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.

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.

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.

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.

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.

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.

Larissimusnigricans sp. nov. (Hymenoptera, Braconidae), a new reared species of a rare neotropical genus recovered through biodiversity inventory in Ecuador.

A new species of the rarely collected neotropical microgastrine braconid wasp genus Larissimus Nixon, represented previously by only a single described species, L.cassander Nixon, was recovered by the Caterpillars and Parasitoids of the Eastern Andes in Ecuador inventory project. Larissimusnigricanssp. nov. was reared from an unidentified species of arctiine Erebidae feeding on the common bamboo species Chusqueascandens Kunth at the Yanayacu Biological Station near Cosanga, Napo Province, Ecuador. The new species is described and diagnosed from L.cassander using both morphological and DNA barcode data.

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.

Extreme drought disrupts plant phenology: Insights from 35 years of cloud forest data in Venezuela.

The potential effects of climate change on plant reproductive phenology include asynchronies with pollinators and reductions in plant fitness, leading to extinction and loss of ecosystem function. In particular, plant phenology is sensitive to extreme weather events, which are occurring with increasing severity and frequency in recent decades and are linked to anthropogenic climate change and shifts in atmospheric circulation. For 15 plant species in a Venezuelan cloud forest, we documented dramatic changes in monthly flower and fruit community composition over a 35-year time series, from 1983 to 2017, and these changes were linked directly to higher temperatures, lower precipitation, and decreased soil water availability. The patterns documented here do not mirror trends in temperate zones but corroborate results from the Asian tropics. More intense droughts are predicted to occur in the region, which will cause dramatic changes in flower and fruit availability.

The chemical ecology of tropical forest diversity: Environmental variation, chemical similarity, herbivory, and richness.

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 (1 H-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.

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.

Phytochemistry reflects different evolutionary history in traditional classes versus specialized structural motifs.

Foundational hypotheses addressing plant-insect codiversification and plant defense theory typically assume a macroevolutionary pattern whereby closely related plants have similar chemical profiles. However, numerous studies have documented variation in the degree of phytochemical trait lability, raising the possibility that phytochemical evolution is more nuanced than initially assumed. We utilize proton nuclear magnetic resonance (1H NMR) data, chemical classification, and double digest restriction-site associated DNA sequencing (ddRADseq) to resolve evolutionary relationships and characterize the evolution of secondary chemistry in the Neotropical plant clade Radula (Piper; Piperaceae). Sequencing data substantially improved phylogenetic resolution relative to past studies, and spectroscopic characterization revealed the presence of 35 metabolite classes. Metabolite classes displayed phylogenetic signal, whereas the crude 1H NMR spectra featured little evidence of phylogenetic signal in multivariate tests of chemical resonances. Evolutionary correlations were detected in two pairs of compound classes (flavonoids with chalcones; p-alkenyl phenols with kavalactones), where the gain or loss of a class was dependent on the other's state. Overall, the evolution of secondary chemistry in Radula is characterized by strong phylogenetic signal of traditional compound classes and weak phylogenetic signal of specialized chemical motifs, consistent with both classic evolutionary hypotheses and recent examinations of phytochemical evolution in young lineages.

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.

Secondary metabolites in a neotropical shrub: spatiotemporal allocation and role in fruit defense and dispersal.

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.

Macrophyte Diversity and Complexity Reduce Larval Mosquito Abundance.

The role of aquatic arthropod diversity and community interactions of larval mosquitoes are important for understanding mosquito population dynamics. We tested the effects of aquatic macrophyte diversity and habitat structural complexity in shaping the predator and competitor invertebrate communities associated with mosquito larvae. Experimental mesocosms were planted with live aquatic macrophytes and allowed to be naturally colonized by local invertebrates. Results indicated a positive effect of macrophyte diversity on competitor diversity and a negative effect on predator diversity. In turn, predator diversity negatively impacted mosquito abundance through a direct effect, while competitor diversity showed an indirect negative effect on mosquito larval abundance through its positive effect on predator diversity. The enhancement of aquatic macrophyte diversity and structural complexity has practical applications for the reduction of mosquito populations in managed systems where complete source elimination is not possible.

