How does herbivory affect individuals and populations of the perennial herb Paeonia officinalis?

In this study we quantified variability in foliage herbivory and pre-dispersal seed predation and its effects on plant performance and demography in populations of a rare and protected perennial herb, Paeonia officinalis. An individual-based survey was performed during four years in four populations, which contained plants in both open habitat and woodland. We detected marked spatial and temporal variation among and within populations in foliage herbivory (by insects) and pre-dispersal seed predation (by insects, rodents and Roe Deer). Foliage herbivory decreased with plant demographic stages in open habitats, from seedlings to reproductive individuals, but no significant trend was detected in woodland habitats. This may be due to different demographic origin of larger vegetative plants in this habitat. Depending on demographic stage, herbivory was higher in open habitats or not significantly different between habitats. This suggests differences in herbivore abundance in different habitats within sites. Pre-dispersal seed predation remained weak and did not depend on habitat. We did not detect any consequence of foliage herbivory on seedling mortality and individual growth in our study. Our results illustrate the need to investigate plant-herbivore interactions over several years in distinct populations in order to more accurately evaluate herbivore impact on plant population dynamics.     

The role of inbreeding and outbreeding in herbivore resistance and tolerance in Vincetoxicum hirundinaria

Background and Aims

Inbreeding via self-fertilization may have negative effects on plant fitness (i.e. inbreeding depression). Outbreeding, or cross-fertilization between genetically dissimilar parental plants, may also disrupt local adaptation or allelic co-adaptation in the offspring and again lead to reduced plant fitness (i.e. outbreeding depression). Inbreeding and outbreeding may also increase plant vulnerability to natural enemies by altering plant quality or defence. The effects of inbreeding and outbreeding on plant size and response to herbivory in the perennial herb, Vincetoxicum hirundinaria, were investigated.

Methods

Greenhouse experiments were conducted using inbred and outbred (within- and between-population) offspring of 20 maternal plants from four different populations, quantifying plant germination, size, resistance against the specialist folivore, Abrostola asclepiadis, and tolerance of simulated defoliation.

Key Results

Selfed plants were smaller and more susceptible to damage by A. asclepiadis than outcrossed plants. However, herbivore biomass on selfed and outcrossed plants did not differ. The effects of inbreeding on plant performance and resistance did not differ among plant populations or families, and no inbreeding depression at all was found in tolerance of defoliation. Between-population outcrossing had no effect on plant performance or resistance against A. asclepiadis, indicating a lack of outbreeding depression.

Conclusions

Since inbreeding depression negatively affects plant size and herbivore resistance, inbreeding may modify the evolution of the interaction between V. hirundinaria and its specialist folivore. The results further suggest that herbivory may contribute to the maintenance of a mixed mating system of the host plants by selecting for outcrossing and reduced susceptibility to herbivore attack, and thus add to the growing body of evidence on the effects of inbreeding on the mating system evolution of the host plants and the dynamics of plant–herbivore interactions.     

Parallel evolution in an invasive plant: effect of herbivores on competitive ability and regrowth of Jacobaea vulgaris

A shift in the composition of the herbivore guild in the invasive range is expected to select for plants with a higher competitive ability, a lower regrowth capacity and a lower investment in defence. We show here that parallel evolution took place in three geographically distinct invasive regions that differed significantly in climatic conditions. This makes it most likely that indeed the shifts in herbivore guilds were causal to the evolutionary changes. We studied competitive ability and regrowth of invasive and native Jacobaea vulgaris using an intraspecific competition set‐up with and without herbivory. Without herbivores invasive genotypes have a higher competitive ability than native genotypes. The invasive genotypes were less preferred by the generalist Mamestra brassicae but more preferred by the specialist Tyria jacobaeae, consequently their competitive ability was significantly increased by the first and reduced by the latter. Invasive genotypes showed a lower regrowth ability in both herbivore treatments.     

