Sequential effects of root and foliar herbivory on aboveground and belowground induced plant defense responses and insect performance

Plants are often simultaneously or sequentially attacked by multiple herbivores and changes in host plants induced by one herbivore can influence the performance of other herbivores. We examined how sequential feeding on the plant Plantago lanceolata by the aboveground herbivore Spodoptera exigua and the belowground herbivore Agriotes lineatus influences plant defense and the performance of both insects. Belowground herbivory caused a reduction in the food consumption by the aboveground herbivore independent of whether it was initiated before, at the same time, or after that of the aboveground herbivore. By contrast, aboveground herbivory did not significantly affect belowground herbivore performance, but significantly reduced the performance of later arriving aboveground conspecifics. Interestingly, belowground herbivores negated negative effects of aboveground herbivores on consumption efficiency of their later arriving conspecifics, but only if the belowground herbivores were introduced simultaneously with the early arriving aboveground herbivores. Aboveground–belowground interactions could only partly be explained by induced changes in an important class of defense compounds, iridoid glycosides (IGs). Belowground herbivory caused a reduction in IGs in roots without affecting shoot levels, while aboveground herbivory increased IG levels in roots in the short term (4 days) but only in the shoots in the longer term (17 days). We conclude that the sequence of aboveground and belowground herbivory is important in interactions between aboveground and belowground herbivores and that knowledge on the timing of exposure is essential to predict outcomes of aboveground–belowground interactions.     

Above‐ and belowground herbivory jointly impact defense and seed dispersal traits in Taraxacum officinale

Plants are able to cope with herbivores by inducing defensive traits or growth responses that allow them to reduce or avoid the impact of herbivores. Since above‐ and belowground herbivores differ substantially in life‐history traits, for example feeding types, and their spatial distribution, it is likely that they induce different responses in plants. Moreover, strong interactive effects on defense and plant growth are expected when above‐ and belowground herbivores are jointly present. The strengths and directions of these responses have been scarcely addressed in the literature. Using Taraxacum officinale, the root‐feeding nematode Meloidogyne hapla and the locust Schistocerca gregaria as a model species, we examined to what degree above‐ and belowground herbivory affect (1) plant growth responses, (2) the induction of plant defensive traits, that is, leaf trichomes, and (3) changes in dispersal‐related seed traits and seed germination. We compared the performance of plants originating from different populations to address whether plant responses are conserved across putative different genotypes. Overall, aboveground herbivory resulted in increased plant biomass. Root herbivory had no effect on plant growth. Plants exposed to the two herbivores showed fewer leaf trichomes than plants challenged only by one herbivore and consequently experienced greater aboveground herbivory. In addition, herbivory had effects that reached beyond the individual plant by modifying seed morphology, producing seeds with longer pappus, and germination success.     

Genetic variation in plant below-ground response to elevated CO2 and two herbivore species

Aims

It is unclear how changing atmospheric conditions, including rising carbon dioxide concentration, influence interactions between above and below-ground systems and if intraspecific variation exists in this response.

Methods

We assessed interactive effects of atmospheric CO₂ concentration, above-ground herbivory, and plant genotype on root traits and mycorrhizal associations. Plants from five families of Asclepias syriaca, a perennial forb, were grown under ambient and elevated atmospheric CO₂ concentrations. Foliar herbivory by either lepidopteran caterpillars or phloem-feeding aphids was imposed. Mycorrhizal colonization, below-ground biomass, root biomass, and secondary defensive chemistry in roots were quantified.

Results

We observed substantial genetic variation among A. syriaca families in their mycorrhizal colonization levels in response to elevated CO₂ and herbivory treatments. Elevated CO₂ treatment increased root biomass in all genetic families, whereas foliar herbivory tended to decrease root biomass. Root cardenolide concentration and composition varied greatly among plant families, and elevated CO₂ treatment increased root cardenolides in two of the five plant families. Moreover, herbivores differentially affected the composition of cardenolides expressed below ground.

Conclusions

Increased atmospheric CO₂ has the potential to influence interactions among plants, herbivores and mycorrhizal fungi and intraspecific variation suggests that such interactions can evolve.     

