Pollen nutrition structures bee and plant community interactions.

As bees' main source of protein and lipids, pollen is critical for their development, reproduction, and health. Plant species vary considerably in the macronutrient content of their pollen, and research in bee model systems has established that this variation both modulates performance and guides floral choice. Yet, how variation in pollen chemistry shapes interactions between plants and bees in natural communities is an open question, essential for both understanding the nutritional dynamics of plant-pollinator mutualisms and informing their conservation. To fill this gap, we asked how pollen nutrition (relative protein and lipid content) sampled from 109 co-flowering plant species structured visitation patterns observed among 75 subgenera of pollen-collecting bees in the Great Basin/Eastern Sierra region (USA). We found that the degree of similarity in co-flowering plant species' pollen nutrition predicted similarity among their visitor communities, even after accounting for floral morphology and phylogeny. Consideration of pollen nutrition also shed light on the structure of this interaction network: Bee subgenera and plant genera were arranged into distinct, interconnected groups, delineated by differences in pollen macronutrient values, revealing potential nutritional niches. Importantly, variation in pollen nutrition alone (high in protein, high in lipid, or balanced) did not predict the diversity of bee visitors, indicating that plant species offering complementary pollen nutrition may be equally valuable in supporting bee diversity. Nutritional diversity should thus be a key consideration when selecting plants for habitat restoration, and a nutritionally explicit perspective is needed when considering reward systems involved in the community ecology of pollination.

Thirty-six years of butterfly monitoring, snow cover, and plant productivity reveal negative impacts of warmer winters and increased productivity on montane species.

Climate change is contributing to declines of insects through rising temperatures, altered precipitation patterns, and an increasing frequency of extreme events. The impacts of both gradual and sudden shifts in weather patterns are realized directly on insect physiology and indirectly through impacts on other trophic levels. Here, we investigated direct effects of seasonal weather on butterfly occurrences and indirect effects mediated by plant productivity using a temporally intensive butterfly monitoring dataset, in combination with high-resolution climate data and a remotely sensed indicator of plant primary productivity. Specifically, we used Bayesian hierarchical path analysis to quantify relationships between weather and weather-driven plant productivity on the occurrence of 94 butterfly species from three localities distributed across an elevational gradient. We found that snow pack exerted a strong direct positive effect on butterfly occurrence and that low snow pack was the primary driver of reductions during drought. Additionally, we found that plant primary productivity had a consistently negative effect on butterfly occurrence. These results highlight mechanisms of weather-driven declines in insect populations and the nuances of climate change effects involving snow melt, which have implications for ecological theories linking topographic complexity to ecological resilience in montane systems.

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.

A window to the world of global insect declines: Moth biodiversity trends are complex and heterogeneous.

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.

Multiple and contrasting pressures determine intraspecific phytochemical variation in a tropical shrub.

Intraspecific phytochemical variation across a landscape can cascade up trophic levels, potentially mediating the composition of entire insect communities. Surprisingly, we have little understanding of the processes that regulate and maintain phytochemical variation within species, likely because these processes are complex and operate simultaneously both temporally and spatially. To assess how phytochemistry varies within species, we tested the degree to which resource availability, contrasting soil type, and herbivory generate intraspecific chemical variation in growth and defense of the tropical shrub, Piper imperiale (Piperaceae). We quantified changes in both growth (e.g., nutritional protein, above- and below-ground biomass) and defense (e.g., imide chemicals) of individual plants using a well-replicated fully factorial shade-house experiment in Costa Rica. We found that plants grown in high light, nutrient- and richer old alluvial soil had increased biomass. High light was also important for increasing foliar protein. Thus, investment into growth was determined by resource availability and soil composition. Surprisingly, we found that chemical defenses decreased in response to herbivory. We also found that changes in plant protein were more plastic compared to plant defense, indicating that constitutive defenses may be relatively fixed, and thus an adaptation to chronic herbivory that is common in tropical forests. We demonstrate that intraspecific phytochemical variation of P. imperiale is shaped by resource availability from light and soil type. Because environmental heterogeneity occurs over small spatial scales (tens of meters), herbivores may be faced with a complex phytochemical landscape that may regulate how much damage any individual plant sustains.

Jack-of-all-trades paradigm meets long-term data: Generalist herbivores are more widespread and locally less abundant.

Insect herbivores are relatively specialized. Why this is so is not clear. We examine assumptions about associations between local abundance and dietary specialization using an 18-year data set of caterpillar-plant interactions in Ecuador. Our data consist of caterpillar-plant associations and include standardized plot-based samples and general collections of caterpillars, allowing for diet breadth and abundance estimates across spatial scales for 1917 morphospecies. We find that more specialized caterpillars are locally more abundant than generalists, consistent with a key component of the 'jack of all trades, master of none' hypothesis. As the diet breadth of species increased, generalists were not as abundant in any one location, but they had broader occupancy across the landscape, which is a pattern that could reflect high plant beta diversity and is consistent with an alternative neutral hypothesis. Our finding that more specialized species can be both rare and common highlights the ecological complexity of specialization.

