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A window to the world of global insect declines
Moths are the most taxonomically and ecologically diverse insect taxon for which there exist considerable time-series abundance data. There is an alarming record of decreases in moth abundance and diversity from across Europe, with rates varying markedly among and within regions. Recent reports from Costa Rica reveal steep cross-lineage declines of caterpillars, while other sites (Ecuador and Arizona, reported here) show no or only modest long-term decreases over the past two decades. Rates of decline for dietary and ecological specialists are steeper than those for ecologically generalized taxa. Additional traits commonly associated with elevated risks include large wingspans, small geographic ranges, low dispersal ability, and univoltinism; taxa associated with grasslands, aridlands, and nutrient-poor habitats also appear to be at higher risk. In temperate areas, many moth taxa limited historically by abiotic factors are increasing in abundance and range. We regard the most important continental-scale stressors to include reductions in habitat quality and quantity resulting from land-use change and climate change and, to a lesser extent, atmospheric nitrification and introduced species. Site-specific stressors include pesticide use and light pollution. Our assessment of global macrolepidopteran population trends includes numerous cases of both region-wide and local losses and studies that report no declines. Spatial variation of reported losses suggests that multiple stressors are in play. With the exception of recent reports from Costa Rica, the most severe examples of moth declines are from Northern Hemisphere regions of high human-population density and intensive agriculture.
Journal Article
Costs of Defense and a Test of the Carbon-Nutrient Balance and Growth-Differentiation Balance Hypotheses for Two Co-Occurring Classes of Plant Defense
One of the goals of chemical ecology is to assess costs of plant defenses. Intraspecific trade-offs between growth and defense are traditionally viewed in the context of the carbon-nutrient balance hypothesis (CNBH) and the growth-differentiation balance hypothesis (GDBH). Broadly, these hypotheses suggest that growth is limited by deficiencies in carbon or nitrogen while rates of photosynthesis remain unchanged, and the subsequent reduced growth results in the more abundant resource being invested in increased defense (mass-balance based allocation). The GDBH further predicts trade-offs in growth and defense should only be observed when resources are abundant. Most support for these hypotheses comes from work with phenolics. We examined trade-offs related to production of two classes of defenses, saponins (triterpenoids) and flavans (phenolics), in Pentaclethra macroloba (Fabaceae), an abundant tree in Costa Rican wet forests. We quantified physiological costs of plant defenses by measuring photosynthetic parameters (which are often assumed to be stable) in addition to biomass. Pentaclethra macroloba were grown in full sunlight or shade under three levels of nitrogen alone or with conspecific neighbors that could potentially alter nutrient availability via competition or facilitation. Biomass and photosynthesis were not affected by nitrogen or competition for seedlings in full sunlight, but they responded positively to nitrogen in shade-grown plants. The trade-off predicted by the GDBH between growth and metabolite production was only present between flavans and biomass in sun-grown plants (abundant resource conditions). Support was also only partial for the CNBH as flavans declined with nitrogen but saponins increased. This suggests saponin production should be considered in terms of detailed biosynthetic pathway models while phenolic production fits mass-balance based allocation models (such as the CNBH). Contrary to expectations based on the two defense hypotheses, trade-offs were found between defenses and photosynthesis, indicating that studies of plant defenses should include direct measures of physiological responses.
Journal Article
Does plant apparency matter? Thirty years of data provide limited support but reveal clear patterns of the effects of plant chemistry on herbivores
According to the plant-apparency hypothesis, apparent plants allocate resources to quantitative defenses that negatively affect generalist and specialist herbivores, while unapparent plants invest more in qualitative defenses that negatively affect nonadapted generalists. Although this hypothesis has provided a useful framework for understanding the evolution of plant chemical defense, there are many inconsistencies surrounding associated predictions, and it has been heavily criticized and deemed obsolete.
We used a hierarchical Bayesian meta-analysis model to test whether defenses from apparent and unapparent plants differ in their effects on herbivores. We collected a total of 225 effect sizes from 158 published papers in which the effects of plant chemistry on herbivore performance were reported.
As predicted by the plant-apparency hypothesis, we found a prevalence of quantitative defenses in woody plants and qualitative defenses in herbaceous plants. However, the detrimental impacts of qualitative defenses were more effective against specialists than generalists, and the effects of chemical defenses did not significantly differ between specialists and generalists for woody or herbaceous plants.
A striking pattern that emerged from our data was a pervasiveness of beneficial effects of secondary metabolites on herbivore performance, especially generalists. This pattern provides evidence that herbivores are evolving effective counteradaptations to putative plant defenses.
Journal Article
Phytochemical diversity drives plant–insect community diversity
What are the ecological causes and consequences of variation in phytochemical diversity within and between plant taxa? Despite decades of natural products discovery by organic chemists and research by chemical ecologists, our understanding of phytochemically mediated ecological processes in natural communities has been restricted to studies of either broad classes of compounds or a small number of well-characterized molecules. Until now, no studies have assessed the ecological causes or consequences of rigorously quantified phytochemical diversity across taxa in natural systems. Consequently, hypotheses that attempt to explain variation in phytochemical diversity among plants remain largely untested. We use spectral data from crude plant extracts to characterize phytochemical diversity in a suite of co-occurring plants in the tropical genusPiper(Piperaceae). In combination with 20 years of data focused onPiper-associated insects, we find that phytochemical diversity has a direct and positive effect on the diversity of herbivores but also reduces overall herbivore damage. Elevated chemical diversity is associated with more specialized assemblages of herbivores, and the cascading positive effect of phytochemistry on herbivore enemies is stronger as herbivore diet breadth narrows. These results are consistent with traditional hypotheses that predict positive associations between plant chemical diversity, insect herbivore diversity, and trophic specialization. It is clear from these results that high phytochemical diversity not only enhances the diversity of plant-associated insects but also contributes to the ecological predominance of specialized insect herbivores.