Species-specific herbivore–herbivore interactions and plant responses to sequential attack by multiple herbivores on a perennial woody plant

When plants are sequentially attacked by multiple herbivores, herbivore identity and host specialization can greatly influence the patterns of herbivore–herbivore and plant–herbivore interactions. However, how prior herbivory and the resulting induced plant responses potentially affect subsequent herbivores deserves further investigation. In this study, we conducted a common-garden experiment that manipulated sequential herbivory by the specialist caterpillar Gadirtha fusca Pogue (Lepidoptera: Nolidae) and the generalist caterpillar Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) on Chinese tallow, Triadica sebifera (L.) Small (Euphorbiaceae). We tested how prior exposure to herbivores with different levels of host specialization affected the performance of subsequently arriving con- and heterospecifics, as well as plant growth and defense responses under subsequent herbivory. We found that prior exposure to the specialist G. fusca facilitated the performance of subsequent conspecifics, resulting in a significant decrease in the growth (height and stem diameter at ground level) of tallow plants. However, prior exposure to the generalist S. litura did not affect the feeding of subsequent con- or heterospecifics or the growth of tallow plants. Sequential herbivory by specialist and generalist conspecifics resulted in lower levels of tannins and flavonoids, respectively, in leaves of tallow plants, whereas sequential herbivory by the two species did not affect the levels of tannins or flavonoids, compared to a single damage event. We conclude that herbivore species-specific plant responses appear to be more important than herbivore identity or specialization in determining herbivore–herbivore interactions and plant responses to sequential herbivore attack.     

Herbivory and local genetic differentiation in natural populations of Arabidopsis thaliana (Brassicaceae)

To explore genetic variation in defence against the natural herbivores of Arabidopsis thaliana, we transplanted genotypes between a dune habitat and inland habitat in both of which A. thaliana occurred naturally. In previous years we had observed that the specialist weevils Ceutorhynchus atomus and C. contractus (Curculionidae) fed conspicuously on flowers and fruits of A. thaliana in the dunes, while these weevils were always rare in inland habitats. Taking all plants together, total fruit damage was indeed much higher in our experimental plots in the dune habitat (59.7%) relative to the inland garden habitat (18.9%). Within a habitat, additional differences existed between plants of different origins, pointing to genetic differences in ecologically relevant characters; plants of inland origin flowered a week earlier, grew better and produced more fruits than plants of dune origin. However, plants of inland origin experienced more total fruit damage by the specialist weevils (75.4%) than plants of dune origin (44.0%) when the two types grew side by side in the dune habitat. Escape from herbivory gives dune genotypes an advantage in their native habitat, whereas stronger growth and higher survival gives inland genotypes an edge under garden conditions.     

How do two specialist butterflies determine growth and biomass of a shared host plant?

Although insect herbivory can modify subsequent quantity and quality of their host plants, change in plant quantity following herbivory has received less attention than plant quality. In particular, little is known about how previous herbivore damage determines plant growth and biomass in an insect species-specific manner. We explored whether herbivore species-specific food demand influences plant growth and biomass. To do this, we conducted a series of experiments and field survey using two specialist butterflies, Sericinus montela and Atrophaneura alcinous, and their host plant, Aristolochia debilis. It is known that A. alcinous larva requires four times more food resources to fulfill its development than S. montela larva. Despite that A. alcinous larvae imposed greater damage on plants than S. montela larvae, plant growth did not differ due to herbivory by these species both in single and multiple herbivory events. On the other hand, total aboveground biomass of the plants was reduced more by A. alcinous than S. montela feeding regardless of the number of herbivory events. Feeding on plants with a history of previous herbivory neither decreased nor increased larval growth. Our results suggest that food demand of the two butterfly species determined subsequent plant biomass, although the plant response may depend on tolerance of the host plant (i.e., ability to compensate for herbivore damage). Such difference in the effects of different herbivore species on host plant biomass is more likely to occur than previously thought, because food demand differs in most herbivore species sharing a host plant.     

