Plant Secondary Chemistry Research Articles

Variation in insect herbivory across an urbanization gradient: The role of abiotic factors and leaf secondary metabolites

Urbanization impacts plant-herbivore interactions, which are crucial for ecosystem functions such as carbon sequestration and nutrient cycling. While some studies have reported reductions in insect herbivory in urban areas (relative to rural or natural forests), this trend is not consistent and the underlying causes for such variation remain unclear. We conducted a continental-scale study on insect herbivory along urbanization gradients for three European tree species: Quercus robur, Tilia cordata, and Fraxinus excelsior, and further investigated their biotic and abiotic correlates to get at mechanisms. To this end, we quantified insect leaf herbivory and foliar secondary metabolites (phenolics, terpenoids, alkaloids) for 176 trees across eight European cities. Additionally, we collected data on microclimate (air temperature) and soil characteristics (pH, carbon, nutrients) to test for abiotic correlates of urbanization effects directly or indirectly (through changes in plant secondary chemistry) linked to herbivory. Our results showed that urbanization was negatively associated with herbivory for Q. robur and F. excelsior, but not for T. cordata. In addition, urbanization was positively associated with secondary metabolite concentrations, but only for Q. robur. Urbanization was positively associated with air temperature for Q. robur and F. excelsior, and negatively with soil nutrients (magnesium) in the case of F. excelsior, but these abiotic variables were not associated with herbivory. Contrary to expectations, we found no evidence for indirect effects of abiotic factors via plant defences on herbivory for either Q. robur or F. excelsior. Additional biotic or abiotic drivers must therefore be accounted for to explain observed urbanization gradients in herbivory and their interspecific variation.

Complementary effects of biochar, secondary metabolites, and bacteria biocontrol agents rejuvenate ratoon sugarcane traits and stimulate soil fertility

Bacteria biological control agents (BCAs) against diseases and pests are widely deemed a sustainable approach in agriculture. However, the extent to which the multifunctionality of plant secondary metabolites and BC interactions shape soil chemistry (e.g., C and N cycling enzymes) and BCAs communities in complex environments, especially under a cropping system (e.g., ratooning) prone to nutrient depletion, disease, etc., is not well established. Besides, the role metabolites-BCAs-BC interactions play in rejuvenating growth conditions necessary for ratoon sugarcane and suppressing plant pathogens/soil-borne diseases remains unclear. Here, we leveraged high-throughput sequencing and LC–MS/MS analyses to illuminate the regulatory effects of BC and plant secondary metabolites interactions on soil chemistry and BCAs communities. Additionally, we explored the roles metabolites-BCAs-BC interactions play in rejuvenating growth conditions necessary for ratoon sugarcane and suppressing plant pathogens/soil-borne diseases. Our finding revealed a pronounced rejuvenation of sugarcane ratoon traits and edaphic factors under the BC amendment soil, primarily due to the role metabolites-BCAs-BC interactions play in remediating soil fertility and health. We also proved that the BC-amended soils were worthy of enriching essential BCAs communities, including Pseudomonas, Bacillus, Streptomyces, Pantoea, Serratia, Weissella, and Leuconostoc. Abscisic aldehyde had a positive correlation with BCAs genera, including Bacillus, Pseudomonas, Serratia, Pantoea, and Ligilactobacillus. Whereas Pseudomonas, Pseudonocardia, Weissella, Bacillus, and Pantoea responded strongly and positively to jasmonic acid. Additionally, benzoate exhibited a strong positive association with BCAs genera, namely, Pseudomonas, Pseudonocardia, Weissella, Bacillus, Pantoea, and Ligilactobacillus in the different plant tissues. In the rhizosphere zone, BCAs genera such as Pseudomonas and Ligilactobacillus responded strongly to phenyllactic acid. Plant secondary metabolites, including apigenin and naringenin, demonstrated a strong positive relationship with N-cycling enzymes, including urease and phosphatase, respectively. Whereas palmitic acid, jasmonic acid, apiin, and abscisic aldehyde exhibited a significant positive correlation with soil TN, urease, pH, and AP, respectively. BugBase functional analysis confirmed that potentially pathogenic bacterial predicted phenotypes were low in the BC amendment. This work demonstrates how the multifunctionality of plant secondary metabolites-BCAs-BC interactions remediate soil fertility and suppress the presence of pathogens/parasites (e.g., Exserohilum, Aphis gossypii Glover, and Colletotrichum), thereby rejuvenating ratoon sugarcane growth and productivity.