Intermediate herbivory intensity of an aboveground pest promotes soil labile resources and microbial biomass via modifying rice growth

Background and Aims

The importance of aboveground herbivores for modifying belowground ecosystems has prompted numerous studies; however, studies can be biased by context dependent conditions which lead to extremely inconsistent results. So far, the impacts of herbivory intensity by important rice pests on rice paddy soil ecosystems are lacking. The aim of this study was to test the hypothesis that intermediate herbivory intensity of the brown planthopper (Nilaparvata lugens Stål) could promote soil labile resources and microbial biomass, while high intensity would show a reverse pattern, by mediating rice plant growth. This study will also help the development of integrative pest management.

Methods

Four hopper infestation density treatments (0, 4, 8 and 12 nymphs per rice plant) and two infestation duration treatments (9 and 15 days after N. lugens infestation, DAI 9 and DAI 15) were established in a glasshouse experiment. Soil and plant were sampled destructively from four replicates and analysed for soil labile resources availability, soil microbial biomass and plant performance, respectively.

Results

The infestation density significantly affected both shoot and root mass of rice (P?<?0.05), soil dissolved organic carbon (DOC) and nitrogen (DON), and microbial biomass carbon (MBC) and nitrogen (MBN), and the effects were further enhanced by prolonged infestation duration. Compared to the control (CK) without N. lugens, plant dry mass, DOC, DON, MBC and MBN increased under low (LD) and moderate hopper densities (MD) but decreased under high density (HD) on DAI 9. Moreover, the LD treatment exerted the most promotional effects on DAI 15. Rice root to shoot ratio generally increased in treatments subjected to herbivory. The labile resources and microbial biomass showed close relationships with both shoot and root mass across treatments, in particular with root mass on DAI 15. Such a trend indicated that the shift of photosynthate allocation to belowground contributed to changes of soil resource availability and microbial biomass.

Conclusions

Intermediate herbivory intensity showed positive effects on rice seedling performance and, further, promoted soil labile resource availability and microbial biomass. The importance of extrapolating temporal and spatial scale, i.e. from the short-term greenhouse experiment to an entire rice growing season in the field, was highlighted.     

Plant responses to variable timing of aboveground clipping and belowground herbivory depend on plant age

Aims Plants use different types of responses such as tolerance and induced defense to mitigate the effects of herbivores. The direction and magnitude of both these plant responses can vary with plant age. However, most studies have focused on aboveground herbivory, whereas important feeding occurs belowground. Here, we tested the hypothesis that plant tolerance and defense following shoot damage or root herbivory depends on plant age.     

Effects of above- and belowground herbivory on growth,pollination, and reproduction in cucumber

Plants experience unique challenges due to simultaneous life in two spheres, above- and belowground. Interactions with other organisms on one side of the soil surface may have impacts that extend across this boundary. Although our understanding of plant–herbivore interactions is derived largely from studies of leaf herbivory, belowground root herbivores may affect plant fitness directly or by altering interactions with other organisms, such as pollinators. In this study, we investigated the effects of leaf herbivory, root herbivory, and pollination on plant growth, subsequent leaf herbivory, flower production, pollinator attraction, and reproduction in cucumber (Cucumis sativus). We manipulated leaf and root herbivory with striped cucumber beetle (Acalymma vittatum) adults and larvae, respectively, and manipulated pollination with supplemental pollen. Both enhanced leaf and root herbivory reduced plant growth, and leaf herbivory reduced subsequent leaf damage. Plants with enhanced root herbivory produced 35% fewer female flowers, while leaf herbivory had no effect on flower production. While leaf herbivory reduced the time that honey bees spent probing flowers by 29%, probing times on root-damaged plants were over twice as long as those on control plants. Root herbivory increased pollen limitation for seed production in spite of increased honey bee preference for plants with root damage. Leaf damage and hand-pollination treatments had no effect on fruit production, but plants with enhanced root damage produced 38% fewer fruits that were 25% lighter than those on control plants. Despite the positive effect of belowground damage on honey bee visitation, root herbivory had a stronger negative effect on plant reproduction than leaf herbivory. These results demonstrate that the often-overlooked effects of belowground herbivores may have profound effects on plant performance.     

