Root herbivore identity matters in plant-mediated interactions between root and shoot herbivores

Plants are simultaneously attacked by a multitude of herbivores that affect plant responses and plant-mediated interactions in a variety of ways. So far, studies on indirect interactions between below- and aboveground herbivores have almost exclusively focused on interactions between only one root and one shoot herbivore species at the same time. Since these studies show a variety of outcomes, we test the hypothesis that root herbivore identity matters in below-/aboveground interactions. We studied the combined effects root-feeding nematodes (Pratylenchus penetrans) and wireworms (Agriotes lineatus larvae) on Plantago lanceolata and on the performance of aboveground phloem-feeding aphids (Myzus persicae) and chewing caterpillars (Chrysodeixis chalcites larvae). Since root herbivores may also affect resource availability and the microbial community in the rhizosphere, we examined resource utilization by soil microorganisms using BIOLOG EcoPlates™.

Wireworms decreased root biomass by 13%, but led to compensatory shoot growth. Nematodes and the aboveground herbivores did not affect the biomass of Plantago lanceolata. Feeding by C. chalcites larvae enhanced the concentration of aucubin in leaves, which might explain the high mortality of the caterpillars. Aphids and the belowground herbivores did not change iridoid glycoside levels in the leaves. However, the number of aphid offspring was reduced by 44% when nematodes had been added to the soil, whereas wireworms had no effect. We observed higher utilization of BIOLOG carbon sources by the soil microorganisms only in the presence of Pratylenchus penetrans. Our results suggest that the outcome of below–aboveground interactions highly depends on herbivore identity.     

Interactions between a fungal pathogen, foliar properties, and generalist herbivores

American [Castanea dentata (Marsh) Borkh.] × Chinese [Castanea mollissima Blume] chestnut (Fagac, ae) hybrids are a novel system in which to study influences of phytopathogenic fungi and woody plant hybridization on herbivore susceptibility, as the hybrids are well characterized with regard to resistance to the chestnut blight fungus [Cryphonectria parasita (Murr) Barr (Endothia) Diaporthales: Valsaceae] and variability is present. We chose two groups of resistance‐rated backcross chestnut that shared an F1 parent and had different American parents. Foliage from both backcross groups and the parent trees was sampled on three dates for use in feeding assays with gypsy moth larvae [Lymantria dispar (L.) [Lepidoptera: Lymantriidae], adult Japanese beetles [Popillia japonica Newman (Coleoptera: Scarabaeidae)], and fall webworm larvae [Hyphantria cunea Drury (Lepidoptera: Arctiidae)], respectively. Foliar analyses were performed concurrently and included carbohydrate, tannin, and nitrogen content, toughness, and density. Blight resistance had almost no effect on herbivore performance or foliar chemistry. When the parent trees and backcross groups were compared, however, significant differences in gypsy moth performance and Japanese beetle consumption were evident. There were no differences in fall webworm consumption. Most foliar characteristics measured differed among chestnut genotypes at some point in the season, and all varied seasonally. No clear pattern emerges with respect to the relationship among blight resistance, herbivore susceptibility, foliar properties, and plant genotype, and more research is needed to separate these effects.     

Facilitative interactions between two lepidopteran herbivores of Asimina

Summary Insect herbivores that require young foliage for successful larval development are often restricted to a single generation during a year by the scarcity of suitable food over most of the growing season. The major specialist herbivore attacking shrubs in the genus Asimina in Florida, Eurytides marcellus, requires young foliage for successful larval development. Field manipulations were used to investigate the role of the young foliage produced by Asimina in response to defoliation by the late-season feeder Omphalocera munroei, a second specialist herbivore of Asimina in Florida, in maintaining Eurytides populations during the summer months when young foliage is otherwise scarce. Defoliation by Omphalocera proved to be the major inducer of young growth during the summer because Omphalocera defoliated Asimina shrubs so frequently and severely. When compared to young leaves produced in the absence of damage, the teaves produced by Asimina in response to defoliation were equally as suitable as food for Eurytides larvae and as acceptable as oviposition sites by Eurytides females. The availability of young foliage in an Asimina population was correlated with the size of the associated Eurytides population. The combination of regular, severe defoliation by Omphalocera and lack of a defensive response to damage by Asimina lead to a positive affect of Omphalocera on Eurytides population size, and may be central to other facilitative interactions between herbivores as well.     