Plant genotype and induced responses affect resistance to herbivores on evening primrose (Oenothera biennis)

Abstract. 1. Although both genotype and induced responses affect a plant's resistance to herbivores, little is known about their relative and interactive effects. This study examined how plant genotype of a native plant (Oenothera biennis) and induced plant responses to herbivory affect resistance to, and interactions among, several herbivores. 2. In a field experiment, genetic and environmental variation among habitats led to variation in the amount of early season damage and plant quality. The pattern of variation in early season infestation by spittlebugs (Philaenus spumarius, a piercing–sucking herbivore) negatively correlated with oviposition preference by a later feeding specialist weevil (Tyloderma foveolatum, a leaf‐chewer). 3. To determine if plant genotype and induced responses to herbivory might be responsible for these field patterns, we performed no‐choice and choice bioassays using four genotypes of O. biennis that varied in resistance. Plants were induced by either spittlebugs or weevils and assays measured the responses of the same specialist weevil as well as a generalist caterpillar (Spodoptera exigua). 4. Resistance to adult weevils was largely unaffected by plant genotype, while they experienced induced resistance following damage by conspecific weevils in no‐choice assays. Caterpillars were more strongly affected by plant genotype than induced responses in both no‐choice and choice assays, but they also fed less and experienced higher mortality on plants previously damaged by weevils. In contrast to the pattern suggested by the field experiment, spittlebugs did consistently induce resistance against either weevils or caterpillars in the bioassay experiment. 5. These results support recent findings that show herbivore species can compete via induced plant responses. Additionally, a quantitative review of the literature demonstrates that plant genotype tends to be more important than interspecific competition among herbivores (plant‐mediated or otherwise) in affecting herbivore preference and performance.     

Herbivory on planted oak seedlings across a habitat edge created by timber harvest

Edge habitats create environmental gradients that affect plant community composition and herbivore behavior. Silvicultural disturbance creates edge habitat with direct (via changes in light) and indirect (via changes in herbivore behavior) consequences for the growth and survival of tree seedlings, and thus, the composition of the future forest stands. Herbivores, particularly ungulates, can be a major limiting factor in oak regeneration, and silvicultural disturbance may alter the abundance or behavior of herbivores following harvest. We measured the severity of herbivory on experimentally planted white (Quercus alba) and black oak (Quercus velutina) seedlings by white-tailed deer (Odocoileus virginianus) and eastern cottontail rabbits (Sylvilagus floridanus), as well as foliar damage from insects, across gradients created by clearcuts in a deciduous forest in Indiana, USA. Overall browse pressure on oaks was low in our study. Nonetheless, spatial variation in herbivory depended on herbivore taxa; herbivory by rabbits was highest inside harvest openings, whereas foliar damage by insects peaked in the forest. Intensity of deer herbivory was constant across the edge. In addition, we observed indirect interactions among herbivore species mediated by a seedling’s browsing history. Herbivore damage by deer was positively related to past browsing by rabbits, and foliar damage from insects was positively related to past browsing by both deer and rabbits. Increasing woody plant competition reduced herbivory on seedlings by both deer and rabbits. Given the lack of spatial variability in deer herbivory and low overall herbivory by rabbits, we suspect that interactions between timber harvesting and herbivory did not have a strong impact on oak seedlings at our study sites.     

No evidence for an ‘evolution of increased competitive ability’ for the invasive Lepidium draba

