Community heterogeneity and the evolution of interactions between plants and insect herbivores

Plant communities vary tremendously in terms of productivity, species diversity, and genetic diversity within species. This vegetation heterogeneity can impact both the likelihood and strength of interactions between plants and insect herbivores. Because altering plant-herbivore interactions will likely impact the fitness of both partners, these ecological effects also have evolutionary consequences. We review several hypothesized and well-documented mechanisms whereby variation in the plant community alters the plant-herbivore interaction, discuss potential evolutionary outcomes of each of these ecological effects, and conclude by highlighting several avenues for future research. The underlying theme of this review is that the neighborhood of plants is an important determinant of insect attack, and this results in feedback effects on the plant community. Because plants exert selection on herbivore traits and, reciprocally, herbivores exert selection on plant-defense traits, variation in the plant community likely contributes to spatial and temporal variation in both plant and insect traits, which could influence macroevolutionary patterns.     

Climate change triggers effects of fungal pathogens and insect herbivores on litter decomposition

Increasing infestation by insect herbivores and pathogenic fungi in response to climate change will inevitably impact the amount and quality of leaf litter inputs into the soil. However, little is known on the interactive effect of infestation severity and climate change on litter decomposition, and no such study has been published for deciduous forests in Central Europe. We assessed changes in initial chemical quality of beech (Fagus sylvatica L.) and maple litter (Acer platanoides L.) in response to infestation by the gall midge Mikiola fagi Hart. and the pathogenic fungus Sawadaea tulasnei Fuckel, respectively, and investigated interactive effects of infestation severity, changes in temperature and soil moisture on carbon mineralization in a short-term laboratory study. We found that infestation by the gall midge M. fagi and the pathogenic fungus S. tulasnei significantly changed the chemical quality of beech and maple litter. Changes in element concentrations were generally positive and more pronounced, and if negative less pronounced for maple than beech litter most likely due to high quality fungal tissue remaining on litter after abscission. More importantly, alterations in litter chemical quality did not translate to distinct patterns of carbon mineralization at ambient conditions, but even low amounts of infested litter accelerated carbon mineralization at moderately increased soil moisture and in particular at higher temperature. Our results indicate that insect herbivores and fungal pathogens can markedly alter initial litter chemical quality, but that afterlife effects on carbon mineralization depend on soil moisture and temperature, suggesting that increased infestation severity under projected climate change potentially increases soil carbon release in deciduous forests in Central Europe.     

Tri-trophic level interactions affect host plant development and abundance of insect herbivores

Understanding the interactions among plants, hemipterans, and ants has provided numerous insights into a range of ecological and evolutionary processes. In these systems, however, studies concerning the isolated direct and indirect effects of aphid colonies on host plant and other herbivores remain rare at best. The aphid Uroleucon erigeronensis forms dense colonies on the apical shoots of the host plant Baccharis dracunculilfolia (Asteraceae). The honeydew produced by these aphids attracts several species of ants that might interfere with other herbivores. Four hypotheses were tested in this system: (1) ants tending aphids reduce the abundance of other herbivores; (2) the effects of ants and aphids upon herbivores differ between chewing and fluid-sucking herbivores; (3) aphids alone reduce the abundance of other herbivores; and (4), the aphid presence negatively affects B. dracunculifolia shoot growth. The hypotheses were evaluated with ant and aphid exclusion experiments, on isolated plant shoots, along six consecutive months. We adjusted linear mixed-effects models for longitudinal data (repeated measures), with nested spatial random effect. The results showed that: (1) herbivore abundance was lower on shoots with aphids than on shoots without aphids, and even lower on shoots with aphids and ants; (2) both chewing and fluid-sucking insects responded similarly to the treatment, and (3) aphid presence affected negatively B. dracunculifolia shoot growth. Thus, since aphids alone changed plant growth and the abundance of insect herbivores, we suggest that the ant–aphid association is important to the organization of the system B. dracunculifolia-herbivorous insects.     

