Chemical Camouflage Induced by Diet in a Pest Treehopper on Host Plants.

Ants patrol foliage and exert a strong selective pressure on herbivorous insects, being their primary predators. As ants are chemically oriented, some organisms that interact with them (myrmecophiles) use chemical strategies mediated by their cuticular hydrocarbons (CHCs) to deal with ants. Thus, a better understanding of the ecology and evolution of the mutualistic interactions between myrmecophiles and ants depends on the accurate recognition of these chemical strategies. Few studies have examined whether treehoppers may use an additional strategy called chemical camouflage to reduce ant aggression, and none considered highly polyphagous pest insects. We analyzed whether the chemical similarity of the CHC profiles of three host plants from three plant families (Fabaceae, Malvaceae, and Moraceae) and the facultative myrmecophilous honeydew-producing treehopper Aetalion reticulatum (Hemiptera: Aetalionidae), a pest of citrus plants, may play a role as a proximate mechanism serving as a protection against ant attacks on plants. We found a high similarity (>80%) between the CHCs of the treehoppers and two of their host plants. The treehoppers acquire CHCs through their diet, and the chemical similarity varies according to host plant. Chemical camouflage on host plants plays a role in the interaction of treehoppers with their ant mutualistic partners.

Green turtles shape the seascape through grazing patch formation around habitat features: Experimental evidence.

Understanding how megaherbivores incorporate habitat features into their foraging behavior is key toward understanding how herbivores shape the surrounding landscape. While the role of habitat structure has been studied within the context of predator-prey dynamics and grazing behavior in terrestrial systems, there is a limited understanding of how structure influences megaherbivore grazing in marine ecosystems. To investigate the response of megaherbivores (green turtles) to habitat features, we experimentally introduced structure at two spatial scales in a shallow seagrass meadow in The Bahamas. Turtle density increased 50-fold (to 311 turtles ha-1 ) in response to the structures, and turtles were mainly grazing and resting (low vigilance behavior). This resulted in a grazing patch exceeding the size of the experimental setup (242 m2 ), with reduced seagrass shoot density and aboveground biomass. After structure removal, turtle density decreased and vigilance increased (more browsing and shorter surfacing times), while seagrass within the patch partly recovered. Even at a small scale (9 m2 ), artificial structures altered turtle grazing behavior, resulting in grazing patches in 60% of the plots. Our results demonstrate that marine megaherbivores select habitat features as foraging sites, likely to be a predator refuge, resulting in heterogeneity in seagrass bed structure at the landscape scale.

Which variables influence the herbivory amount on Montrichardia spp. (Araceae) in aquatic ecosystems? / ¿Qué variables influyen en la herbivoría en Montrichardia spp. (Araceae) en los ecosistemas acuáticos?

Abstract Introduction: The study of herbivory is fundamental in ecology and includes how plants invest in strategies and mechanisms to reduce herbivore damage. However, there is still a lack of information about how the environment, plant density, and functional traits influence herbivory in aquatic ecosystems. Objective: To assess if there is a relationship between herbivory, environmental variables, and plant traits two species of Montrichardia, a neotropical aquatic plant. Methods: In September 2018, we studied 78 specimens of Montrichardia arborescens and 18 of Montrichardia linifera, in 18 sites in Melgaço, Pará, Brazil. On each site, we measured water depth, distance to the margin, and plant density. From plants, we measured plant height and leaf thickness, and photographed the leaves to calculate the specific leaf area and percentage herbivory. To identify anatomical structures, we collected fully expanded leaves from three individuals per quadrat. Results: For M. arborescens, plants with thicker leaves and higher specific leaf area have less herbivore damage. For M. linifera, plants from deeper sites and with thicker leaves had more herbivore damage, while plants that grew farther from the margin had less damage. We found anatomical structures related to defense, such as idioblast cells with phenolic compounds, and cells with solid inclusions that can contribute to avoiding severe damage. Conclusions: Herbivory in these Montrichardia species can be explained by a combination of plant and environmental traits (patch isolation and water depth). The main plant traits are leaf thickness and area, but chemical compounds and solid inclusions also help Montrichardia to sustain less damage than other macrophytes.