The ‘evolution of increased competitive ability’ (EICA) hypothesis states that reduced herbivory in the introduced range causes an evolutionary shift in resource allocation from herbivore defense to growth. Therefore, according to EICA, introduced genotypes are expected to grow more vigorously than conspecific native genotypes when cultivated under common standardized conditions. The EICA hypothesis also assumes that herbivores will perform better on introduced genotypes compared to native genotypes, because they are less well defended. However, selection for either defense or growth will depend on the type of defense (quantitative or qualitative) employed by the plant, and whether the plant is released from generalist or specialist herbivores. The predictions of the EICA hypothesis might be reversed if a plant experiences increased generalist herbivore pressure in the introduced range, and therefore invests more in qualitative defense. We examined this idea with the invasive perennial mustard, Lepidium draba. We grew a total of 16 populations of L. draba from both its native European and introduced western US ranges under common conditions in a greenhouse. We also tested for differences in plant resistance to the specialist herbivore, Psylliodes wrasei, by conducting a leaf disc feeding bioassay with native and introduced L. draba genotypes. Furthermore, we quantified the generalist herbivore load on L. draba in both ranges in order to assess the selection pressure for increased qualitative defense. Contrary to the original EICA prediction, all plant traits (biomass, number of shoots, length and diameter of longest leaf) tended to be greater for the native, rather than introduced L. draba genotypes. There was no significant difference in the proportion of leaf area consumed by the specialist herbivore between native and introduced genotypes. The generalist herbivore load on L. draba was significantly greater in the introduced range. Our data suggest that the EICA hypothesis does not explain the invasion success of L. draba in the US. Instead, we propose that the reduced vigor of introduced genotypes may be due to selection for increased defense against generalist herbivores in the introduced range.     

Plant genotypic diversity reduces the rate of consumer resource utilization

While plant species diversity can reduce herbivore densities and herbivory, little is known regarding how plant genotypic diversity alters resource utilization by herbivores. Here, we show that an invasive folivore—the Japanese beetle (Popillia japonica)—increases 28 per cent in abundance, but consumes 24 per cent less foliage in genotypic polycultures compared with monocultures of the common evening primrose (Oenothera biennis). We found strong complementarity for reduced herbivore damage among plant genotypes growing in polycultures and a weak dominance effect of particularly resistant genotypes. Sequential feeding by P. japonica on different genotypes from polycultures resulted in reduced consumption compared with feeding on different plants of the same genotype from monocultures. Thus, diet mixing among plant genotypes reduced herbivore consumption efficiency. Despite positive complementarity driving an increase in fruit production in polycultures, we observed a trade-off between complementarity for increased plant productivity and resistance to herbivory, suggesting costs in the complementary use of resources by plant genotypes may manifest across trophic levels. These results elucidate mechanisms for how plant genotypic diversity simultaneously alters resource utilization by both producers and consumers, and show that population genotypic diversity can increase the resistance of a native plant to an invasive herbivore.     

A herbivory-induced increase in the proportion of floating seeds in an invasive plant

It is important to determine the factors prompting seed dispersal because for plant species seed dispersal is the only opportunity to disperse into a new habitat. Previous studies showed that the maternal stress, such as high density and low nutrient levels, induces the adaptive plastic increase of the dispersal ability in seed heteromorphic plants. In this study, we examined whether herbivory can change the relative proportion of dispersal-related seed heteromorphism (floating or non floating seeds) in an invasive weed Ambrosia artemisiifolia. Because A. artemisiifolia often distributes in the riparian habitat, floating seeds might contribute to the long distance dispersal by hydrochory. Floating ability and seed weight were compared between plants damaged by a specialist herbivore Ophraella communa and undamaged plants. The damaged plants produced lighter and more likely floating seeds than the undamaged plants. However, multi-regression analysis revealed that the probability of floating was affected by seed weight but was not affected by herbivore treatment (damaged vs. undamaged plants). These results suggest that the increased proportion of floating seeds was not a direct response to the herbivore signal but an indirect response through the herbivore's effect on the reduction of seed weight. Plants damaged by herbivores might not only decrease seed production and quality but also increase the dispersal ability. These responses in dispersal ability against the herbivores might contribute to the spread of invasive plants.     