Positive interactions between herbivores and plant diversity shape forest regeneration

The effects of herbivores and diversity on plant communities have been studied separately but rarely in combination. We conducted two concurrent experiments over 3 years to examine how tree seedling diversity, density and herbivory affected forest regeneration. One experiment factorially manipulated plant diversity (one versus 15 species) and the presence/absence of deer (Odocoileus virginianus). We found that mixtures outperformed monocultures only in the presence of deer. Selective browsing on competitive dominants and associational protection from less palatable species appear responsible for this herbivore-driven diversity effect. The other experiment manipulated monospecific plant density and found little evidence for negative density dependence. Combined, these experiments suggest that the higher performance in mixture was owing to the acquisition of positive interspecific interactions rather than the loss of negative intraspecific interactions. Overall, we emphasize that realistic predictions about the consequences of changing biodiversity will require a deeper understanding of the interaction between plant diversity and higher trophic levels. If we had manipulated only plant diversity, we would have missed an important positive interaction across trophic levels: diverse seedling communities better resist herbivores, and herbivores help to maintain seedling diversity.     

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.     

Interaction between a fungal endophyte and root herbivores of Ammophila arenaria

The effect of an endophytic fungus (Acremonium strictum) on plant-growth related parameters of marram grass (Ammophila arenaria), and its potential as a protective agent against root herbivores (Pratylenchus dunensis and Pratylenchus penetrans, root-lesion nematodes) was investigated in two inoculation experiments under different conditions. Acremonium strictum-inoculated plants showed increased plant development in terms of root biomass in the first experiment and increased number of tillers in the second experiment and biomass was less suppressed by nematodes than the Acremonium strictum-free plants. In neither experiment did Acremonium strictum reduce multiplication of root herbivores. On the contrary, Acremonium strictum-inoculated plants seemed to increase herbivore multiplication. Plants infected with P. penetrans benefitted more from the endophytic fungus than those with P. dunensis in terms of total biomass. The effect of Acremonium strictum on interspecific competition was also analyzed by plant inoculation with both nematode species. In Acremonium strictum-free plants with mixed nematode inoculum, the total number of nematodes, compared to numbers observed in one-species inoculation, was less than expected, suggesting that interspecific competition took place. In Acremonium strictum-inoculated plants no interspecific competition was observed. Plants inoculated with P. dunensis, P. penetrans and Acremonium strictum showed decreased total biomass compared to Acremonium strictum-free plants inoculated with the same nematodes. The implications of increased tillering and root growth of plants with Acremonium endophytes are discussed in relation to the sand stabilizing role of Ammophila arenaria in coastal dunes.     

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.     

Specific impacts of two root herbivores and soil nutrients on plant performance and insect–insect interactions

Soil‐dwelling insects commonly co‐occur and feed simultaneously on belowground plant parts, yet patterns of damage and consequences for plant and insect performance remain poorly characterized. We tested how two species of root‐feeding insects affect the performance of a perennial plant and the mass and survival of both conspecific and heterospecific insects. Because root damage is expected to impair roots’ ability to take up nutrients, we also evaluated how soil fertility alters belowground plant–insect and insect–insect interactions. Specifically, we grew common milkweed Asclepias syriaca in low or high nutrient soil and added seven densities of milkweed beetles Tetraopes tetraophthalmus, wireworms (mainly Hypnoides abbreviatus), or both species. The location and severity of root damage was species‐specific: Tetraopes caused 59% more damage to main roots than wireworms, and wireworms caused almost seven times more damage to fine roots than Tetraopes. Tetraopes damage decreased shoot, main root and fine root biomass, however substantial damage by wireworms did not decrease any component of plant biomass. With the addition of soil nutrients, main root biomass increased three times more, and fine root biomass increased five times more when wireworms were present than when Tetraopes were present. We detected an interactive effect of insect identity and nutrient availability on insect mass. Under high nutrients, wireworm mass decreased 19% overall and was unaffected by the presence of Tetraopes. In contrast, Tetraopes mass increased 114% overall and was significantly higher when wireworms were also present. Survival of wireworms decreased in the presence of Tetraopes, and both species’ survival was negatively correlated with conspecific density. We conclude that insect identity, density and soil nutrients are important in mediating the patterns and consequences of root damage, and suggest that these factors may account for some of the contradictory plant responses to belowground herbivory reported in the literature.     