Constitutive plant toxins and their role in defense against herbivores and pathogens

Most recent investigations have focused on induced, rather than constitutive, plant defenses. Yet significant research has helped to illuminate some of the principal characteristics of constitutive defenses, including mechanisms of action and synergistic effects, as well as strategies used by herbivores and pathogens to circumvent them.     

Mechanisms and ecological implications of plant-mediated interactions between belowground and aboveground insect herbivores

Plant-mediated interactions between belowground (BG) and aboveground (AG) herbivores have received increasing interest recently. However, the molecular mechanisms underlying ecological consequences of BG–AG interactions are not fully clear yet. Herbivore-induced plant defenses are complex and comprise phytohormonal signaling, gene expression and production of defensive compounds (defined here as response levels), each with their own temporal dynamics. Jointly they shape the response that will be expressed. However, because different induction methods are used in different plant-herbivore systems, and only one or two response levels are measured in each study, our ability to construct a general framework for BG–AG interactions remains limited. Here we aim to link the mechanisms to the ecological consequences of plant-mediated interactions between BG and AG insect herbivores. We first outline the molecular mechanisms of herbivore-induced responses involved in BG–AG interactions. Then we synthesize the literature on BG–AG interactions in two well-studied plant-herbivore systems, Brassica spp. and Zea mays, to identify general patterns and specific differences. Based on this comprehensive review, we conclude that phytohormones can only partially mimic induction by real herbivores. BG herbivory induces resistance to AG herbivores in both systems, but only in maize this involves drought stress responses. This may be due to morphological and physiological differences between monocotyledonous (maize) and dicotyledonous (Brassica) species, and differences in the feeding strategies of the herbivores used. Therefore, we strongly recommend that future studies explicitly account for these basic differences in plant morphology and include additional herbivores while investigating all response levels involved in BG–AG interactions.     

The role of plant resistance and tolerance to herbivory in mediating the effects of introduced herbivores

While the generally negative consequences of introduced species are well known, little is appreciated on the role of the evolutionary history of plants with herbivores in mediating the indirect impacts of herbivory. We examined how variation in plant resistance and tolerance traits can mediate the effects of herbivory and can have differential indirect impacts on other species and processes. We used two examples of a native and an introduced herbivore, Castor canadensis (American beaver) and Cervus elaphus (Rocky Mountain elk) with Populus spp. to test a conceptual model regarding possible outcomes of species interactions with native and exotic mammalian herbivores. Using these two herbivore test cases, we make two predictions to create testable hypotheses across systems and taxa: First, adaptive traits of tolerance or resistance to herbivory will be fewer when exotic species feed on plant species with which they have no evolutionary history. Second, historical constraints of species interactions will allow for negative feedbacks to stabilize the effects of herbivory by a native species. Overall, these two case studies illustrate that plant resistance and tolerance traits can mediate the indirect consequences of herbivory on associated interacting species. Specifically, when there is no evolutionary history between the plants and herbivores, which is often the case with species introductions, the effects of herbivory are more likely to reduce genetic variation and habitat mosaics, thus indirectly affecting associated species.     

Airborne interactions between undamaged plants of different cultivars affect insect herbivores and natural enemies

This study investigated the effects of airborne interaction between different barley cultivars on the behaviour of bird cherry-oat aphid Rhopalosiphum padi, the ladybird Coccinella septempunctata and the parasitoid Aphidius colemani. In certain cultivar combinations, exposure of one cultivar to air passed over a different cultivar caused barley to have reduced aphid acceptance and increased attraction of ladybirds and parasitoids. Parasitoids attacked aphids that had developed on plants under exposure more often than those from unexposed plants, leading to a higher parasitisation rate. Ladybirds, but not parasitoids, were more attracted to combined odours from certain barley cultivars than either cultivar alone. The results show that airborne interactions between undamaged plants can affect higher trophic levels, and that odour differences between different genotypes of the same plant species may be sufficient to affect natural enemy behaviour.     

