Root-feeding Herbivores Research Articles

Host search behaviors of specialist and generalist root feeding herbivores (Diabrotica spp.) on host and non-host plants

Western, northern, Mexican, and southern corn rootworms (WCR, NCR, MCR, and SCR) are serious corn pests. We evaluated host search behavior of these pests on six plant species using a video tracking system. After a 5-min exposure to plant roots, behavioral parameters were automatically recorded and used to quantify the search behavior. The search behavior was not observed for sorghum since no neonates survived after contacting sorghum roots. After exposures to corn roots, all neonates exhibited the localized search behaviors (i.e., shortening total distance traveled, lowering movement speed, increasing turn angle, moving farther from origin) which are used to stay in and search within root systems. When larvae contacted roots of wheat, barley, oats, soybean, or controls, they expanded the search area by extending the travel path, increasing velocity, and reducing turn angles and total distance moved. The intensity of the search expansion is highly associated with the host preferences known for the four rootworm species and subspecies. Neonates of each corn rootworm exhibited distinct search behaviors. In fact, NCR larvae had the highest speed, the greatest travel path, and the lowest turn angle, whereas MCR larvae had the highest turn angle and moved faster than WCR and SCR larvae.

Drought Stress Affects Spectral Separation of Maize Infested by Western Corn Rootworm

Root-feeding herbivores present challenges for insect scouting due to the reliance on aboveground visual cues. These challenges intensify in multi-stress environments, where one stressor can mask another. Pre-visual identification of plant stress offers promise in addressing this issue. Hyperspectral data have emerged as a measurement able to identify plant stress before visible symptoms appear. The effectiveness of spectral data to identify belowground stressors using aboveground vegetative measurements, however, remains poorly understood, particularly in multi-stress environments. We investigated the potential of hyperspectral data to detect Western corn rootworm (WCR; Diabrotica virgifera virgirefa) infestations in resistant and susceptible maize genotypes in the presence and absence of drought. Under well-watered conditions, the spectral profiles separated between WCR treatments, but the presence of drought eliminated spectral separation. The foliar spectral profiles separated under drought conditions, irrespective of WCR presence. Spectral data did not classify WCR well; drought was well classified, and the presence of drought further reduced WCR classification accuracy. We found that multiple plant traits were not affected by WCR but were negatively affected by drought. Our study highlights the possibility of detecting WCR and drought stress in maize using hyperspectral data but highlights limitations of the approach for assessing plant health in multi-stress conditions.

A Novel Insect Overwintering Strategy: The Case of Mealybugs.

Insects have limited ability to regulate their body temperature and have thus required a range of strategies to withstand thermally stressful environments. Under unfavorable winter conditions, insects often take refuge under the soil surface to survive. Here, the mealybug insect family was selected for the study. Field experiments were performed in fruit orchards in eastern Spain. We used specifically designed floor sampling methods combined with fruit tree canopy pheromone traps. We found that in temperate climates, the large majority of the mealybugs move from the tree canopy to the roots during the winter, where they turn into belowground root-feeding herbivores to survive and continue underground the reproductive process. Within the rhizosphere, mealybugs complete at least one generation before emerging on the soil surface. The preferred area to overwinter is within 1 m in diameter around the fruit tree trunk, where more than 12,000 mealybug flying males per square meter can emerge every spring. This overwintering pattern has not previously been reported for any other group of insects showing cold avoidance behavior. These findings have implications at the winter ecology level but also at the agronomical level since treatments to control mealybug pests are, until now, only based on the fruit trees' canopy.

Leaf-chewing herbivores affect preference and performance of a specialist root herbivore

Plants interact with a diversity of phytophagous insects above- and belowground. By inducing plant defence, one insect herbivore species can antagonize or facilitate other herbivore species feeding on the same plant, even when they are separated in space and time. Through systemic plant-mediated interactions, leaf-chewing herbivores may affect the preference and performance of root-feeding herbivores. We studied how six different leaf-chewing herbivore species of Brassica oleracea plants affected oviposition preference and larval performance of the root-feeding specialist Delia radicum. We expected that female D. radicum flies would oviposit where larval performance was highest, in accordance with the preference–performance hypothesis. We also assessed how the different leaf-chewing herbivore species affected defence-related gene expression in leaves and primary roots of B. oleracea, both before and after infestation with the root herbivore. Our results show that leaf-chewing herbivores can negatively affect the performance of root-feeding D. radicum larvae, although the effects were relatively weak. Surprisingly, we found that adult D. radicum females show a strong preference to oviposit on plants infested with a leaf-chewing herbivore. Defence-related genes in primary roots of B. oleracea plants were affected by the leaf-chewing herbivores, but these changes were largely overridden upon local induction by D. radicum. Infestation by leaf herbivores makes plants more attractive for oviposition by D. radicum females, while decreasing larval performance. Therefore, our findings challenge the preference–performance hypothesis in situations where other herbivore species are present.