Belowground ABA boosts aboveground production of DIMBOA and primes induction of chlorogenic acid in maize

Plants are important mediators between above- and belowground herbivores. Consequently, interactions between root and shoot defenses can have far-reaching impacts on entire food webs. We recently reported that infestation of maize roots by larvae of the beetle Diabrotica virgifera virgifera induced shoot resistance against herbivores and pathogens. Root herbivory also enhanced aboveground DIMBOA and primed for enhanced induction of chlorogenic acid, two secondary metabolites that have been associated with plant stress resistance. Interestingly, the plant hormone abscisic acid (ABA) emerged as a putative long-distance signal in the regulation of these systemic defenses. In this addendum, we have investigated the role of root-derived ABA in aboveground regulation of DIMBOA and the phenolic compounds chlorogenic acid, caffeic and ferulic acid. Furthermore, we discuss the relevance of ABA in relation to defense against the leaf herbivore Spodoptera littoralis. Soil-drench treatment with ABA mimicked root herbivore-induced accumulation of DIMBOA in the leaves. Similarly, ABA mimicked aboveground priming of chlorogenic acid production, causing augmented induction of this compound after subsequent shoot attack by S. littoralis caterpillars. These findings confirm our notion that ABA acts as an important signal in the regulation of aboveground defenses during belowground herbivory. However, based on our previous finding that ABA alone is not sufficient to trigger aboveground resistance against S. littoralis caterpillars, our results also suggest that the ABA-inducible effects on DIMBOA and chlorogenic acid are not solely responsible for root herbivore-induced resistance against S. littoralis.Key words: induced resistance, Spodoptera littoralis, Zea mays, Diabrotica virgifera, DIMBOA, chlorogenic acid, absisic acid, priming     

Chemical defense lowers plant competitiveness

Both plant competition and plant defense affect biodiversity and food web dynamics and are central themes in ecology research. The evolutionary pressures determining plant allocation toward defense or competition are not well understood. According to the growth–differentiation balance hypothesis (GDB), the relative importance of herbivory and competition have led to the evolution of plant allocation patterns, with herbivore pressure leading to increased differentiated tissues (defensive traits), and competition pressure leading to resource investment towards cellular division and elongation (growth-related traits). Here, we tested the GDB hypothesis by assessing the competitive response of lima bean (Phaseolus lunatus) plants with quantitatively different levels of cyanogenesis—a constitutive direct, nitrogen-based defense against herbivores. We used high (HC) and low cyanogenic (LC) genotypes in different competition treatments (intra-genotypic, inter-genotypic, interspecific), and in the presence or absence of insect herbivores (Mexican bean beetle, Epilachna varivestis) to quantify vegetative and generative plant parameters (above and belowground biomass as well as seed production). Highly defended HC-plants had significantly lower aboveground biomass and seed production than LC-plants when grown in the absence of herbivores implying significant intrinsic costs of plant cyanogenesis. However, the reduced performance of HC- compared to LC-plants was mitigated in the presence of herbivores. The two plant genotypes exhibited fundamentally different responses to various stresses (competition, herbivory). Our study supports the GDB hypothesis by demonstrating that competition and herbivory affect different plant genotypes differentially and contributes to understanding the causes of variation in defense within a single plant species.     

Interactive effects of soil nutrient heterogeneity and belowground herbivory on the growth of plants with different root foraging traits

Aims

Plants with precise root foraging patterns can proliferate roots preferentially in nutrient-rich soil patches. When nutrients are distributed heterogeneously, this trait is often competitively advantageous in pot experiments but not field experiments. We hypothesized that this difference is due to belowground herbivory under field conditions.

Methods

We performed pot experiments using seedlings of Lolium perenne (a more precise root foraging species) and Plantago lanceolata (a less precise root foraging species). The experiment had a two-way factorial randomized block design, with nutrient distribution pattern (homogeneous or heterogeneous) and belowground herbivore (present or absent) as the two factors. Each pot contained one seedling of each species.

Results

With no herbivore present, plant biomass was smaller in the heterogeneous nutrient treatment than in the homogeneous treatment in P. lanceolata, but not in L. perenne. Under homogeneous nutrient distribution, plant biomass was lower in both species with a herbivore present than with no herbivore. Under heterogeneous nutrient distribution, biomass reduction due to herbivory occurred only in L. perenne.