The effect of nutrients on pyrrolizidine alkaloids in Senecio plants and their interactions with herbivores and pathogens

The aim of this review is to combine the knowledge of studies on effects of nutrients on pyrrolizidine alkaloids (PAs) in Senecio with those studies of effects of PAs on herbivores and pathogens in order to predict the effects that nutrients may have on herbivores and pathogens via changes in PAs. We discuss whether these predictions match with the outcome of studies where the effect of nutrients on herbivores and insects were measured. PA concentrations in S. jacobaea, S. vulgaris and S. aquaticus were mostly reduced by NPK fertilization, with genotype-specific effects occurring. Plant organs varied in their response to increased fertilization; PA concentrations in flowers remained constant, while shoot and roots were mostly negatively affected. Biomass change is probably largely responsible for the change in concentrations. Nutrients affect both the variety and the levels of PAs in the plant. The reduced PA concentrations after NPK fertilization was expected to benefit herbivores, but no or negative responses from insect herbivores were observed. Apparently other changes in the plant after fertilization are overriding the effect of PAs. Pathogens do seem to benefit from the lower PA concentrations after fertilization; they were more detrimental to fertilized plants than to unfertilized control plants. Future studies should include the effect of each element of nutrients separately and in combinations in order to gain more insight in the effect of specific nutrients on PA content in Senecio plants.     

Fire effects on insect herbivores in an oak savanna: the role of light and nutrients

Abstract.  1. Environmental heterogeneity created by prescribed burning provided the context for testing whether the distribution of an oak specialist (the lace bug, Corythuca arcuata ) could be explained by stoichiometric mismatches between herbivore and host plant composition.
2. Field observations showed that lace bug density was seven-fold higher in frequently burned than in unburned units.
3. Lace bug density did not increase with leaf nutrient concentrations, but was instead associated with higher light levels, higher concentrations of leaf carbon (C), lignin and total phenolics, and lower levels of cellulose. In addition, lace bugs reared on high-light leaves had higher levels of survivorship than those fed on low-light leaves.
4. Sampling restricted to full-sun leaves was used to test whether fire-related changes in leaf nitrogen (N) and phosphorus (P) concentrations have a secondary influence on lace bug success. This sampling provided only limited evidence for nutrient limitation, as decreases in leaf N and P were associated with an increase in lace bug mass but a decrease in density.
5. It is concluded that burning probably promotes lace bug population growth by increasing canopy openness, light penetration, and the availability of C-based metabolites, and thus simple stoichoimetric mismatches between herbivores and host plants are not of primary importance in this system.     

Co-evolutionary analysis of domains in interacting proteins reveals insights into domain-domain interactions mediating protein-protein interactions

Recent advances in functional genomics have helped generate large-scale high-throughput protein interaction data. Such networks, though extremely valuable towards molecular level understanding of cells, do not provide any direct information about the regions (domains) in the proteins that mediate the interaction. Here, we performed co-evolutionary analysis of domains in interacting proteins in order to understand the degree of co-evolution of interacting and non-interacting domains. Using a combination of sequence and structural analysis, we analyzed protein-protein interactions in F1-ATPase, Sec23p/Sec24p, DNA-directed RNA polymerase and nuclear pore complexes, and found that interacting domain pair(s) for a given interaction exhibits higher level of co-evolution than the non-interacting domain pairs. Motivated by this finding, we developed a computational method to test the generality of the observed trend, and to predict large-scale domain-domain interactions. Given a protein-protein interaction, the proposed method predicts the domain pair(s) that is most likely to mediate the protein interaction. We applied this method on the yeast interactome to predict domain-domain interactions, and used known domain-domain interactions found in PDB crystal structures to validate our predictions. Our results show that the prediction accuracy of the proposed method is statistically significant. Comparison of our prediction results with those from two other methods reveals that only a fraction of predictions are shared by all the three methods, indicating that the proposed method can detect known interactions missed by other methods. We believe that the proposed method can be used with other methods to help identify previously unrecognized domain-domain interactions on a genome scale, and could potentially help reduce the search space for identifying interaction sites.     