Plant water limitation and its impact on the oviposition preferences of the monarch butterfly (Lepidoptera: Nymphalidae).

Intensifying drought conditions across the western United States due to global climate change are altering plant-insect interactions. Specialist herbivores must find their host plants within a matrix of nonhosts, and thus often rely upon specific plant secondary chemistry for host location and oviposition cues. Climate-induced alterations to plant chemistry could thus affect female selection of larval food plants. Here, we investigated whether host-plant water limitation influenced oviposition preference in a threatened invertebrate: the monarch butterfly (Danaus plexippus). We found that females deposited more eggs on reduced-water than on well-watered narrowleaf milkweed plants (Asclepias fascicularis), but we could not attribute this change to any specific change in plant chemistry. Specialist herbivores, such as the monarch butterfly, which are tightly linked to specific plant cues, may experience shift in preferences under global-change conditions. Understanding oviposition preferences will be important to directing ongoing habitat restoration activities for this declining insect.

In memoriam Klaus Kubitzki (1933–2022)

In memoriam Klaus Kubitzki (1933–2022)

Effects of Host Plants on Development and Immunity of a Generalist Insect Herbivore.

Secondary plant chemistry mediates a variety of communication signals among species, playing a fundamental role in the evolutionary diversification of communities and ecosystems. Herein, we explored diet-mediated host plant effects on development and immune response of a generalist insect herbivore. Vanessa cardui (Nymphalidae) caterpillars were reared on leaves of three host plants that vary in secondary metabolites, Plantago lanceolata (Plantaginaceae), Taraxacum officinale (Asteraceae) and Tithonia diversifolia (Asteraceae). Insect development was evaluated by larval and pupal viabilities, survivorship, and development rate. Immune response was measured as phenoloxidase (PO) activity. Additionally, chemical profiles of the host plants were obtained by liquid chromatograph-mass spectrometry (LC-MS) and the discriminant metabolites were determined using a metabolomic approach. Caterpillars reared on P. lanceolata exhibited the highest larval and pupal viabilities, as well as PO activity, and P. lanceolata leaves were chemically characterized by the presence of iridoid glycosides, phenylpropanoids and flavonoids. Taraxacum officinale leaves were characterized mainly by the presence of phenylpropanoids, flavones O-glycoside and germacranolide-type sesquiterpene lactones; caterpillars reared on this host plant fully developed to the adult stage, however they exhibited lower larval and pupal viabilities compared to individuals reared on P. lanceolata. Conversely, caterpillars reared on T. diversifolia leaves, which contain phenylpropanoids, flavones and diverse furanoheliangolide-type sesquiterpene lactones, were not able to complete larval development and exhibited the lowest PO activity. These findings suggested that V. cardui have adapted to tolerate potentially toxic metabolites occurring in P. lanceolata (iridoid glycosides), however caterpillars were not able to cope with potentially detrimental metabolites occurring in T. diversifolia (furanoheliangolides). Therefore, we suggest that furanoheliangolide-type sesquiterpene lactones were responsible for the poor development and immune response observed for caterpillars reared on T. diversifolia.

A chromosome-level genome assembly of the orange wheat blossom midge, Sitodiplosis mosellana Géhin (Diptera: Cecidomyiidae) provides insights into the evolution of a detoxification system.

The orange wheat blossom midge Sitodiplosis mosellana Géhin (Diptera: Cecidomyiidae), an economically important pest, has caused serious yield losses in most wheat-growing areas worldwide in the past half-century. A high-quality chromosome-level genome for S. mosellana was assembled using PacBio long read, Illumina short read, and Hi-C sequencing technologies. The final genome assembly was 180.69 Mb, with contig and scaffold N50 sizes of 998.71 kb and 44.56 Mb, respectively. Hi-C scaffolding reliably anchored 4 pseudochromosomes, accounting for 99.67% of the assembled genome. In total, 12,269 protein-coding genes were predicted, of which 91% were functionally annotated. Phylogenetic analysis indicated that S. mosellana and its close relative, the swede midge Contarinia nasturtii, diverged about 32.7 MYA. The S. mosellana genome showed high chromosomal synteny with the genome of Drosophila melanogaster and Anopheles gambiae. The key gene families involved in the detoxification of plant secondary chemistry were analyzed. The high-quality S. mosellana genome data will provide an invaluable resource for research in a broad range of areas, including the biology, ecology, genetics, and evolution of midges, as well as insect–plant interactions and coevolution.