Conclusions

Roots of the precise root foraging species were grazed more under the heterogeneous nutrient distribution, suggesting that the herbivore more efficiently foraged for roots in nutrient-rich soil patches.     

Effects of belowground vertical distribution of a herbivore on plant biomass and survival in Lolium perenne

Root herbivory affects plant performance, but the effects are not well understood. We tested the effects of the vertical distribution of a root-feeding beetle larva (Anomala cuprea) by restricting its access to the top, middle, or bottom zone in pots of perennial ryegrass (Lolium perenne) or by allowing unrestricted access. We predicted that plant mortality, biomass, and biomass allocation should change with the zone of root herbivory, because both the magnitude of root loss and the consequences of such loss are specific to the point of damage. Seven of nine plants died in each treatment in which the larvae had access to the top zone. In contrast, no plants died when larvae occupied the middle or bottom zones. Plants were killed when the larvae grazed the root base and severed the shoots from the roots. Moreover, total plant biomass and biomass allocation to roots were significantly lower when the larvae were confined to the top and middle feeding zones. The greatest number of roots were removed when the larvae occupied the top feeding zone. Thus, the vertical distribution of a belowground herbivore is crucially important to plant fate. In nature, most belowground herbivores are concentrated near the soil surface, and thus the effects of belowground herbivory are often more severe than the effects of aboveground herbivory.     

Simulation models of the interactions between herbivore foraging strategies, social behavior, and plant community dynamics

Herbivory often operates through a feedback in which herbivores affect the success and location of plants, which in turn affects the foraging behavior of animals. Factors other than food, such as social behavior, may influence the interactions between herbivores and the plants they consume. We used a simulation model to compare the effects of foraging and social behavior on plant distribution and foraging efficiency by gophers (Thomomys bottae) in a system characteristic of California grasslands. In this system, annual forbs are the preferred food items, and their abundance increases in areas disturbed by gopher burrowing. In addition, gopher social interactions generate buffer zones between adjacent burrows. During the first year of the simulations, before gophers affected the plant community, feeding efficiency declined with increased gopher density. However, after 40 yr, annual plant abundance increased with increasing gopher density, yielding higher maximum gopher density and per capita foraging efficiency. Conversely, increased width of the buffer zones lowered maximum gopher density and annual plant abundance resulting in lower feeding efficiency. In addition, the compact burrow structure of gophers employing an area-restricted search strategy allowed a higher density of gophers to coexist, resulting in higher annual plant abundance and higher per capita food-capture rates.     

A soil-free root observation system for the study of root-microorganism interactions in maize

Background and aims

The root surface of a plant usually exceeds the leaf area and is constantly exposed to a variety of soil-borne microorganisms. Root pathogens and pests, as well as belowground interactions with beneficial microbes, can significantly influence a plants' performance. Unfortunately, the analysis of these interactions is often limited because of the arduous task of accessing roots growing in soil. Here, we present a soil-free root observation system (SF-ROBS) designed to grow maize (Zea mays) plants and to study root interactions with either beneficial or pathogenic microbes.

Methods

The SF-ROBS consists of pouches lined with wet filter paper supplying nutrient solution.

Results

The aspect of maize grown in the SF-ROBS was similar to soil-grown maize; the plant growth was similar for the shoot but different for the roots (biomass and length increased in the SF-ROBS). SF-ROBS-grown roots were successfully inoculated with the hemi-biotrophic maize fungal pathogen Colletotrichum graminicola and the beneficial rhizobacteria Pseudomonas putida KT2440. Thus, the SF-ROBS is a system suitable to study two major belowground phenomena, namely root fungal defense reactions and interactions of roots with beneficial soil-borne bacteria.

Conclusions

This system contributes to a better understanding of belowground plant microbe interactions in maize and most likely also in other crops.     