Journal Article
Multidimensional diversity associated with plants
There are substantive ethical and aesthetic concerns about current anthropogenic losses of species, but there is also the academic issue: When we lose the tangled bank and all of its component species and interactions, we risk losing much of the inspiration and foundation of scientific inquiry into diversity. Understanding and documenting loss of biodiversity is a major priority for botanists, and more generally for biologists and includes all attempts to document and predict the consequences of continued habitat loss, fragmentation, invasive species, and climate change. Here, Dyer makes the case for continued development of two integrated measures of biodiversity, \"interaction diversity\", and \"phytochemical diversity\", with a focus on how richness and abundance (frequency) of chemically mediated multitrophic interactions vary across different scales. This focus on the number of unique interactions (richness) rather than species should increase understanding of relationships between biodiversity and ecosystem function.
Journal Article
Loss of dominant caterpillar genera in a protected tropical forest
Reports of biodiversity loss have increasingly focused on declines in abundance and diversity of insects, but it is still unclear if substantive insect diversity losses are occurring in intact low-latitude forests. We collected 22 years of plant-caterpillar-parasitoid data in a protected tropical forest and found reductions in the diversity and density of insects that appear to be partly driven by a changing climate and weather anomalies. Results also point to the potential influence of variables not directly measured in this study, including changes in land-use in nearby areas. We report a decline in parasitism that represents a reduction in an important ecosystem service: enemy control of primary consumers. The consequences of these changes are in many cases irreversible and are likely to be mirrored in nearby forests; overall declines in the region will have negative consequences for surrounding agriculture. The decline of important tropical taxa and associated ecosystem function illuminates the consequences of numerous threats to global insect diversity and provides additional impetus for research on tropical diversity.
Journal Article
Effects of CO2 and Temperature on Tritrophic Interactions
There has been a significant increase in studies of how global change parameters affect interacting species or entire communities, yet the combined or interactive effects of increased atmospheric CO2 and associated increases in global mean temperatures on chemically mediated trophic interactions are mostly unknown. Thus, predictions of climate-induced changes on plant-insect interactions are still based primarily on studies of individual species, individual global change parameters, pairwise interactions, or parameters that summarize communities. A clear understanding of community response to global change will only emerge from studies that examine effects of multiple variables on biotic interactions. We examined the effects of increased CO2 and temperature on simple laboratory communities of interacting alfalfa, chemical defense, armyworm caterpillars, and parasitoid wasps. Higher temperatures and CO2 caused decreased plant quality, decreased caterpillar development times, developmental asynchrony between caterpillars and wasps, and complete wasp mortality. The effects measured here, along with other effects of global change on natural enemies suggest that biological control and other top-down effects of insect predators will decline over the coming decades.
Journal Article
Effects of climate change on Lepidoptera pollen loads and their pollination services in space and time
Shifts in flowering time among plant communities as a result of climate change, including extreme weather events, are a growing concern. These plant phenological changes may affect the quantity and quality of food sources for specialized insect pollinators. Plant–pollinator interactions are threatened by habitat alterations and biodiversity loss, and changes in these interactions may lead to declines in flower visitors and pollination services. Most prior research has focused on short-term plant–pollinator interactions, which do not accurately capture changes in pollination services. Here, we characterized long-term plant–pollinator interactions and identified potential risks to specialized butterfly species due to habitat loss, fragmented landscapes, and changes in plant assemblages. We used 21 years of historical data from museum specimens to track the potential effects of direct and indirect changes in precipitation, temperature, monsoons, and wildfires on plant–pollinator mutualism in the Great Basin and Sierra Nevada. We found decreased pollen richness associated with butterflies within sites, as well as an increase in pollen grain abundance of drought-tolerant plants, particularly in the past 10 years. Moreover, increased global temperatures and the intensity and frequency of precipitation and wildfires were negatively correlated with pollen diversity. Our findings have important implications for understanding plant–pollinator interactions and the pollination services affected by global warming.
Journal Article
The chemical ecology of tropical forest diversity
Species richness in tropical forests is correlated with other dimensions of diversity, including the diversity of plant–herbivore interactions and the phytochemical diversity that influences those interactions. Understanding the complexity of plant chemistry and the importance of phytochemical diversity for plant—insect interactions and overall forest richness has been enhanced significantly by the application of metabolomics to natural systems. The present work used proton nuclear magnetic resonance spectroscopy (¹H-NMR) profiling of crude leaf extracts to study phytochemical similarity and diversity among Piper plants growing naturally in the Atlantic Rainforest of Brazil. Spectral profile similarity and chemical diversity were quantified to examine the relationship between metrics of phytochemical diversity, specialist and generalist herbivory, and understory plant richness. Herbivory increased with understory species richness, while generalist herbivory increased and specialist herbivory decreased with the diversity of Piper leaf material available. Specialist herbivory increased when conspecific host plants were more spectroscopically dissimilar. Spectral similarity was lower among individuals of common species, and they were also more spectrally diverse, indicating phytochemical diversity is beneficial to plants. Canopy openness and soil nutrients also influenced chemistry and herbivory. The complex relationships uncovered in this study add information to our growing understanding of the importance of phytochemical diversity for plant—insect interactions and tropical plant species richness.
Journal Article