Woody plant secondary chemicals increase in response to abundant deer and arrival of invasive plants in suburban forests.

Plants in suburban forests of eastern North America face the dual stressors of high white‐tailed deer density and invasion by nonindigenous plants. Chronic deer herbivory combined with strong competition from invasive plants could alter a plant's stress‐ and defense‐related secondary chemistry, especially for long‐lived juvenile trees in the understory, but this has not been studied. We measured foliar total antioxidants, phenolics, and flavonoids in juveniles of two native trees, Fraxinus pennsylvanica (green ash) and Fagus grandifolia (American beech), growing in six forests in the suburban landscape of central New Jersey, USA. The trees grew in experimental plots subjected for 2.5 years to factorial treatments of deer access/exclosure × addition/no addition of the nonindigenous invasive grass Microstegium vimineum (Japanese stiltgrass). As other hypothesized drivers of plant secondary chemistry, we also measured nonstiltgrass herb layer cover, light levels, and water availability. Univariate mixed model analysis of the deer and stiltgrass effects and multivariate structural equation modeling (SEM) of all variables showed that both greater stiltgrass cover and greater deer pressure induced antioxidants, phenolics, and flavonoids, with some variation between species. Deer were generally the stronger factor, and stiltgrass effects were most apparent at high stiltgrass density. SEM also revealed that soil dryness directly increased the chemicals; deer had additional positive, but indirect, effects via influence on the soil; in beech photosynthetically active radiation (PAR) positively affected flavonoids; and herb layer cover had no effect. Juvenile trees’ chemical defense/stress responses to deer and invasive plants can be protective, but also could have a physiological cost, with negative consequences for recruitment to the canopy. Ecological implications for species and their communities will depend on costs and benefits of stress/defense chemistry in the specific environmental context, particularly with respect to invasive plant competitiveness, extent of invasion, local deer density, and deer browse preferences.

From the leaf to the community: Distinct dimensions of phytochemical diversity shape insect–plant interactions within and among individual plants

Abstract Plant secondary chemistry is known to be an important driver of plant–insect community structure across ecological scales. Recently, the concept of phytochemical diversity (PD) has been introduced to help describe variation in plant secondary chemistry and explain how this variation affects community structure. Previous studies show that PD among individuals and species results in phytochemical mosaics, known as the phytochemical landscape. However, plant traits can vary at finer scales, such as within individuals, and even a single host plant may be perceived as an entire phytochemical landscape by an interacting insect. Using the neotropical shrub Piper amalago, we tested and compared how herbivory, caterpillar biodiversity and plant–herbivore network structure are affected by the compositional (number and concentration of compounds) and structural (diversity of distinct chemical structures) dimensions of PD. We analysed variation among individual plants and among‐plant height strata within individual plants. This allowed us to decompose PD within and among plant individuals and analyse how variation at both scales affects the plant–herbivore network. We found that both within and among plants greater structural diversity decreased herbivore feeding damage. Furthermore, each dimension of PD has different effects on herbivore biodiversity and network structure depending on the scale of biological organization. Within plants, the compositional dimension, specifically low concentrations of compounds tentatively identified as Piper amides, increased herbivore biodiversity. This dimension also increased the capacity of strata within plants to mediate ecological cascades through direct and indirect effects on herbivore abundance in the plant–herbivore network. In contrast, a greater structural diversity among plants decreased herbivore biodiversity and the capacity of plants to affect all other herbivores and plants directly and indirectly in the network. Synthesis. Based on our results we expand the concept of the phytochemical landscape to multiple scales of biological organization and provide evidence that PD may be maintained by how its multiple dimensions have distinct roles across scales of biological organization.