Differences in dietary composition and preference maintained despite gene flow across a woodrat hybrid zone

1. Ecotones, characterized by adjacent yet distinct biotic communities, provide natural laboratories in which to investigate how environmental selection influences the ecology and evolution of organisms. For wild herbivores, differential plant availability across sharp ecotones may be an important source of dietary‐based selection.
2. We studied small herbivore diet composition across a sharp ecotone where two species of woodrat, Neotoma bryanti and N. lepida, come into secondary contact with one another and hybridize. We quantified woodrat dietary preference through trnL metabarcoding of field‐collected fecal pellets and experimental choice trials. Despite gene flow, parental N. bryanti and N. lepida maintain distinct diets across this fine spatial scale, and across temporal scales that span both wet and dry conditions.
3. Neotoma bryanti maintained a more diverse diet, with Frangula californica (California coffeeberry) making up a large portion of its diet. Neotoma lepida maintains a less diverse diet, with Prunus fasciculata (desert almond) comprising more than half of its diet. Both F. californica and P. fasciculata are known to produce potentially toxic plant secondary compounds (PSCs), which should deter herbivory, yet these plants have relatively high nutritional value as measured by crude protein content.
4. Neotoma bryanti and N. lepida consumed F. californica and P. fasciculata, respectively, in greater abundance than these plants are available on the landscape—indicating dietary selection. Finally, experimental preference trials revealed that N. bryanti exhibited a preference for F. californica, while N. lepida exhibited a relatively stronger preference for P. fasciculata. We find that N. bryanti exhibit a generalist herbivore strategy relative to N. lepida, which exhibit a more specialized feeding strategy in this study system.
5. Our results suggest that woodrats respond to fine‐scale environmental differences in plant availability that may require different metabolic strategies in order to balance nutrient acquisition while minimizing exposure to potentially toxic PSCs.

     

The effects of large herbivores on the landscape dynamics of a perennial herb

Background and Aims

Models assessing the prospects of plant species at the landscape level often focus primarily on the relationship between species dynamics and landscape structure. However, the short-term prospects of species with slow responses to landscape changes depend on the factors affecting local population dynamics. In this study it is hypothesized that large herbivores may be a major factor affecting the short-term prospects of slow-responding species in the European landscape, because large herbivores have increased in number in this region in recent decades and can strongly influence local population dynamics.

Methods

The impact of browsing by large herbivores was simulated on the landscape-level dynamics of the dry grassland perennial polycarpic herb Scorzonera hispanica. A dynamic, spatially explicit model was used that incorporated information on the location of patches suitable for S. hispanica, local population dynamics (matrices including the impact of large herbivores), initial population sizes and dispersal rate of the species. Simulations were performed relating to the prospects of S. hispanica over the next 30 years under different rates of herbivory (browsing intensity) and varying frequencies of population destruction (e.g. by human activity).

Key Results

Although a high rate of herbivory was detected in most populations of S. hispanica, current landscape-level dynamics of S. hispanica were approximately in equilibrium. A decline or increase of over 20 % in the herbivory rate promoted rapid expansion or decline of S. hispanica, respectively. This effect was much stronger in the presence of population destruction.

Conclusions

Browsing by large herbivores can have a dramatic effect on the landscape dynamics of plant species. Changes in the density of large herbivores and the probability of population destruction should be incorporated into models predicting species abundance and distribution.     

Survivorship of penstemon grandiflorus in an oak woodland: combined effects of fire and pocket gophers

Summary The effects of fire and pocket gophers, Geomys bursarius, on the survivorship of Penstemon grandiflorus growing in an oak woodland in Minnesota were studied from 1986 to 1990. Plants growing in sparse vegetation experienced mortality rates twice that of plants growing in dense vegetation. This difference was due partly to pocket gophers whose earth moving activities reduce the density of vegetation and bury and kill individual Penstemon plants. Laboratory feeding trials showed that gophers readily eat Penstemon, particularly the fleshy roots. An experiment involving the removal of 25–75% of the root tissue in 90 plants showed that root loss significantly reduced survivorship, suggesting that gopher herbivory might also kill plants. When gophers were experimentally excluded, plants growing in sparse vegetation exhibited significantly lower mortality rates than those growing in dense vegetation. Plants in the smallest size class exhibited reduced survivorship following a late spring burn; however, overall patterns of survivorship of plants in burned areas did not differ markedly from those in the unburned areas. A longitudenal analysis of plants with different reproductive histories revealed no survivorship cost to reproduction. Mortality rates decreased with increasing plant size. Small plants were more likely to be killed by fire and by being buried under gopher mounds. Differences in underground energy reserves of small and large plants can account for most of the survivorship patterns observed in this study. The study shows that within openings of the oak woodland, fire and gophers reduce the survival of individual Penstemon plants. Nevertheless, since both gophers and fire also serve to perpetuate suitable habitat in the woodland, Penstemon is ultimately dependent on both for its long term persistence in the landscape.     