The effects of pulsed fertilization and chronic herbivory by periodical cicadas on tree growth.

Although many studies have investigated plant growth in the context of episodic herbivory and pressed resource availability, relatively few have examined how plant growth is affected by pulsed resources and chronic herbivory. Periodical cicada (Magicicada spp.) adults represent a pulsed detrital subsidy that fertilizes plants, and live cicada nymphs are long-lived root-feeding herbivores. Previous studies of cicada herbivory effects have been inconclusive, and previous studies of cicada-mediated fertilization did not examine effects on trees, or on a multiyear timescale. Here, we describe the results of a 3-yr experiment that factorially manipulated the presence and absence of cicada fertilization and herbivory in a population of 100 American sycamore (Platanus occidentalis) trees. We found that cicada fertilization strongly increased tree growth in the year of emergence, creating differences in tree size that persisted at least 2yr later. By comparison, we did not detect reductions in tree growth associated with cicada herbivory in any year of this experiment. However, cicada herbivory reduced the densities of, and damage from, other aboveground herbivores. These results suggest that cicadas affect the size structure of forests over multiple years, and raise questions about how cicada-mediated fertilization and herbivory will affect tree growth over longer timescales.

A conserved pattern in plant-mediated interactions between herbivores.

Plant-mediated interactions between herbivores are important determinants of community structure and plant performance in natural and agricultural systems. Current research suggests that the outcome of the interactions is determined by herbivore and plant identity, which may result in stochastic patterns that impede adaptive evolution and agricultural exploitation. However, few studies have systemically investigated specificity versus general patterns in a given plant system by varying the identity of all involved players. We investigated the influence of herbivore identity and plant genotype on the interaction between leaf-chewing and root-feeding herbivores in maize using a partial factorial design. We assessed the influence of leaf induction by oral secretions of six different chewing herbivores on the response of nine different maize genotypes and three different root feeders. Contrary to our expectations, we found a highly conserved pattern across all three dimensions of specificity: The majority of leaf herbivores elicited a negative behavioral response from the different root feeders in the large majority of tested plant genotypes. No facilitation was observed in any of the treatment combinations. However, the oral secretions of one leaf feeder and the responses of two maize genotypes did not elicit a response from a root-feeding herbivore. Together, these results suggest that plant-mediated interactions in the investigated system follow a general pattern, but that a degree of specificity is nevertheless present. Our study shows that within a given plant species, plant-mediated interactions between herbivores of the same feeding guild can be stable. This stability opens up the possibility of adaptations by associated organisms and suggests that plant-mediated interactions may contribute more strongly to evolutionary dynamics in terrestrial (agro)ecosystems than previously assumed.

How do belowground organisms influence plant-pollinator interactions?

Aims The majority of angiosperms are pollinated by animals, and this interaction is of enormous importance in both agricultural and natural systems. Pollinator behavior is influenced by plants’ floral traits, and these traits may be modified by interactions with other community members. In recent years, knowledge of ecological linkages between above- and belowground organisms has grown tremendously. Soil communities are extremely diverse, and when their interactions with plants influence floral characteristics, they have the potential to alter pollinator attraction and visitation, but plant‐pollinator interactions have been neglected in studies of the direct and indirect effects of soil organism‐root interactions. Here, we review these belowground interactions, focusing on the effects of nitrogen-fixing bacteria, arbuscular mycorrhizal fungi and root-feeding herbivores, and their effects on floral traits and pollinators. Further, we identify gaps in our knowledge of these indirect effects and recommend promising directions and topics that should be addressed by future research.