Proximity to canopy mediates changes in the defensive chemistry and herbivore loads of an understory tropical shrub, Piper kelleyi.

Phytochemical traits are a key component of plant defense theory. Chemical ecology has been biased towards studying effects of individual metabolites even though effective plant defenses are comprised of diverse mixtures of metabolites. We tested the phytochemical landscape hypothesis, positing that trophic interactions are contingent upon their spatial location across a phytochemically diverse landscape. Specifically, intraspecific phytochemical changes associated with vertical strata in forests were hypothesised to affect herbivore communities of the neotropical shrub Piper kelleyi Tepe (Piperaceae). Using a field experiment, we found that phytochemical diversity increased with canopy height, and higher levels of phytochemical diversity located near the canopy were characterised by tradeoffs between photoactive and non-photoactive biosynthetic pathways. For understory plants closer to the ground, phytochemical diversity increased as direct light transmittance decreased, and these plants were characterised by up to 37% reductions in herbivory. Our results suggest that intraspecific phytochemical diversity structures herbivore communities across the landscape, affecting total herbivory.

Host plant associated enhancement of immunity and survival in virus infected caterpillars.

Understanding the interaction between host plant chemistry, the immune response, and insect pathogens can shed light on host plant use by insect herbivores. In this study, we focused on how interactions between the insect immune response and plant secondary metabolites affect the response to a viral pathogen. Based upon prior research, we asked whether the buckeye caterpillar, Junonia coenia (Nymphalidae), which specializes on plants containing iridoid glycosides (IGs), is less able to resist the pathogenic effects of a densovirus infection when feeding on plants with high concentrations of IGs. In a fully factorial design, individuals were randomly assigned to three treatments, each of which had two levels: (1) exposed to the densovirus versus control, (2) placed on a plant species with high concentrations of IGs (Plantago lanceolata, Plantaginaceae) versus low concentrations of IGs (P. major), and (3) control versus surface sterilized to exclude surface microbes that may contribute to viral resistance. We measured phenoloxidase (PO) activity, hemocyte counts, and gut bacterial diversity (16S ribosomal RNA) during the fourth larval instar, as well as development time, pupal weight, and survival to adult. Individuals infected with the virus were immune-suppressed (as measured by PO response and hemocyte count) and developed significantly faster than virus-free individuals. Contrary to our predictions,mortality was significantly less for virus challengedindividuals reared on the high IG plant compared to the low IG plant.This suggests that plant secondary metabolites can influence survival from viral infection and may be associated with activation of PO. Removing egg microbes did not affect the immune response or survival of the larvae. In summary, these results suggest that plant secondary metabolites are important for survival against a viral pathogen. Even though the PO response was better on the high IG plant, the extent to which this result contributes to survival against the virus needs further investigation.

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 genus Piper (Piperaceae). In combination with 20 years of data focused on Piper-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.

The global distribution of diet breadth in insect herbivores.

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 interacting 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.

Similarity in volatile communities leads to increased herbivory and greater tropical forest diversity.

A longstanding paradigm in ecology is that there are positive associations between herbivore diversity, specialization, and plant species diversity, with a focus on taxonomic diversity. However, phytochemical diversity is also an informative metric, as insect herbivores interact with host plants not as taxonomic entities, but as sources of nutrients, primary metabolites, and mixtures of attractant and repellant chemicals. The present research examines herbivore responses to phytochemical diversity measured as volatile similarity in the tropical genus Piper. We quantified associations between naturally occurring volatile variation and herbivory by specialist and generalist insects. Intraspecific similarity of volatile compounds across individuals was associated with greater overall herbivory. A structural equation model supported the hypothesis that plot level volatile similarity caused greater herbivory by generalists, but not specialists, which led to increased understory plant richness. These results demonstrate that using volatiles as a functional diversity metric is informative for understanding tropical forest diversity and indicate that generalist herbivores contribute to the maintenance of diversity.

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.

Intraspecific phytochemical variation shapes community and population structure for specialist caterpillars.

Chemically mediated plant-herbivore interactions contribute to the diversity of terrestrial communities and the diversification of plants and insects. While our understanding of the processes affecting community structure and evolutionary diversification has grown, few studies have investigated how trait variation shapes genetic and species diversity simultaneously in a tropical ecosystem. We investigated secondary metabolite variation among subpopulations of a single plant species, Piper kelleyi (Piperaceae), using high-performance liquid chromatography (HPLC), to understand associations between plant phytochemistry and host-specialized caterpillars in the genus Eois (Geometridae: Larentiinae) and associated parasitoid wasps and flies. In addition, we used a genotyping-by-sequencing approach to examine the genetic structure of one abundant caterpillar species, Eois encina, in relation to host phytochemical variation. We found substantive concentration differences among three major secondary metabolites, and these differences in chemistry predicted caterpillar and parasitoid community structure among host plant populations. Furthermore, E. encina populations located at high elevations were genetically different from other populations. They fed on plants containing high concentrations of prenylated benzoic acid. Thus, phytochemistry potentially shapes caterpillar and wasp community composition and geographic variation in species interactions, both of which can contribute to diversification of plants and insects.