Loss of specificity: native but not invasive populations of Triadica sebifera vary in tolerance to different herbivores

During introduction, invasive plants can be released from specialist herbivores, but may retain generalist herbivores and encounter novel enemies. For fast-growing invasive plants, tolerance of herbivory via compensatory regrowth may be an important defense against generalist herbivory, but it is unclear whether tolerance responses are specifically induced by different herbivores and whether specificity differs among native and invasive plant populations. We conducted a greenhouse experiment to examine the variation among native and invasive populations of Chinese tallow tree, Triadica sebifera, in their specificity of tolerance responses to herbivores by exposing plants to herbivory from either one of two generalist caterpillars occurring in the introduced range of Triadica. Simultaneously, we measured the specificity of another defensive trait, extrafloral nectar (EFN) production, to detect potential tradeoffs between resistance and tolerance of herbivores. Invasive populations had higher aboveground biomass tolerance than native populations, and responded non-specifically to either herbivore, while native populations had significantly different and specific aboveground biomass responses to the two herbivores. Both caterpillar species similarly induced EFN in native and invasive populations. Plant tolerance and EFN were positively correlated or had no relationship and biomass in control and herbivore-damaged plants was positively correlated, suggesting little costs of tolerance. Relationships among these vegetative traits depended on herbivore type, suggesting that some defense traits may have positive associations with growth-related processes that are differently induced by herbivores. Importantly, loss of specificity in invasive populations indicates subtle evolutionary changes in defenses in invasive plants that may relate to and enhance their invasive success.     

Mammalian Herbivores Alter the Population Growth and Spatial Establishment of an Early-Establishing Grassland Species

Plant-herbivore interactions influence the establishment context of plant species, as herbivores alter the community context in which individual species establish, and the spatial relationship between individuals and their source population as plants invade. This relationship can be described using an establishment kernel, which takes into account movement through seed dispersal, and subsequent establishment of adults. Mammalian herbivores are hypothesized to influence plant population growth and establishment through a combination of consumption of seeds and seedlings, and movement of seeds. While the movement abilities of plants are well known, we have very few empirical mechanistic tests of how biotic factors like mammalian herbivores influence this spread potential. As herbivores of all sizes are abundant on the landscape, we asked the question, how do mammalian herbivores influence the population growth, spatial establishment, and the community establishment context of an early-recruiting native prairie legume, Chamaecrista fasciculata? We planted C. fasciculata in source populations within a four-acre tallgrass prairie restoration in plots with and without herbivores, and monitored its establishment with respect to distance from the source populations. We found that herbivores decreased population growth, and decreased the mean and range establishment distance. Additionally, C. fasciculata established more often without herbivores, and when surrounded by weedy, annual species. Our results provide insight into how the interactions between plants and herbivores can alter the spatial dynamics of developing plant communities, which is vital for colonization and range spread with fragmentation and climate change. Mammalian herbivores have the potential to both slow rates of establishment, but also determine the types of plant communities that surround invading species. Therefore, it is essential to consider the herbivore community when attempting to restore functioning plant communities.     

Sex-Related Differences in Reproductive Allocation,Growth, Defense and Herbivory in Three Dioecious Neotropical Palms

Background

Frequently, in dioecious plants, female plants allocate more resources to reproduction than male plants. Therefore it is expected that asymmetrical allocation to reproduction may lead to a reproduction-growth tradeoff, whereby female plants grow less than male plants, but invest more in defenses and thus experience lower herbivory than male plants.