A soil bacterium can shape belowground interactions between maize,herbivores and entomopathogenic nematodes

Plant and Soil - Entomopathogenic nematodes (EPN) use odor cues to locate and infect their insect hosts in the soil, making them an important tool in sustainable management of agricultural insect...     

Atmospheric change alters frass quality of forest canopy herbivores

This study examined the independent and interactive effects of elevated atmospheric carbon dioxide (CO₂) and tropospheric ozone (O₃) on the foliar and litter chemistry of two deciduous tree species and the frass chemistry of four lepidopteran folivores. Trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera) were grown under elevated levels of CO₂ and/or O₃ at the Aspen FACE research site in northern WI, USA. We measured the effects of CO₂ and O₃ on nitrogen, carbon to nitrogen (C:N), and condensed tannin levels in aspen and birch leaves and senescent litter and also in the frass of folivores fed aspen or birch green leaves. Overall, the effects of elevated CO₂ on foliar chemistry were less pronounced than those of elevated O₃, and aspen responded more strongly than birch. While the effects of elevated CO₂ and O₃ on foliar chemistry were generally reflected in frass chemistry, the magnitude of the response varied among insect species. Insect frass had higher nitrogen and condensed tannin levels and lower C:N ratios than did litter, although the magnitude of this response varied among fumigation treatments and insect species. Our findings demonstrate that the quality of insect-mediated organic deposition can be indirectly affected by atmospheric change, through altered foliar quality. Our findings also suggest that the quality of frass deposited on the forest floor via herbivory will be strongly affected by herbivore community composition.     

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.     

Plant growth-form alters the relationship between foliar morphology and species shade-tolerance ranking in temperate woody taxa

Variation in leaf size (area per leaf) and leaf dry weight per area (LWA) in relation to species shade- and drought-tolerance, characterised by Ellenberg's light (ELD) and water demand (EWD) values, respectively, were examined in 60 temperate woody taxa at constant relative irradiance. LWA was independent of plant size, but leaf size increased with total plant height at constant ELD. Canopy position also affected leaf morphology: leaves from the upper crown third had higher LWA and were larger than leaves from the lower third. Leaf size and LWA were negatively correlated, and leaf size decreased and LWA increased with decreasing species shade-tolerance. Mean LWA was similar for trees and shrubs, but trees had larger leaves than shrubs. Furthermore, all relationships were altered by plant growth-form: none of the qualitative tendencies was significant for trees. This implies the considerably lower plasticity of foliar parameters in trees than those in shrubs. Accordingly, shade-tolerance of trees, having relatively constant leaf structure, may be most affected by the variability in biomass partitioning and crown geometry which influence foliage distribution and spacing and finally determine canopy light absorptance. Alteration of leaf form and investment pattern for construction of unit foliar surface area which change the efficiency of light interception per unit biomass investment in leaves, is a competitive strategy inherent to shrubs. EWD as well as wood anatomy did not control LWA and leaf size, though there was a trend of ring-porous tree species to be more shade-tolerant than diffuse-porous trees. Since ring-porous species are more vulnerable to cavitation than diffuse-porous species, they may be constrained to environments where irradiances and consequently evaporative demand is lower.     