Resumen Introducción: La herbivoría es fundamental para comprender cómo las plantas invierten en diferentes estrategias para evitar la depredación, lo que implica diferentes mecanismos de defensa. Factores relacionados con el medio ambiente, la densidad de plantas y/o los rasgos funcionales de las plantas pueden influir en la herbivoría en los ecosistemas acuáticos. Sin embargo, todavía falta información sobre cómo esos factores influyen en la herbivoría en los ecosistemas acuáticos y pueden contribuir a la carga de herbivoría. Objetivo: Evaluar si existe una relación entre la herbivoría y las variables ambientales (p. ej., profundidad del agua y distancia al margen), los factores ecológicos (densidad de plantas) y los rasgos estructurales de las plantas (altura, grosor de la hoja y área foliar) e indicar estructuras anatómicas que actúen junto con los rasgos estructurales en el sistema de defensa de especies de Montrichardia. Métodos: Se evaluaron 96 individuos de Montrichardia spp. (78 de M. arborescens y 18 de M. linifera, en 18 sitios) recolectados en septiembre de 2018. En cada sitio, se midió la profundidad del agua, la distancia al margen y la densidad de plantas. De los individuos, medimos la altura de la planta, el grosor de la hoja y fotografiamos las hojas para calcular el área foliar específica y la cantidad de herbivoría (en porcentaje). Para identificar las estructuras anatómicas relacionadas con la defensa de las plantas, se recogió hojas completamente expandidas de tres individuos por cuadrante. Resultados: Para M. arborescens, las plantas con hojas más gruesas y mayor área foliar específica tienen menos daño por herbivoría. Para M. linifera, las plantas con hojas más gruesas y que habitan en sitios más profundos tienen más daño por herbívoros, mientras que las plantas más alejadas del margen tienen menos daño por herbívoros. Se encontró estructuras anatómicas relacionadas con la defensa, como células idioblásticas con compuestos fenólicos y células con inclusiones sólidas que pueden contribuir a evitar daños severos en las características de las hojas. Conclusiones: Nuestros resultados indican que la herbivoría en las especies de Montrichardia podría explicarse por una combinación de características ambientales (aislamiento del parche y profundidad del agua) y de la planta. Descubrimos que los rasgos de las hojas eran factores importantes que impulsaban los cambios en la carga de herbivoría, especialmente el grosor de las hojas y el área foliar específica. Además, las especies de Montrichardia invierten en compuestos químicos e inclusiones sólidas para evitar daños graves en las hojas y, por lo tanto, pueden sufrir menos daños que otras especies de macrófitos.

Patterns of Plumericin Concentration in Leaves of Himatanthus tarapotensis (Apocynaceae) and Its Interactions with Herbivory in the Peruvian Amazon.

We explored the concentration patterns of the bioactive metabolite plumericin produced by Himatanthus tarapotensis (Apocynaceae) under different edaphic conditions and variations in rainfall intensity, as well as its potential role in the chemical defense against insect herbivores. Values of plumericin concentration from leaves were obtained by High-Performance Liquid Chromatography, and evaluated as a function of differences in soil types, variation of precipitation, and variation of the abundance of insect herbivores, using first a Repeated Measures Correlation (rmcorr) and then a Generalized Linear Mixed Model (GLMM) analysis. Plumericin concentration is highly variable among plants, but with a significantly higher concentration in plants growing on clay soil compared to that of the white-sand soil habitat (p < 0.001). Plumericin concentration is not affected by precipitation. The caterpillar of Isognathus leachii (Lepidoptera: Sphingidae) is the most conspicuous herbivore of H. tarapotensis, and its presence is continuous but not related to plumericin concentration, probably because of its capacity to elude the chemical defense of this plant. Nevertheless, our multivariate model revealed that plumericin concentration is related to the abundance of Hymenoptera (Formicidae), and this relationship is significantly influenced by the soil parameters of carbon percentage, clay percentage, and phosphorous percentage (p < 0.001). Plumericin is a mediating agent in the interaction between H. tarapotensis and its natural environment. Variation in plumericin concentration would be induced by the abundance of Hymenoptera (Formicidae), probably as a chemical response against these insects, and by differences in soil nutrient availability.

Micronutrient Fertilizers Affect the Digestibility, Intermediary Metabolism, and Oxidative Stress in Myzus persicae (Sulzer).