Ecological interactions among insect herbivores,ants and the host plant Baccharis dracunculifolia in a Brazilian mountain ecosystem

Insect–plant interactions occur in several ways and have considerable environmental and ecological importance. Many feeding strategies have evolved among herbivorous insects, with host–herbivore systems likely being influenced by trophobionts with ants. We investigated how these interactions vary across elevation gradients by evaluating the structure of the herbivorous insect community and ants associated with Baccharis dracunculifolia at three distinct elevations (800, 1100, and 1400 m a.s.l.) on a mountain in southeastern Brazil. Moreover, we evaluated the diversity and specialisation of interactions between herbivores and host plants along the elevational gradient. We sampled herbivores and ants on 60 plants at each elevation (totalling 180 plant individuals). Herbivore species composition differed among elevations, as did interaction diversity and specialisation. Richness and abundance of chewing insects increased with elevation, while β‐diversity among patches of the host plant was higher at the lowest elevation, probably due to the patchy occurrence of B. dracunculifolia. Richness and abundance of sap‐sucking insects were higher at the intermediate elevation, possibly due to local environmental conditions. We observed a positive relationship between ant and herbivore trophobiont richness on B. dracunculifolia. We found that interactions were more specialised and less diverse at higher elevations compared to the lowest elevation. Changes in vegetation and environmental variables shaped species distributions and their ecological interactions along the elevation gradient. Our study demonstrates that increased elevation changes the structure and patterns of interactions of the herbivore insect guilds associated with the host plant B. dracunculifolia. Ant effects depend on the context, the environment, and the species of ants involved, and are essential for the presence of insect trophobionts.     

Dissipation of insect growth regulators in fresh orange and orange juice

It was studied the dissipation rates of fenoxycarb, Lufenuron, flufenoxuron and pyriproxyfen from their application on navelina orange crops to the production of orange juice. Supervised trials were carried out for the phytosanitary treatments under two situations, one according to Good Agricultural Practices (GAP) and the other one with Critical Agricultural Practices (CAP). Samples of both situations were transformed into orange juice according to the current industrial process. The analytical methodology included acetone and dichloromethane/petroleum ether extraction and aminopropyl-based cleanup. Method validation followed SANCO Guidelines. The final objective was the determination of the exposure to the residues in raw and processed orange when good and critical agricultural conditions are used in the field.     

Compound effects of induced plant responses on insect herbivores and parasitoids: implications for tritrophic interactions

1. Induced plant responses can affect herbivores either directly, by reducing herbivore development, or indirectly, by affecting the performance of natural enemies. Both the direct and indirect impacts of induction on herbivore and parasitoid success were evaluated in a common experimental system, using clonal poplar trees Populus nigra (Salicales: Salicaceae), the gypsy moth Lymantria dispar (L.) (Lepidoptera: Lymantriidae), and the gregarious parasitoid Glyptapanteles flavicoxis (Marsh) (Hymenoptera: Braconidae). 2. Female parasitoids were attracted to leaf odours from both damaged and undamaged trees, however herbivore‐damaged leaves were three times more attractive to wasps than undamaged leaves. Parasitoids were also attracted to herbivore larvae reared on foliage and to larval frass, but they were not attracted to larvae reared on artificial diet. 3. Prior gypsy moth feeding elicited a systemic plant response that retarded the growth rate, feeding, and survival of gypsy moth larvae, however induction also reduced the developmental success of the parasitoid. 4. The mean number of parasitoid progeny emerging from hosts fed foliage from induced trees was 40% less than from uninduced trees. In addition, the proportion of parasitised larvae that survived long enough to issue any parasitoids was lower on foliage from induced trees. 5. A conceptual and analytical model is provided to describe the net impacts of induced plant responses on parasitoids, and implications for tritrophic interactions and biological control of insect pests are discussed.     