Global weather and local butterflies: variable responses to a large-scale climate pattern along an elevational gradient.

Understanding the spatial and temporal scales at which environmental variation affects populations of plants and animals is an important goal for modern population biology, especially in the context of shifting climatic conditions. The El Niño Southern Oscillation (ENSO) generates climatic extremes of interannual variation, and has been shown to have significant effects on the diversity and abundance of a variety of terrestrial taxa. However, studies that have investigated the influence of such large-scale climate phenomena have often been limited in spatial and taxonomic scope. We used 23 years (1988-2010) of a long-term butterfly monitoring data set to explore associations between variation in population abundance of 28 butterfly species and variation in ENSO-derived sea surface temperature anomalies (SSTA) across 10 sites that encompass an elevational range of 2750 m in the Sierra Nevada mountain range of California. Our analysis detected a positive, regional effect of increased SSTA on butterfly abundance (wetter and warmer years predict more butterfly observations), yet the influence of SSTA on butterfly abundances varied along the elevational gradient, and also differed greatly among the 28 species. Migratory species had the strongest relationships with ENSO-derived SSTA, suggesting that large-scale climate indices are particularly valuable for understanding biotic-abiotic relationships of the most mobile species. In general, however, the ecological effects of large-scale climatic factors are context dependent between sites and species. Our results illustrate the power of long-term data sets for revealing pervasive yet subtle climatic effects, but also caution against expectations derived from exemplar species or single locations in the study of biotic-abiotic interactions.

Permutation tests for analyzing cospeciation in multiple phylogenies: applications in tri-trophic ecology.

There is a need for a reliable statistical test which is appropriate for assessing cospeciation of more than two phylogenies. We have developed an algorithm using a permutation method that can be used to test for and infer tri-trophic evolutionary relationships of organisms given both their phylogenies and pairwise interactions. An overall statistic has been developed based on the dominant eigenvalue of a covariance matrix, and compared to values of the statistic computed when tree labels are permuted. The resulting overall p-value is used to test for the presence or absence of cospeciation in a tri-trophic system. If cospeciation is detected, we propose new test statistics based on partial correlations to uncover more details about the relationships between multiple phylogenies. One of the strengths of our method is that it allows more parasites than hosts or more hosts than parasites, with multiple associations and more than one parasite attached to a host (or one parasite attached to multiple hosts). The new method does not require any parametric assumptions of the distribution of the data, and unlike the old methods, which utilize several pairwise steps, the overall statistic used is obtained in one step. We have applied our method to two published datasets where we obtained detailed information about the strength of associations among species with calculated partial p-values and one overall p-value from the dominant eigenvalue test statistic. Our permutation method produces reliable results with a clear procedure and statistics applied in an intuitive manner. Our algorithm is useful in testing evidence for three-way cospeciation in multiple phylogenies with tri-trophic associations and determining which phylogenies are involved in cospeciation.

Antiherbivore prenylated benzoic acid derivatives from Piper kelleyi.

The known prenylated benzoic acid derivative 3-geranyl-4-hydroxy-5-(3″,3″-dimethylallyl)benzoic acid (1) and two new chromane natural products were isolated from the methanolic extract of the leaves of Piper kelleyi Tepe (Piperaceae), a midcanopy tropical shrub that grows in lower montane rain forests in Ecuador and Peru. Structure determination using 1D and 2D NMR analysis led to the structure of the chromene 2 and to the reassignment of the structure of cumanensic acid as 4, an isomeric chromene previously isolated from Piper gaudichaudianum. The structure and relative configuration of new chromane 3 was determined using 1D and 2D NMR spectroscopic analysis and was found to be racemic by ECD spectropolarimetry. The biological activity of 1-3 was evaluated against a lab colony of the generalist caterpillar Spodoptera exigua (Noctuidae), and low concentrations of 2 and 3 were found to significantly reduce fitness. Further consideration of the biosynthetic relationship of the three compounds led to the proposal that 1 is converted to 2 via an oxidative process, whereas 3 is produced through hetero-[4+2] dimerization of a quinone methide derived from the chromene 2.

Two new species of the hyperdiverse geometrid moth genus Eois (Lepidoptera, Geometridae, Larentiinae) from Ecuador, with descriptions of early stages.