The green peach aphid, Myzus persicae(Sulzer) (Hemiptera: Aphididae), is an important pest of several worldwide crops. This study evaluated the effects of plant micronutrients (alpha-iron (Fe), zinc sulfate (Zn), copper sulfate (Cu), and manganese sulfate (Mn)) on digestive enzymes, intermediary metabolism, and antioxidant responses of M. persicae reared on bell pepper plants under greenhouse conditions. Results showed that M. persicae reared on Mn-treated plants had the digestive enzymes α-amylase, trypsin, chymotrypsin, and elastase inhibited. Moreover, the aphids fed on Mn-treated plants showed the highest activities of catalase, glucose-6-phosphate dehydrogenase, superoxide dismutase, and peroxidase, and lower increase rate of malondialdehyde. These findings indicate that micronutrients can impact the aphid metabolism, which may aid control strategies against this insect pest. We raise the potential for beneficial use of foliar fertilizer application as a pest management tool that could be further evaluated on a production and economical scale, as well as with other insect pests.

Interactions of gall-formers and leaf-chewers on a tropical tree fern: evidence for non-repulsion and co-occurrence between insect guilds.

Host plant selection by herbivores is driven by a complex array of cues, including leaf traits and previous leaf damage. Herbivore-associated cues to host selection at the plant and leaf scale aid understanding of mechanisms responsible for host preference that might translate into increased performance, as well as processes structuring herbivore populations mediated by interactions. We investigated how changes induced by a galling insect in the tropical fern Cyathea phalerata act as repellent or attractant cues for sawfly feeding and the effects of leaf size on herbivory levels. We recorded gall abundance, damage by chewers, leaf size, plant nutritional quality, phenolic concentration and leaf anatomical traits between galled and non-galled leaf samples. Galled samples contained less N, higher levels of phenolics and higher C/N ratio. However, leaf-chewing damage did not differ between galled and non-galled leaves. The gall structure was avoided by chewers, as it had high concentrations of phenolics, lignification and suberization. Larger leaves sustained higher gall abundance, but leaf size did not have a significant effect on chewer damage. A co-occurrence index calculated for both guilds indicated that galls and chewers exhibited a distribution that did not differ from random, reinforcing that the two guilds on C. phalerata do not show patterns of repulsion such as those maintained by interspecific competition. Sawflies dismissing chemical cues indicate that the increase in phenolics caused by galling insects does not generate increased protection of the galled pinnules. Our results highlight ferns as key resources for herbivores and as a potential plant group to study new research avenues on plant-insect interactions.

How much leaf area do insects eat? A data set of insect herbivory sampled globally with a standardized protocol.

Herbivory is ubiquitous. Despite being a potential driver of plant distribution and performance, herbivory remains largely undocumented. Some early attempts have been made to review, globally, how much leaf area is removed through insect feeding. Kozlov et al., in one of the most comprehensive reviews regarding global patterns of herbivory, have compiled published studies regarding foliar removal and sampled data on global herbivory levels using a standardized protocol. However, in the review by Kozlov et al., only 15 sampling sites, comprising 33 plant species, were evaluated in tropical areas around the globe. In Brazil, which ranks first in terms of plant biodiversity, with a total of 46,097 species, almost half (43%) being endemic, a single data point was sampled, covering only two plant species. In an attempt to increase knowledge regarding herbivory in tropical plant species and to provide the raw data needed to test general hypotheses related to plant-herbivore interactions across large spatial scales, we proposed a joint, collaborative network to evaluate tropical herbivory. This network allowed us to update and expand the data on insect herbivory in tropical and temperate plant species. Our data set, collected with a standardized protocol, covers 45 sampling sites from nine countries and includes leaf herbivory measurements of 57,239 leaves from 209 species of vascular plants belonging to 65 families from tropical and temperate regions. They expand previous data sets by including a total of 32 sampling sites from tropical areas around the globe, comprising 152 species, 146 of them being sampled in Brazil. For temperate areas, it includes 13 sampling sites, comprising 59 species. Thus, when compared to the most recent comprehensive review of insect herbivory (Kozlov et al.), our data set has increased the base of available data for the tropical plants more than 460% (from 33 to 152 species) and the Brazilian sampling was increased 7,300% (from 2 to 146 species). Data on precise levels of herbivory are presented for more than 57,000 leaves worldwide. There are no copyright restrictions. Please cite this paper when using the current data in publications; the authors request to be informed how the data is used in the publications.