The draft genome of the specialist flea beetle Altica viridicyanea (Coleoptera: Chrysomelidae)

BackgroundAltica (Coleoptera: Chrysomelidae) is a highly diverse and taxonomically challenging flea beetle genus that has been used to address questions related to host plant specialization, reproductive isolation, and ecological speciation. To further evolutionary studies in this interesting group, here we present a draft genome of a representative specialist, Altica viridicyanea, the first Alticinae genome reported thus far.ResultsThe genome is 864.8 Mb and consists of 4490 scaffolds with a N50 size of 557 kb, which covered 98.6% complete and 0.4% partial insect Benchmarking Universal Single-Copy Orthologs. Repetitive sequences accounted for 62.9% of the assembly, and a total of 17,730 protein-coding gene models and 2462 non-coding RNA models were predicted. To provide insight into host plant specialization of this monophagous species, we examined the key gene families involved in chemosensation, detoxification of plant secondary chemistry, and plant cell wall-degradation.ConclusionsThe genome assembled in this work provides an important resource for further studies on host plant adaptation and functionally affiliated genes. Moreover, this work also opens the way for comparative genomics studies among closely related Altica species, which may provide insight into the molecular evolutionary processes that occur during ecological speciation.

Genome size evolution is associated with climate seasonality and glucosinolates, but not life history, soil nutrients or range size, across a clade of mustards.

We investigate patterns of evolution of genome size across a morphologically and ecologically diverse clade of Brassicaceae, in relation to ecological and life history traits. While numerous hypotheses have been put forward regarding autecological and environmental factors that could favour small vs. large genomes, a challenge in understanding genome size evolution in plants is that many hypothesized selective agents are intercorrelated. We contribute genome size estimates for 47 species of Streptanthus Nutt. and close relatives, and take advantage of many data collections for this group to assemble data on climate, life history, soil affinity and composition, geographic range and plant secondary chemistry to identify simultaneous correlates of variation in genome size in an evolutionary framework. We assess models of evolution across clades and use phylogenetically informed analyses as well as model selection and information criteria approaches to identify variables that can best explain genome size variation in this clade. We find differences in genome size and heterogeneity in its rate of evolution across subclades of Streptanthus and close relatives. We show that clade-wide genome size is positively associated with climate seasonality and glucosinolate compounds. Model selection and information criteria approaches identify a best model that includes temperature seasonality and fraction of aliphatic glucosinolates, suggesting a possible role for genome size in climatic adaptation or a role for biotic interactions in shaping the evolution of genome size. We find no evidence supporting hypotheses of life history, range size or soil nutrients as forces shaping genome size in this system. Our findings suggest climate seasonality and biotic interactions as potential forces shaping the evolution of genome size and highlight the importance of evaluating multiple factors in the context of phylogeny to understand the effect of possible selective agents on genome size.

Intraspecific trait variation in plants: a renewed focus on its role in ecological processes.

Investigating the causes and consequences of intraspecific trait variation (ITV) in plants is not novel, as it has long been recognized that such variation shapes biotic and abiotic interactions. While evolutionary and population biology have extensively investigated ITV, only in the last 10 years has interest in ITV surged within community and comparative ecology. Despite this recent interest, still lacking are thorough descriptions of ITV's extent, the spatial and temporal structure of ITV, and stronger connections between ITV and community and ecosystem properties. Our primary aim in this review is to synthesize the recent literature and ask: (1) How extensive is intraspecific variation in traits across scales, and what underlying mechanisms drive this variation? (2) How does this variation impact higher-order ecological processes (e.g. population dynamics, community assembly, invasion, ecosystem productivity)? (3) What are the consequences of ignoring ITV and how can these be mitigated? and (4) What are the most pressing research questions, and how can current practices be modified to suit our research needs? Our secondary aim is to target diverse and underrepresented traits and plant organs, including anatomy, wood, roots, hydraulics, reproduction and secondary chemistry. In addressing these aims, we showcase papers from the Special Issue. Plant ITV plays a key role in determining individual and population performance, species interactions, community structure and assembly, and ecosystem properties. Its extent varies widely across species, traits and environments, and it remains difficult to develop a predictive model for ITV that is broadly applicable. Systematically characterizing the sources (e.g. ontogeny, population differences) of ITV will be a vital step forward towards identifying generalities and the underlying mechanisms that shape ITV. While the use of species means to link traits to higher-order processes may be appropriate in many cases, such approaches can obscure potentially meaningful variation. We urge the reporting of individual replicates and population means in online data repositories, a greater consideration of the mechanisms that enhance and constrain ITV's extent, and studies that span sub-disciplines.