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.

A species-level taxonomic review and host associations of Glyptapanteles (Hymenoptera, Braconidae, Microgastrinae) with an emphasis on 136 new reared species from Costa Rica and Ecuador.

The descriptive taxonomic study reported here is focused on Glyptapanteles, a species-rich genus of hymenopteran parasitoid wasps. The species were found within the framework of two independent long-term Neotropical caterpillar rearing projects: northwestern Costa Rica (Área de Conservación Guanacaste, ACG) and eastern Andes, Ecuador (centered on Yanayacu Biological Station, YBS). One hundred thirty-six new species of Glyptapanteles Ashmead are described and all of them are authored by Arias-Penna. None of them was recorded in both countries; thus, 78 are from Costa Rica and the remaining 58 from Ecuador. Before this revision, the number of Neotropical described Glyptapanteles did not reach double digits. Reasonable boundaries among species were generated by integrating three datasets: Cytochrome Oxidase I (COI) gene sequencing data, natural history (host records), and external morphological characters. Each species description is accompanied by images and known geographical distribution. Characteristics such as shape, ornamentation, and location of spun Glyptapanteles cocoons were imaged as well. Host-parasitoid associations and food plants are also here published for the first time. A total of 88 species within 84 genera in 15 Lepidoptera families was encountered as hosts in the field. With respect to food plants, these wild-caught parasitized caterpillars were reared on leaves of 147 species within 118 genera in 60 families. The majority of Glyptapanteles species appeared to be relatively specialized on one family of Lepidoptera or even on some much lower level of taxonomic refinement. Those herbivores in turn are highly food-plant specialized, and once caterpillars were collected, early instars (1-3) yielded more parasitoids than later instars. Glyptapanteles jimmilleri Arias-Penna, sp. nov. is the first egg-larval parasitoid recorded within the genus, though there may be many more since such natural history requires a more focused collection of eggs. The rate of hyperparasitoidism within the genus was approximately 4% and was represented by Mesochorus spp. (Ichneumonidae). A single case of multiparasitoidism was reported, Copidosoma floridanum Ashmead (Encyrtidae) and Glyptapanteles ilarisaaksjarvi Arias-Penna, sp. nov. both parasitoid species emerged from the caterpillar of Noctuidae: Condica cupienta (Cramer). Bodyguard behavior was observed in two Glyptapanteles species: G. howelldalyi Arias-Penna, sp. nov. and G. paulhansoni Arias-Penna, sp. nov. A dichotomous key for all the new species is provided. The numerous species described here, and an equal number already reared but not formally described, signal a far greater Glyptapanteles species richness in the Neotropics than suggested by the few described previously.

Challenges and advances in the study of latitudinal gradients in multitrophic interactions, with a focus on consumer specialization.

Increases in data availability and geographic ranges of studies have allowed for more thorough tests of latitudinal gradients in trophic interactions, with numerous recent studies testing hypotheses that strength of interactions, herbivory, plant chemical defense, and dietary specialization all increase with decreasing latitude. We review the issues surrounding these latitudinal gradients, discuss some methodological challenges, and provide some caveats relevant to inferences from existing approaches. To examine some potential issues with studies on latitudinal gradients in dietary specialization, we simulate a latitudinal gradient of communities that increase in diversity and specialization towards the equator then test the power of different sampling designs for detecting the gradient. Based on this simple simulation, as well as apparent incongruities in the literature, we conclude that subtle differences in sampling design can be responsible for failure to detect existing gradients. Despite calls for rejecting some latitudinal gradient hypotheses, it is clear that a great deal of careful research remains to determine important correlates of the well-established latitudinal gradient in diversity. In particular, future studies should focus on replicated gradients, greater emphasis on continuous sampling, and use of taxonomic controls that allow for meaningful analyses across latitudes.