Genomic and chemical evidence for local adaptation in resistance to different herbivores in Datura stramonium.

Because most species are collections of genetically variable populations distributed to habitats differing in their abiotic/biotic environmental factors and community composition, the pattern and strength of natural selection imposed by species on each other's traits are also expected to be highly spatially variable. Here, we used genomic and quantitative genetic approaches to understand how spatially variable selection operates on the genetic basis of plant defenses to herbivores. To this end, an F2 progeny was generated by crossing Datura stramonium (Solanaceae) parents from two populations differing in their level of chemical defense. This F2 progeny was reciprocally transplanted into the parental plants' habitats and by measuring the identity by descent (IBD) relationship of each F2 plant to each parent, we were able to elucidate how spatially variable selection imposed by herbivores operated on the genetic background (IBD) of resistance to herbivory, promoting local adaptation. The results highlight that plants possessing the highest total alkaloid concentrations (sum of all alkaloid classes) were not the most well-defended or fit. Instead, specific alkaloids and their linked loci/alleles were favored by selection imposed by different herbivores. This has led to population differentiation in plant defenses and thus, to local adaptation driven by plant-herbivore interactions.

Nectar Secretion of Floral Buds of Tococa guianensis Mediates Interactions With Generalist Ants That Reduce Florivory.

The specialised mutualism between Tococa guianensis and ants housed in its leaf domatia is a well-known example of myrmecophily. A pollination study on this species revealed that flowers in the bud stage exude a sugary solution that is collected by ants. Given the presence of this unexpected nectar secretion, we investigated how, where, and when floral buds of T. guianensis secret nectar and what function it serves. We studied a population of T. guianensis occurring in a swampy area in the Cerrado of Brazil by analyzing the chemical composition and secretion dynamics of the floral-bud nectar and the distribution and ultrastructure of secretory tissues. We also measured flower damage using ant-exclusion experiments. Floral bud nectar was secreted at the tip of the petals, which lack a typical glandular structure but possess distinctive mesophyll due to the presence of numerous calcium oxalate crystals. The nectar, the production of which ceased after flower opening, was composed mainly of sucrose and low amounts of glucose and fructose. Nectar was consumed by generalist ants and sporadically by stingless bees. Ant exclusion experiments resulted in significantly increased flower damage. The floral nectar of T. guianensis is produced during the bud stage. This bud-nectar has the extranuptial function of attracting generalist ants that reduce florivory. Pollen is the unique floral resource attracting pollinators during anthesis. Tococa guianensis, thus, establishes relationships with two functional groups of ant species: specialist ants acting against herbivory and generalist ants acting against florivory.

Evolution of growth traits in invasive Pereskia aculeata (Cactaceae): testing the EICA hypothesis using its specialist herbivore, Catorhintha schaffneri (Coreidae).

BACKGROUND: Species introduced into new habitats are fitter than their native populations, as hypothesized by the 'evolution of increased competitive ability' (EICA). Here, Pereskia aculeata Miller was used as a model to test EICA and explore how 'enemy release' may have influenced the invasion success of its 400-year-old introduced populations (genotypes) compared with native populations. Plant growth traits (height and shoot length) of 15 genotypes [four from the introduced range (South Africa) and 11 from the native range (Brazil and Argentina, Venezuela and The Dominican Republic)] were assessed. Damage and impact of a shoot-feeding, sap-sucking specialist Catorhintha schaffneri Brailovsky & Garcia on ten genotypes were also compared. RESULTS: All but one of the invasive genotypes were significantly taller than native genotypes. Although the invasive genotypes were relatively more damaged by herbivory than some of the native genotypes, the observed differences were not explained completely by their origins. Nonetheless, the findings partially supported the predictions of the EICA hypothesis because invasive genotypes were generally taller than native genotypes, but did not fully support the hypothesis because they were not always more damaged than the native genotypes by C. schaffneri. CONCLUSION: Invasive genotypes had an advantage in the introduced range as they can climb neighbouring vegetation more quickly than native genotypes, but the damage incurred by the invasive genotypes relative to the native genotypes suggests only that C. schaffneri would be as damaging in South Africa, where it serves as a biocontrol agent, as it is in its native distribution in Brazil. © 2020 Society of Chemical Industry.