Methodology/Principal Findings

We tested these expectations by comparing resource allocation to reproduction, growth and defense and its consequences on herbivory in three sympatric dioecious Chamaedorea palms (C. alternans, C. pinnatifrons and C. ernesti-augusti) using a pair-wise design (replicated male/female neighboring plants) in a Mexican tropical rain forest. Our findings support the predictions. Biomass allocation to reproduction in C. pinnatifrons was 3-times higher in female than male plants, consistent with what is known in C. alternans and C. ernesti-augusti. Growth (height and leaf production rate and biomass production) was higher in male plants of all three species. Female plants of the three species had traits that suggest greater investment in defense, as they had 4–16% tougher leaves, and 8–18% higher total phenolic compounds concentration. Accordingly, female plants sustained 53–78% lower standing herbivory and 49–87% lower herbivory rates than male plants.

Conclusions/Significance

Our results suggests that resource allocation to reproduction in the studied palms is more costly to female plants and this leads to predictable intersexual differences in growth, defense and herbivory. We conclude that resource allocation to reproduction in plants can have important consequences that influence their interaction with herbivores. Since herbivory is recognized as an important selective force in plants, these results are of significance to our understanding of plant defense evolution.     

Ginkgo biloba responds to herbivory by activating early signaling and direct defenses

Background

Ginkgo biloba (Ginkgoaceae) is one of the most ancient living seed plants and is regarded as a living fossil. G. biloba has a broad spectrum of resistance or tolerance to many pathogens and herbivores because of the presence of toxic leaf compounds. Little is known about early and late events occurring in G. biloba upon herbivory. The aim of this study was to assess whether herbivory by the generalist Spodoptera littoralis was able to induce early signaling and direct defense in G. biloba by evaluating early and late responses.

Methodology/Principal Findings

Early and late responses in mechanically wounded leaves and in leaves damaged by S. littoralis included plasma transmembrane potential (Vm) variations, time-course changes in both cytosolic calcium concentration ([Ca²⁺]_cyt) and H₂O₂ production, the regulation of genes correlated to terpenoid and flavonoid biosynthesis, the induction of direct defense compounds, and the release of volatile organic compounds (VOCs). The results show that G. biloba responded to hebivory with a significant Vm depolarization which was associated to significant increases in both [Ca²⁺]_cyt and H₂O₂. Several defense genes were regulated by herbivory, including those coding for ROS scavenging enzymes and the synthesis of terpenoids and flavonoids. Metabolomic analyses revealed the herbivore-induced production of several flavonoids and VOCs. Surprisingly, no significant induction by herbivory was found for two of the most characteristic G. biloba classes of bioactive compounds; ginkgolides and bilobalides.

Conclusions/Significance

By studying early and late responses of G. biloba to herbivory, we provided the first evidence that this “living fossil” plant responds to herbivory with the same defense mechanisms adopted by the most recent angiosperms.     

No evolution of reduced resistance and compensation for psyllid herbivory by the invasive <Emphasis Type="Italic">Genista monspessulana</Emphasis>

The evolution of redirecting resources from plant defense to growth or reproduction may explain why some exotic species are successful invaders in new environments. For example, the evolution of increased competitive ability hypothesis posits that escape from herbivores by invasive plants results in the selection of more vigorous genotypes that reduce their allocation of resources to defense. In addition, understanding the defense strategy of an invasive plant may help forecast the likely impact of herbivory. We tested the prediction of reduced defense (i.e., resistance) in Genista monspessulana, measured indirectly as the performance of a specialist psyllid herbivore, by comparing five native and introduced plant populations. We also examined the ability of G. monspessulana to compensate for herbivory in the presence and the absence of psyllids for a single plant population from the native and introduced regions. Plant origin (native or introduced) did not influence the psyllid’s abundance and population growth rate, suggesting no change in resistance to herbivory for introduced plants. Similarly, we found no overall difference in plant performance between individuals in the presence and the absence of psyllid herbivory, suggesting that G. monspessulana was able to fully compensate for herbivory. Damaged plants compensated by changing the pattern of branching, which also resulted in greater dry leaf biomass. We conclude that evolution of reduced defenses does not explain the success of G. monspessulana as an invader and that compensation for herbivory may limit the efficacy of the psyllid as a biological control agent.