Micro-climatic effects on plant phenolics at the community level in a Mediterranean savanna

Research has shown that warming and drought change plant phenolics. However, much of this work has centered on the effects of individual abiotic stressors on single plant species rather than the concurrent effects of multiple stressors at the plant community level. To address this gap, we manipulated rainfall and air temperature to test for their individual and interactive effects on the expression of leaf phenolics at the community level for annual plant species occurring in two habitat types (under oak tree canopies or in open grasslands) in a Mediterranean savanna. We found that augmented temperature had a significant positive effect on the community-weighted mean of total phenolics whereas reduced rainfall had no effect. In addition, we found no evidence of interactive effects between climatic stressors and these patterns remained consistent across habitat types. Overall, this study points at increasing efforts to investigate the linkages between climate change and community-level shifts in plant secondary chemistry.

Host affinity of endophytic fungi and the potential for reciprocal interactions involving host secondary chemistry

Interactions between fungal endophytes and their host plants present useful systems for identifying important factors affecting assembly of host-associated microbiomes. Here we investigated the role of secondary chemistry in mediating host affinity of asymptomatic foliar endophytic fungi using Psychotria spp. and Theobroma cacao (cacao) as hosts. First, we surveyed endophytic communities in Psychotria species in a natural common garden using culture-based methods. Then we compared differences in endophytic community composition with differences in foliar secondary chemistry in the same host species, determined by liquid chromatography-tandem mass spectrometry. Finally, we tested how inoculation with live and heat-killed endophytes affected the cacao chemical profile. Despite sharing a common environment and source pool for endophyte spores, different Psychotria host species harbored strikingly different endophytic communities that reflected intrinsic differences in their leaf chemical profiles. In T. cacao, inoculation with live and heat-killed endophytes produced distinct cacao chemical profiles not found in uninoculated plants or pure fungal cultures, suggesting that endophytes, like pathogens, induce changes in secondary chemical profiles of their host plant. Collectively our results suggest at least two potential processes: (1) Plant secondary chemistry influences assembly and composition of fungal endophytic communities, and (2) host colonization by endophytes subsequently induces changes in the host chemical landscape. We propose a series of testable predictions based on the possibility that reciprocal chemical interactions are a general property of plant-endophyte interactions.

Modulation of above-belowground plant-herbivore interactions by entomopathogenic nematodes

Plants indirectly mediate above-belowground interactions between root- and shoot- herbivores via changes in primary and secondary metabolism. Such effects can cascade up to affect higher trophic level organisms such as predators, however, to what extent predators can in turn influence plant-mediated above-belowground interactions needs to be further elucidated. In this study, we examined the effect of entomopathogenic nematodes (EPNs) (Heterorhabditis bacteriophora and Steinernema carpocapsae) on the interactions between a belowground herbivore, the root-knot nematode (RKN) Meloidogyne arenaria, and an aboveground herbivore, the green-peach aphid Myzus persicae on tobacco (Nicotiana tabacum) plants. We found that the effect of RKNs on aphid population growth and reproduction was negative only when EPNs were inoculated near the rhizosphere. We also observed that the addition of EPNs in the rhizosphere annihilated the positive effect of the aphids on the RKNs feeding on tobacco roots. While aphids and RKNs feeding, respectively, reduced the root and shoot biomass independently of EPNs presence in the rhizosphere, the concentration of glucose and nicotine in tobacco leaves was modified by the presence of EPNs in a species-dependent manner. Our study reveals that tobacco plants detect the presence of EPNs in the rhizosphere and in turn they respond by modifying their interactions with the above- and belowground herbivores. Therefore, soil-dwelling organisms that are not directly associated with the plants can also have community-wide effects that are mediated by changes in plant primary and secondary chemistry.