A comparison of inducible, ontogenetic, and interspecific sources of variation in the foliar metabolome in tropical trees.

Plant interactions with other organisms are mediated by chemistry, yet chemistry varies among conspecific and within individual plants. The foliar metabolome-the suite of small-molecule metabolites found in the leaf-changes during leaf ontogeny and is influenced by the signaling molecule jasmonic acid. Species differences in secondary metabolites are thought to play an important ecological role by limiting the host ranges of herbivores and pathogens, and hence facilitating competitive coexistence among plant species in species-rich plant communities such as tropical forests. Yet it remains unclear how inducible and ontogenetic variation compare with interspecific variation, particularly in tropical trees. Here, we take advantage of novel methods to assemble mass spectra of all compounds in leaf extracts into molecular networks that quantify their chemical structural similarity in order to compare inducible and ontogenetic chemical variation to among-species variation in species-rich tropical tree genera. We ask (i) whether young and mature leaves differ chemically, (ii) whether jasmonic acid-inducible chemical variation differs between young and mature leaves, and (iii) whether interspecific exceeds intraspecific chemical variation for four species from four hyperdiverse tropical tree genera. We observed significant effects of the jasmonic acid treatment for three of eight combinations of species and ontogenetic stage evaluated. Three of the four species also exhibited large metabolomic differences with leaf ontogenetic stage. The profound effect of leaf ontogenetic stage on the foliar metabolome suggests a qualitative turnover in secondary chemistry with leaf ontogeny. We also quantified foliar metabolomes for 45 congeners of the four focal species. Chemical similarity was much greater within than between species for all four genera, even when within-species comparisons included leaves that differed in age and jasmonic acid treatment. Despite ontogenetic and inducible variation within species, chemical differences among congeneric species may be sufficient to partition niche space with respect to chemical defense.

Ontogenetic trajectories of direct and indirect defenses of myrmecophytic plants colonized either by mutualistic or opportunistic ant species.

Myrmecophytic plants are expected to produce greater direct defenses when young and switch towards indirect defenses once they reach the size and vigor to produce enough rewards for their ant mutualists. The presence of opportunistic ant species, however, is likely to promote the variation in these ontogenetic trajectories. When plants do not obtain benefits from ants, they cannot rely on this indirect defense. Hence, the expression of direct defenses is expected to remain constant or even increase during the development of plants colonized by opportunistic ants, whereas a reduction in resource allocation to indirect defenses should be observed. To assess if myrmecophytic plants adjust their ontogenetic trajectories in defense as a function of the colonizing ant species, we estimated direct and indirect defenses at four ontogenetic stages of the myrmecophytic plant Vachellia hindsii colonized by either mutualistic or opportunistic ant partners. We report that cyanogenic potential decreased while leaf thickness and the production of sugar in extrafloral nectaries increased along plant development. The magnitude of these ontogenetic changes, however, varied as a function of the identity of the colonizing ants. As expected, when colonized by opportunistic ants, plants produced more direct defenses and reduced the production of rewards. We suggest that facultative changes in the expression of ontogenetic trajectories in direct and indirect defenses could be a mechanism to reduce the fitness costs associated with opportunistic interactions.

Herbivore performance and plant defense after sequential attacks by inducing and suppressing herbivores.

It is well known that herbivore-induced plant defenses alter host plant quality and can affect the behavior and performance of later arriving herbivores. Effects of sequential attacks by herbivores that either suppress or induce plant defenses are less well studied. We sequentially infested leaves of tomato plants with a strain of the phytophagous spider mite Tetranychus urticae that induces plant defenses and the closely related Tetranychus evansi, which suppresses plant defenses. Plant quality was quantified through oviposition of both spider mite species and by measuring proteinase inhibitor activity using plant material that had been sequentially attacked by both herbivore species. Spider-mite oviposition data show that T. evansi could suppress an earlier induction of plant defenses by T. urticae, and T. urticae could induce defenses in plants previously attacked by T. evansi in 1 day. Longer attacks by the second species did not result in further changes in oviposition. Proteinase inhibitor activity levels showed that T. evansi suppressed the high activity levels induced by T. urticae to constitutive levels in 1 day, and further suppressed activity to levels similar to those in plants attacked by T. evansi alone. Attacks by T. urticae induced proteinase inhibitor activity in plants previously attacked by T. evansi, eventually to similar levels as induced by T. urticae alone. Hence, plant quality and plant defenses were significantly affected by sequential attacks and the order of attack does not affect subsequent performance, but does affect proteinase inhibitor activity levels. Based on our results, we discuss the evolution of suppression of plant defenses.

