govern organismal strategies and interactions. Using open-top chambers in a Neotropical wet forest, we applied a full-factorial combination of active warming and CO 2 fertilization to investigate the above-ground, short-term effects of climate change on plant-herbivore interactions in a common Neotropical shrub, Piper gener alense. We aimed to answer two main questions: (1) Could climate change alter plantherbivore systems through direct effects on plant growth rate, chemical defense, and/or insect herbivore damage rate? and (2) Could climate change affect plantherbivore systems indirectly by altering (a) the strength of plant resource allocation trade-offs between growth and defense or (b) the effectiveness of plant chemicaldefense against herbivory? None of the microclimate treatments had direct effects on plant growth, chemical defense, or herbivore damage. However, we did observe a positive relationship between growth and chemical defense in treatments mimicking climate-change conditions, which partially supports the growth-differentiation balance hypothesis. We did not detect any effects of treatments on the effectiveness of plant chemical defense against herbivory. It appears that, in this system, increased CO 2 concentration and temperature may cause indirect, cascading consequences, even where direct effects are not observable. We recommend more climate-change experiments addressing multi-trophic interactions that focus not only on the direct responses of organisms but also on the ways in which climate change can restructure the relationships that govern complex biotic systems.
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