Aboveground resource allocation in response to root herbivory as affected by the arbuscular mycorrhizal symbiosis

Arbuscular mycorrhizal (AM) fungi associate with the majority of terrestrial plants, influencing their growth, nutrient uptake and defence chemistry. Consequently, AM fungi can significantly impact plant-herbivore interactions, yet surprisingly few studies have investigated how AM fungi affect plant responses to root herbivores. This study aimed to investigate how AM fungi affect plant tolerance mechanisms to belowground herbivory. We examined how AM fungi affect plant (Saccharum spp. hybrid) growth, nutrient dynamics and secondary chemistry (phenolics) in response to attack from a root-feeding insect (Dermolepida albohirtum). Root herbivory reduced root mass by almost 27%. In response, plants augmented investment in aboveground biomass by 25%, as well as increasing carbon concentrations. The AM fungi increased aboveground biomass, phosphorus and carbon. Meanwhile, root herbivory increased foliar phenolics by 31% in mycorrhizal plants, and increased arbuscular colonisation of roots by 75% overall. AM fungi also decreased herbivore performance, potentially via increasing root silicon concentrations. Our results suggest that AM fungi may be able to augment plant tolerance to root herbivory via resource allocation aboveground and, at the same time, enhance plant root resistance by increasing root silicon. The ability of AM fungi to facilitate resource allocation aboveground in this way may be a more widespread strategy for plants to cope with belowground herbivory.

Plant species richness elicits changes in the metabolome of grassland species via soil biotic legacy

Abstract Species‐rich plant communities can induce unique soil biotic legacy effects through changing the abundance and composition of soil biota. These soil legacy effects can cause feedbacks to influence plant performance. In addition, soil biota can induce (defensive) secondary metabolites in shoots and roots and thus affect plant–herbivore interactions. We hypothesize that plant diversity‐driven soil biotic legacy effects elicit changes in the shoot and root metabolome. We tested this hypothesis by establishing an experiment with four plant species. We grew plants in a sterile substrate inoculated with soil conditioned by different plant species communities: (a) monocultures of either of the four species, (b) the four species in a mixture, (c) an eight species mixture including all four species or (d) a sterile inoculum. After at least 8 weeks in the field, we estimated shoot herbivory. At the same time, we took root and shoot samples for metabolomics analyses by liquid chromatography quadrupole time‐of‐flight mass spectrometry. We found that shoot and root metabolomes of all plants grown in sterile soil differed significantly from those grown in living soil. The plant metabolomes in living soils differed by species and tissue. Across all species, shoots displayed a greater richness of secondary metabolites than roots. The richness of secondary metabolites differed by species and among living soils. The conditioning species richness significantly affected the Shannon diversity of secondary metabolites in Centaurea jacea. Shoot herbivory positively correlated with the richness and Shannon diversity of secondary metabolites in Leucanthemum vulgare. We detected multiple metabolites that together explained up to 88% of the variation in herbivory in the shoots of C. jacea and Plantago lanceolata. Synthesis. Our findings suggest that plant diversity‐driven shifts in soil biota elicit changes in the composition and diversity of shoot and root secondary metabolites. However, these plant responses and their effect on shoot herbivores are species‐specific. Tracking changes in plant secondary chemistry in response to soil biotic legacy effects will help to understand the mechanisms that govern species‐specific plant–plant and plant–herbivore interactions.

Carbon dioxide‐ and temperature‐mediated changes in plant defensive compounds alter food utilization of herbivores

AbstractAlthough the impact of elevated carbon dioxide and rising temperature on plants and animals has been extensively documented recently, only limited understanding exists regarding their combined effects. The objective of this research was to address the consequences of using combinations of elevated CO2 and elevated temperature on a plant's defensive chemistry, and subsequent utilization of the plant as insect food. Our results indicated that elevated CO2 and increased temperature, for the most part, act independently on the production of defensive compounds in broccoli leaves (Brassica oleracea L. var. italica). CO2 concentrations had significant effects on the foliar water content, total phenolic compounds, polyphenol oxidase and trypsin inhibitor concentrations. The herbivore Spodoptera litura (Fabricius; Lepidoptera: Noctuidae) responded to changes in the plant secondary chemistry, with larvae consuming more plant materials that had been exposed to elevated CO2. The food utilization efficiencies of second‐instar larvae were more sensitive to CO2‐treated foliage than those of the third‐ and fourth‐instar larvae. Temperature did exert a significant effect on food utilization (ECD) by the larvae. Our study will provide important information in future predictions on plant–insect interactions as a result of climate change. The study also demonstrated that since various larval stages might respond differently to climate change, this possibility needs to be considered in future forecasting and monitoring.