Influence of plant resistance traits in selectiveness and species strength in a tropical plant-herbivore network.

PREMISE OF THE STUDY: Plant-herbivore networks are highly specialized in their interactions, yet they are highly variable with regard to the relative importance of specific host species for herbivores. How host species traits determine specialization and species strength in this antagonistic network is still an unanswered question that we addressed in this study. METHODS: We assessed plant cover and antiherbivore resistance traits to assess the extent to which they accounted for the variation in specialization and strength of interactions among species in a plant-herbivore network. We studied a tropical antagonistic network including a diverse herbivore-host plant assemblages in different habitat types and climatic seasons, including host plants with different life histories. KEY RESULTS: Particular combinations of leaf toughness, trichome density, and phenolic compounds influenced herbivore specialization and host species strength, but with a significant spatiotemporal variation among plant life histories. Conversely, plant-herbivore network parameters were not influenced by plant cover. CONCLUSIONS: Our study highlights the importance of species-specific resistance traits of plants to understand the ecological and evolutionary consequences of plant-herbivore interaction networks. The novelty of our research lies in the use of a trait-based approach to understand the variation observed in diverse plant-herbivore networks.

Piper kelleyi, a hotspot of ecological interactions and a new species from Ecuador and Peru.

We describe Piper kelleyi sp. nov., a new species from the eastern Andes of Ecuador and Peru, named in honor of Dr. Walter Almond Kelley. Piper kelleyi is a member of the Macrostachys clade of the genus Piper and supports a rich community of generalist and specialist herbivores, their predators and parasitoids, as well as commensalistic earwigs, and mutualistic ants. This new species was recognized as part of an ecological study of phytochemically mediated relationships between plants, herbivores, predators, and parasitoids. Compared to over 100 other Piper species surveyed, Piper kelleyi supports the largest community of specialist herbivores and parasitoids observed to date.

ResumenDescribimos la nueva especie Piper kelleyisp. nov., proveniente de la vertiente Este de los Andes en el Ecuador y Perú, y nombrada en honor al Dr. Walter Almond Kelley. Piper kelleyi forma parte del clado Macrostachys del género Piper y conforma la base alimenticia de una diversa comunidad de herbívoros, tanto generalistas como especialistas, depredadores y parasitoides de estos herbívoros, así como tijeretas comensales y hormigas mutualistas. Esta nueva especie fue reconocida como parte de una investigación ecológica de las interacciones, mediadas por fitoquímica, entre plantas, herbívoros, depredadores y parasitoides. En comparación con más de otras 100 especies de Piper estudiadas, Piper kelleyi hospeda la comunidad de insectos con mayor diversidad de herbívoros especialistas y parasitoides observada hasta ahora.

The timing of induced resistance and induced susceptibility in the soybean-Mexican bean beetle system.

Induced plant responses to herbivory have been demonstrated in many systems. It has been suggested that the timing of these responses may influence the impact of induced resistance on herbivore populations, and may affect the evolution of induced defenses. This study used a bioassay to characterize the time course of systemic induced responses to Mexican bean beetle herbivory in four genotypes of soybeans. The results suggest that the time course of induced responses in this system is more complex than most previous studies have indicated. Herbivory provoked both rapid induced resistance and subsequent induced susceptibility to beetle feeding. All four genotypes of soybean induced significant resistance to beetle damage (beetles preferred undamaged to damaged plants) by 3 days after damage. By 15 days after damage, this resistance had decayed (beetles showed no preference for undamaged over damaged plants), and by 20 days after damage, all four genotypes exhibited significant induced susceptibility (beetles preferred previously damaged plants over undamaged plants). The magnitude of induced resistance in each genotype correlated strongly with the magnitude of induced susceptibility in that genotype.