Root Chemistry in Populus tremuloides: Effects of Soil Nutrients, Defoliation, and Genotype

Although genetic, environmental, and G x E effects on aboveground phytochemistry have been well documented in trembling aspen (Populus tremuloides), little work has focused on the same factors affecting tissues underground. Belowground plant defenses are likely important mediators of root-feeding herbivores that can strongly influence plant fitness. We used a common garden of potted aspen trees to explore the individual and interactive effects of soil nutrient availability, foliar damage, genotype, and their interactions, on concentrations of phytochemicals in aspen roots. Our common garden experiment employed 12 aspen genotypes that were planted into either low- or high-nutrient soil environments. Half of the trees were subjected to defoliation for two successive years, while the others were protected from damage. At the end of the growing season after the second defoliation, we harvested the trees to obtain root samples for which we assessed levels of phenolic glycosides, condensed tannins, nitrogen, and starch. Phenolic glycosides were most affected by genotype, while the other root phytochemicals were most responsive to soil nutrient conditions. The effects of defoliation were observed in interaction with soil nutrient environment and/or genotype. Interestingly, the effect of defoliation on phenolic glycosides was mediated by soil nutrients, whereas the effect of defoliation on condensed tannins was observed in concert with effects of both soil nutrients and genotype. Comparison of data from this study with an earlier, related study revealed that concentrations of phenolic glycosides and condensed tannins are lower in roots than leaves, and less responsive to defoliation. That soil nutrient environment affects root phytochemical concentrations is not unexpected given the intimate association of roots and soil, but the complex interactions between soil nutrients, aboveground damage, and genotype, and their effects on root phytochemistry, are intriguing. Variation in root chemistry could have wide-reaching effects on soil microbial communities, nutrient cycling, and herbivores. Additionally, the response of phytochemicals to damage across organs can link different, spatially separated herbivores as they use different parts of the same plant resource.

Soil abiotic factors influence interactions between belowground herbivores and plant roots

Root herbivores are important ecosystem drivers and agricultural pests, and, possibly as a consequence, plants protect their roots using a variety of defensive strategies. One aspect that distinguishes belowground from aboveground plant-insect interactions is that roots are constantly exposed to a set of soil-specific abiotic factors. These factors can profoundly influence root resistance, and, consequently, the outcome of the interaction with belowground feeders. In this review, we synthesize the current literature on the impact of soil moisture, nutrients, and texture on root-herbivore interactions. We show that soil abiotic factors influence the interaction by modulating herbivore abundance and behaviour, root growth and resistance, beneficial microorganisms, as well as natural enemies of the herbivores. We suggest that abiotic heterogeneity may explain the high variability that is often encountered in root-herbivore systems. We also propose that under abiotic stress, the relative fitness value of the roots and the potential negative impact of herbivory increases, which may lead to a higher defensive investment and an increased recruitment of beneficial microorganisms by the plant. At the same time, both root-feeding herbivores and natural enemies are likely to decrease in abundance under extreme environmental conditions, leading to a context- and species-specific impact on plant fitness. Only by using tightly controlled experiments that include soil abiotic heterogeneity will it be possible to understand the impact of root feeders on an ecosystem scale and to develop predictive models for pest occurrence and impact.

Herbivory reduces plant interactions with above‐ and belowground antagonists and mutualists

Herbivores affect plants through direct effects, such as tissue damage, and through indirect effects that alter species interactions. Interactions may be positive or negative, so indirect effects have the potential to enhance or lessen the net impacts of herbivores. Despite the ubiquity of these interactions, the indirect pathways are considerably less understood than the direct effects of herbivores, and multiple indirect pathways are rarely studied simultaneously. We placed herbivore effects in a comprehensive community context by studying how herbivory influences plant interactions with antagonists and mutualists both aboveground and belowground. We manipulated early-season aboveground herbivore damage to Cucumis sativus (cucumber, Cucurbitaceae) and measured interactions with subsequent aboveground herbivores, root-feeding herbivores, pollinators, and arbuscular mycorrhizal fungi (AMF). We quantified plant growth and reproduction and used an enhanced pollination treatment to determine if plants were pollen limited. Increased herbivory reduced interactions with both antagonists and mutualists. Plants with high levels of early herbivory were significantly less likely to suffer leaf damage later in the summer and tended to be less attacked by root herbivores. Herbivory also reduced pollinator visitation, likely due to fewer and smaller flowers, and reduced AMF colonization. The net effect of herbivory on plant growth and reproduction was strongly negative, but lower fruit and seed production were not due to reduced pollinator visits, because reproduction was not pollen limited. Although herbivores influenced interactions between plants and other organisms, these effects appear to be weaker than the direct negative effects of early-season tissue loss.