The hyperdiverse geometrid genus Eois Hübner, estimated to encompass more than 1,000 species, is among the most species-rich genera in all of Lepidoptera. While the genus has attracted considerable attention from ecologists and evolutionary biologists in recent decades, limited progress has been made on its alpha taxonomy. This contribution focuses on the Olivacea clade, whose monophyly has been recognized previously through molecular analyses. We attempt to define the clade from a morphological perspective and recognize the following species based on morphology and genomic data: E.olivacea (Felder & Rogenhofer); E.pseudolivacea Doan, sp. nov.; E.auruda (Dognin), stat. rev.; E.beebei (Fletcher, 1952), stat. rev.; E.boliviensis (Dognin), stat. rev.; and E.parumsimii Doan, sp. nov. Descriptions and illustrations of the immature stages of E.pseudolivacea reared from Piper (Piperaceae) in Ecuador are provided.

Harpacticoid copepods expand the scope and provide family-level indicators of the Deepwater Horizon oil spill deep-sea impacts.

The Deepwater Horizon (DWH) blowout and oil spill began on April 20, 2010 in the northern Gulf of Mexico (NGOM) deep sea (1525 m). Previous studies documented an impacted area of deep-sea floor totaling 321 km2 and were based on taxonomy at the macrofauna family level and the meiofauna major taxonomic level. In the present study, finer taxonomic resolution of the meiofauna community was employed, specifically harpacticoid copepod family biodiversity. Severe or moderate impacts to harpacticoid family biodiversity were observed at 35 of 95 sampling stations, covering an estimated area of 2864 km2, 8.9 times greater impacted area than previously reported. Sensitive and tolerant harpacticoid families were observed in the impact zone. The present study greatly expands the understanding of DWH deep-sea impacts in 2010 and demonstrates that the harpacticoid family-level response is the most sensitive indicator (reported to date) of this oil spill pollution event.

Host plant-mediation of viral transmission and its consequences for a native butterfly.

Pathogens play a key role in insect population dynamics, contributing to short-term fluctuations in abundance as well as long-term demographic trends. Two key factors that influence the effects of entomopathogens on herbivorous insect populations are modes of pathogen transmission and larval host plants. In this study, we examined tritrophic interactions between a sequestering specialist lepidopteran, Euphydryas phaeton, and a viral pathogen, Junonia coenia densovirus, on its native host plant, Chelone glabra, and a novel host plant, Plantago lanceolata, to explore whether host plant mediates viral transmission, survival, and viral loads. A two-factor factorial experiment was conducted in the laboratory with natal larval clusters randomly assigned to either the native or novel host plant and crossed with either uninoculated controls or viral inoculation (20% of individuals in the cluster inoculated). Diapausing clusters were overwintered in the laboratory and checked weekly for mortality. At the end of diapause, all surviving individuals were reared to adulthood to estimate survivorship. All individuals were screened to quantify viral loads, and estimate horizontal transmission postmortem. To test for vertical transmission, adults were mated, and the progeny were screened for viral presence. Within virus-treated groups, we found evidence for both horizontal and vertical transmission. Larval clusters reared on the native host plant had slightly higher horizontal transmission. Survival probability was lower in clusters feeding on the native host plant, with inoculated groups reared on the native host plant experiencing complete mortality. Viral loads did not differ by the host plant, although viral loads decreased with increased sequestration of secondary compounds on both host plants. Our results indicate that the use of a novel host plant may confer fitness benefits in terms of survival and reduced viral transmission when larvae feeding on it are infected with this pathogen, supporting hypotheses of potential evolutionary advantages of a host range expansion in the context of tritrophic interactions.

Intra- and interspecific diversity in a tropical plant clade alter herbivory and ecosystem resilience.

Declines in biodiversity generated by anthropogenic stressors at both species and population levels can alter emergent processes instrumental to ecosystem function and resilience. As such, understanding the role of biodiversity in ecosystem function and its response to climate perturbation is increasingly important, especially in tropical systems where responses to changes in biodiversity are less predictable and more challenging to assess experimentally. Using large-scale transplant experiments conducted at five neotropical sites, we documented the impacts of changes in intraspecific and interspecific plant richness in the genus Piper on insect herbivory, insect richness, and ecosystem resilience to perturbations in water availability. We found that reductions of both intraspecific and interspecific Piper diversity had measurable and site-specific effects on herbivory, herbivorous insect richness, and plant mortality. The responses of these ecosystem-relevant processes to reduced intraspecific Piper richness were often similar in magnitude to the effects of reduced interspecific richness. Increased water availability reduced herbivory by 4.2% overall, and the response of herbivorous insect richness and herbivory to water availability were altered by both intra- and interspecific richness in a site-dependent manner. Our results underscore the role of intraspecific and interspecific richness as foundations of ecosystem function and the importance of community and location-specific contingencies in controlling function in complex tropical systems.