Growth and defence of aspen (Populus tremula) after three seasons under elevated temperature and ultraviolet-B radiation

The predicted climate change will affect the growth and secondary chemistry of plants, but most studies only include leaves and leave out the effects on the secondary chemistry of other plant parts. In a field experiment, we studied the stem phenolic chemistry, as well as the growth of male and female genotypes, of aspen (Populus tremula L.) after three years under single (T, UVA, UVB) and combined (UVA + T, UVB + T) treatments at elevated temperature (T, +2 °C) and ultraviolet-B radiation (+30% UVB). In addition, bud mass and photosynthesis, as well as leaf rust attack and leaf herbivory, were measured. We found that elevated temperature markedly reduced concentrations of salicylates, which were the most abundant compounds among the low relative molecular mass phenolics in the stem. Elevated temperature also increased the biomass, height, and diameter of both males and females, as well as leaf area and herbivory damage in leaves. In combination with UVB, elevated temperature decreased the height of both males and females. Moreover, male buds were bigger than female buds, and females had higher chlorophyll content than males. To conclude, warming promoted growth and reduced phenolic concentration in stems of P. tremula with little difference between the sexes during the adult vegetative phase. UVB had no individual effects on any of the studied variables, implying that the plants were fairly tolerant to increased UVB levels.

Mycorrhizae Alter Toxin Sequestration and Performance of Two Specialist Herbivores

Multitrophic species interactions are shaped by both top-down and bottom-up factors. Belowground symbionts of plants, such as arbuscular mycorrhizal fungi (AMF), can alter the strength of these forces by altering plant phenotype. For example, AMF-mediated changes in foliar toxin and nutrient concentrations may influence herbivore growth and fecundity. In addition, many specialist herbivores sequester toxins from their host plants to resist natural enemies, and the extent of sequestration varies with host plant secondary chemistry. Therefore, by altering plant phenotype, AMF may affect both herbivore performance and their resistance to natural enemies. We examined how inoculation of plants with AMF influences toxin sequestration and performance of two specialist herbivores feeding upon four milkweed species (Asclepias incarnata, A. curassavica, A. latifolia, A. syriaca). We raised aphids (Aphis nerii) and caterpillars (Danaus plexippus) on plants for six days in a fully factorial manipulation of milkweed species and level of AMF inoculation (zero, medium, and high). We then assessed aphid and caterpillar sequestration of toxins (cardenolides) and performance, and measured defensive and nutritive traits of control plants. Aphids and caterpillars sequestered higher concentrations of cardenolides from plants inoculated with AMF across all milkweed species. Aphid per capita growth rates and aphid body mass varied nonlinearly with increasing AMF inoculum availability; across all milkweed species, aphids had the lowest performance under medium levels of AMF availability and highest performance under high AMF availability. In contrast, caterpillar survival varied strongly with AMF availability in a plant species-specific manner, and caterpillar growth was unaffected by AMF. Inoculation with AMF increased foliar cardenolide concentrations consistently among milkweed species, but altered aboveground biomasses and foliar phosphorous concentrations in a plant species-specific fashion. Increased herbivore sequestration of cardenolides followed AMF-mediated increases in foliar cardenolide concentrations. Aphid performance declined with increasing foliar cardenolide concentrations, while caterpillar survival increased with aboveground biomass. Our findings suggest that by altering plant phenotype, the availability of AMF in soil has the potential to influence both top-down (via sequestration) and bottom up (via plant defense and nutrition) forces that operate on herbivores.

Insect adaptations toward plant toxins in milkweed–herbivores systems – a review

AbstractStudies of plant defenses and insect herbivores have been important in the development of our understanding of coevolution and specialization. Milkweed–herbivore systems have been a model for studying plant secondary chemistry defense evolution, insect adaptations to that chemistry, and coevolution between toxic plants and their herbivores for over a century. Yet, we are only beginning to unravel the multitude of adaptations required for insect specialization on milkweed plants. We review the empirical evidence for specialist insect adaptations toward milkweed toxins, coevolution between insects and milkweed plants, and canonical paradigms for sequestration and highlight the areas for further research. By comparing research performed with diverse milkweed insects, we discuss the need to comprehensively study adaptations and specialization in divergent insect taxa.