METAPOPULATION DYNAMICS OVERRIDE LOCAL LIMITS ON LONG‐TERM PARASITE PERSISTENCE

A simple null model, particularly germane to small and vulnerable organisms such as parasites, is that local conditions set a stage upon which larger-scale dynamics play out. Soil moisture strongly influences survival of entomopathogenic nematodes (EPN), which in turn drive trophic cascades by protecting vegetation from root-feeding herbivores. In this study, we examine the mechanisms responsible for patchy occurrence of an entomopathogenic nematode, Heterorhabditis marelatus, in a California coastal prairie. One hypothesis proposes that biotic factors such as competition and natural enemies could regulate occurrence of EPN populations. We found that fungi and other enemies of EPN, although locally potent, did not explain the patterns of incidence across sites. Abiotic factors also have strong effects on EPN persistence, especially for vulnerable free-living stages. Thus, we tested the hypothesis that patchy occurrence of EPN on a large landscape was driven by differences in soil moisture. Our research uses long-term data on nematode incidence in combination with a landscape-level experiment to demonstrate the lack of a correlation between soil moisture and long-term persistence. A year-long experiment showed EPN mortality was weakly correlated with soil moisture among our study sites. Thirteen years of data, however, showed that colonization rates were highly correlated with long-term persistence. Sites with highest long-term persistence experienced the highest rates of rhizosphere colonization, extinction, and turnover. As a result, we concluded that metapopulation dynamics override limitations set by local and short-term abiotic conditions to determine long-term persistence in this parasite-driven trophic cascade.

Mechanism of control of root‐feeding nematodes by mycorrhizal fungi in the dune grass Ammophila arenaria

Root-feeding herbivores can affect plant performance and the composition of natural plant communities, but there is little information about the mechanisms that control root herbivores in natural systems. This study explores the interactions between the pioneer dune grass Ammophila arenaria, arbuscular mycorrhizal fungi (AMF) and the root-feeding nematode Pratylenchus penetrans. Our objectives were to determine whether AMF can suppress nematode infection and reproduction and to explore the mechanisms of nematode control by AMF. A sequential inoculation experiment and a split-root experiment were designed to analyse the importance of plant tolerance and resistance and of direct competition between AMF and P. penetrans for the root herbivore and the plant. Root infection and multiplication of P. penetrans were significantly reduced by the native inoculum of AMF. Plant preinoculation with AMF further decreased nematode colonization and reproduction. Nematode suppression by AMF did not occur through a systemic plant response but through local mechanisms. Our results suggest that AMF are crucial for the control of root-feeding nematodes in natural systems and illustrate that locally operating mechanisms are involved in this process.

Climate affects predator control of an herbivore outbreak.

Herbivore outbreaks and the accompanying devastation of plant biomass can have enormous ecological effects. Climate directly affects such outbreaks through plant stress or alterations in herbivore life-history traits. Large-scale variation in climate can indirectly affect outbreaks through trophic interactions, but the magnitude of such effects is unknown. On the California coast, rainfall in years during and immediately previous to mass lupine mortality was two-thirds that of years without such mortality. However, neither mature lupines nor their root-feeding herbivores are directly affected by annual variation in rainfall. By increasing soil moisture to levels characteristic of summers following El Niño/Southern Oscillation (ENSO) events, we increased persistence of a predator (the entomopathogenic nematode Heterorhabditis marelatus). This led to suppression of an outbreak of the herbivorous moth Hepialus californicus, indirectly protecting bush lupine (Lupinus arboreus). Our results are consistent with the marine-oriented Menge-Sutherland hypothesis (Menge and Sutherland 1987) that abiotic stress has greater effects on higher than on lower trophic levels. The mechanisms producing these results differ from those proposed by Menge-Sutherland, however, highlighting differences between trophic processes in underground and terrestrial/marine food webs. Our evidence suggests that herbivore outbreaks and mass lupine mortality are indirectly affected by ENSO's facilitation of top-down control in this food web.

Effects of Simulated Grazing by Below-Ground Herbivores on Growth, CO 2 Exchange, and Carbon Allocation Patterns of Bouteloua gracilis

(1) A series of root-pruning experiments was performed to simulate the effects of grazing by root-feeding herbivores on Bouteloua gracilis. Approximately 37% (% 22 mg) of the root biomass of hydroponically grown plants was removed by clipping all roots 5 cm below the crown bases. (2) Total biomass of root-clipped plants (908 mg) was 20% lower than that of controls (1137 mg) 3 weeks after treatment. This biomass reduction was related to a 55% reduction in tiller production of treated plants. The mean rate of net photosynthesis of treated plants was 35% lower than in control plants for the first six days after treatment. For several days following root-clipping, the proportion of photosynthetically-fixed 14C allocated to roots was lower than in control plants, but this proportion increased until, by 3 weeks after treatment, the proportion allocated to roots of treated plants significantly exceeded that of controls. (3) Because of these effects on plant growth and metabolism, we suggest that below-ground herbivores may control primary production to a greater extent than would be predicted from their biomass or consumption rates.