Evaluation of intraguild interactions between two species of insect herbivores on Pistia stratiotes

Pistia stratiotes L. (Araceae) is an important weed in many waterways around the world. The South American weevil Neohydronomus affinis Hustache (Coleoptera: Curculionidae) is a successful biocontrol agent for this weed but additional agents are needed for some areas. The planthopper Lepidelphax pistiae Remes Lenicov (Hemiptera: Delphacidae) is a specific herbivore of P. stratiotes and is highly damaging in laboratory conditions. A field experiment was designed to evaluate the damage potential of L. pistiae compared to N. affinis and to assess the potential for competition between the two herbivores. Both herbivore species were reared inside floating cages on a P. stratiotes-infested lake. Plant growth indices assessed were clonation levels, biomass and plant diameter. The growth indices of plants exposed to the herbivores, individually and combined, were comparable, and significantly lower than in the control treatments. Population levels of N. affinis inside the cages were not significantly different when alone or together with L. pistae. Conversely, the density of L. pistiae was significantly lower in combination with the weevil. This suggests that L. pistiae is a damaging herbivore that will not reduce the biological control effectiveness of N. affinis.     

Drought changes plant chemistry and causes contrasting responses in lepidopteran herbivores

Drought events are predicted to increase due to climate change, yet consequences for plant–insect interactions are only partially understood. Drought‐mediated interactions between herbivores and their host plants are affected by a combination of factors, including characteristics of the affected plant, its associated herbivore and of the prevailing drought. Studying the effect of these factors in combination may provide important insight into plant and herbivore responses to drought. We studied drought effects on plant resistance to two leaf‐chewing herbivores by considering differing growth conditions, plant chemistry and insect responses in concert. We exposed Alliaria petiolata plants from several wild populations to different intensities of intermittent drought stress and quantified drought‐mediated changes in plant chemistry. Simultaneously, we assessed behavior (feeding preference) and performance of two lepidopteran herbivores: Pieris brassicae, a specialist, and Spodoptera littoralis, a generalist. Drought led to lowest concentrations of secondary defense compounds in severely stressed plants, without affecting total nitrogen content. Additionally, drought evoked opposite patterns in feeding preferences (plant palatability) between the herbivore species. Pieris brassicae consumed most of well‐watered plants, while S. littoralis preferred severely drought‐stressed plants. Hence, feeding preferences of S. littoralis reflected changes in plant secondary chemistry. Contrary to their feeding preference, P. brassicae performed better on drought‐stressed than on well‐watered plants, with faster development and higher attained pupal mass (plant suitability). Spodoptera littoralis showed retarded development in all treatments. In conclusion, drought caused plant secondary defense compounds to decrease consistently across all studied plant populations, which evoked contrasting feeding preferences of two herbivore species of the same feeding guild. These results suggest herbivore specificity as a possible explanation for herbivore responses to drought and emphasize the importance of herbivore characteristics such as feeding specialization in understanding and predicting consequences of future drought events.     

Direct consumptive interactions between mammalian herbivores and plant-dwelling invertebrates: prevalence,significance, and prospectus

Mammalian herbivores induce changes in the chemical composition, phenology, distribution, and abundance of the plants they feed on. Consequently, invertebrate herbivores (predominantly insects) that depend on those plants, and the predators and parasitoids that are associated with them, may be affected. This plant-mediated indirect interaction between mammals and invertebrates has been extensively studied, but mammalian herbivores may also directly affect plant-dwelling invertebrates (PDI) by incidentally ingesting them while feeding. The ubiquity and small size of PDI render them highly susceptible to incidental ingestion, but as common as this interaction may intuitively seem, very little is known about its prevalence and ecological consequences. Nevertheless, cases of incidental ingestion of PDI and associated adaptations for avoiding it that have been sporadically documented in several invertebrate groups and life stages allow us to carefully extrapolate and conclude that it should be common in nature. Incidental ingestion may, therefore, bear significant consequences for PDI, but it may also affect the mammalian herbivores and the shared plants. Future research on incidental ingestion of PDI would have to overcome several technical difficulties to gain better insight into this understudied ecological interaction.