Experimental taphonomy of Artemia reveals the role of endogenous microbes in mediating decay and fossilization

Exceptionally preserved fossils provide major insights into the evolutionary history of life. Microbial activity is thought to play a pivotal role in both the decay of organisms and the preservation of soft tissue in the fossil record, though this has been the subject of very little experimental investigation. To remedy this, we undertook an experimental study of the decay of the brine shrimp Artemia, examining the roles of autolysis, microbial activity, oxygen diffusion and reducing conditions. Our findings indicate that endogenous gut bacteria are the main factor controlling decay. Following gut wall rupture, but prior to cuticle failure, gut-derived microbes spread into the body cavity, consuming tissues and forming biofilms capable of mediating authigenic mineralization, that pseudomorph tissues and structures such as limbs and the haemocoel. These observations explain patterns observed in exceptionally preserved fossil arthropods. For example, guts are preserved relatively frequently, while preservation of other internal anatomy is rare. They also suggest that gut-derived microbes play a key role in the preservation of internal anatomy and that differential preservation between exceptional deposits might be because of factors that control autolysis and microbial activity. The findings also suggest that the evolution of a through gut and its bacterial microflora increased the potential for exceptional fossil preservation in bilaterians, providing one explanation for the extreme rarity of internal preservation in those animals that lack a through gut.     

Invasive insect herbivores as disrupters of chemically-mediated tritrophic interactions: effects of herbivore density and parasitoid learning

Invasive insect herbivores have the potential to interfere with native multitrophic interactions by affecting the chemical cues emitted by plants and disrupting the attraction of natural enemies mediated by herbivore-induced plant volatiles (HIPVs). In a previous study, we found that the presence of the exotic herbivore Spodoptera littoralis on Brassica rapa plants infested by the native herbivore Pieris brassicae makes these dually-infested plants unattractive to the main parasitoid of P. brassicae, the braconid wasp Cotesia glomerata. Here we show that this interference by S. littoralis is strongly dependent on the relative densities of the two herbivores. Parasitoids were only deterred by dually-infested plants when there were more S. littoralis larvae than P. brassicae larvae on a plant. Furthermore, the blend of HIPVs emitted by dually-infested plants differed the most from HIPVs emitted by Pieris-infested plants when S. littoralis density exceeded P. brassicae density. We further found that associative learning by the parasitoid affected its preferences: attraction to dually-infested plants increased after parasitoids were presented a P. brassicae caterpillar (rewarding experience) in presence of the odor of a dually-infested plant, but not when presented a S. littoralis caterpillar (non-rewarding experience). A non-rewarding experience prior to the bioassays resulted in a general decrease in parasitoid motivation to respond to plant odors. We conclude that herbivore density and associative learning may play an important role in the foraging behavior of natural enemies in communities, and such effects should not be overlooked when investigating the ecological impact of exotic species on native food webs.     

The multifaceted function of BAK1/SERK3: Plant immunity to pathogens and responses to insect herbivores

Almost a decade ago BRI1-associated kinase 1 (BAK1) was identified as a co-receptor of brassinosteroid (BR) insensitive 1 (BRI1), the receptor for BRs, which plays an essential role in transducing BR signaling to regulate plant development. BAK1 is also critical in resistance to various pathogens. BAK1 rapidly binds to certain receptors for pathogen/microbe-associated molecular patterns (PAMPs/MAMPs) after the perception of pathogen elicitors and is required for the full elicitation of pathogen-induced defense responses, such as the activation of the mitogen-activated protein kinase 6 (MPK6) and production of reactive oxygen species. Thus, BAK1 functions in both BR signaling and PAMP-triggered immunity (PTI). Recently BAK1 was also found to play an important role in mediating defense responses against an insect herbivore (Manduca sexta) of Nicotiana attenuata. In this interaction, BAK1 positively modulates wound- or herbivore feeding-induced accumulation of jasmonic acid (JA) and JA-isoleucine (JA-Ile). This mini-review summarizes recent advances in our understanding of the functions of BAK1 in resistance to pathogens and herbivores.Key words: BAK1, defense, herbivore, immunity, insect, jasmonate, pathogen, wounding     

The role of indirect interactions in structuring tropical insect communities

Apparent competition is a form of indirect interaction among species that can potentially structure biological communities. In insect communities, parasitoid-mediated apparent competition has been proposed as a particularly important structuring force. We argue that short-term apparent competition may be less important in structuring insect communities in tropical regions, compared with temperate regions. This prediction arises because, compared with temperate insects, tropical insects that share natural enemies are more likely to be isolated in both space and time.