Changes in Defense of an Alien Plant Ambrosia artemisiifolia before and after the Invasion of a Native Specialist Enemy Ophraella communa

The evolution of increased competitive ability hypothesis (EICA) predicts that when alien plants are free from their natural enemies they evolve lower allocation to defense in order to achieve a higher growth rate. If this hypothesis is true, the converse implication would be that the defense against herbivory could be restored if a natural enemy also becomes present in the introduced range. We tested this scenario in the case of Ambrosia artemisiifolia (common ragweed) – a species that invaded Japan from North America. We collected seeds from five North American populations, three populations in enemy free areas of Japan and four populations in Japan where the specialist herbivore Ophraella communa naturalized recently. Using plants grown in a common garden in Japan, we compared performance of O. communa with a bioassay experiment. Consistent with the EICA hypothesis, invasive Japanese populations of A. artemisiifolia exhibited a weakened defense against the specialist herbivores and higher growth rate than native populations. Conversely, in locations where the herbivore O. communa appeared during the past decade, populations of A. artemisiifolia exhibited stronger defensive capabilities. These results strengthen the case for EICA and suggest that defense levels of alien populations can be recuperated rapidly after the native specialist becomes present in the introduced range. Our study implies that the plant defense is evolutionary labile depending on plant-herbivore interactions.     

Explaining differential herbivory in sun and shade: the case of Aristotelia chilensis saplings

Differential herbivory in contrasting environments is commonly explained by differences in plant traits. When several plant traits are considered, separate correlation analyses between herbivory and candidate traits are typically conducted. This makes it difficult to discern which trait best explain the herbivory patterns, or to avoid spurious inferences due to correlated characters. Aristotelia chilensis saplings sustain greater herbivory in shaded environments than in open habitats. We measured alkaloids, phenolics, trichomes, leaf thickness and water content in the same plants sampled for herbivory. We conducted a multiple regression analysis to estimate the relationship between herbivory and each plant trait accounting for the effect of correlated traits, thus identifying which trait(s) better explain(s) the differential herbivory on A. chilensis. We also estimated insect abundance in both light environments. Palatability bioassays tested whether leaf consumption by the main herbivore on A. chilensis was consistent with field herbivory patterns. Overall insect abundance was similar in open and shaded environments. While saplings in open environments had thicker leaves, lower leaf water content, and higher concentration of alkaloids and phenolics, no difference in trichome density was detected. The multiple regression analysis showed that leaf thickness was the only trait significantly associated with herbivory. Thicker leaves received less damage by herbivores. Sawfly larvae consumed more leaf tissue when fed on shade leaves. This result is consistent with field herbivory and, together with results of insect abundance, renders unlikely that the differential herbivory in A. chilensis was due to greater herbivory pressure in open habitats.     

Non-Photochemical Quenching Capacity in Arabidopsis thaliana Affects Herbivore Behaviour

Under natural conditions, plants have to cope with numerous stresses, including light-stress and herbivory. This raises intriguing questions regarding possible trade-offs between stress defences and growth. As part of a program designed to address these questions we have compared herbivory defences and damage in wild type Arabidopsis thaliana and two “photoprotection genotypes”, npq4 and oePsbS, which respectively lack and overexpress PsbS (a protein that plays a key role in qE-type non-photochemical quenching). In dual-choice feeding experiments both a specialist (Plutella xylostella) and a generalist (Spodoptera littoralis) insect herbivore preferred plants that expressed PsbS most strongly. In contrast, although both herbivores survived equally well on each of the genotypes, for oviposition female P. xylostella adults preferred plants that expressed PsbS least strongly. However, there were no significant differences between the genotypes in levels of the 10 most prominent glucosinolates; key substances in the Arabidopsis anti-herbivore chemical defence arsenal. After transfer from a growth chamber to the field we detected significant differences in the genotypes’ metabolomic profiles at all tested time points, using GC-MS, but no consistent “metabolic signature” for the lack of PsbS. These findings suggest that the observed differences in herbivore preferences were due to differences in the primary metabolism of the plants rather than their contents of typical “defence compounds”. A potentially significant factor is that superoxide accumulated most rapidly and to the highest levels under high light conditions in npq4 mutants. This could trigger changes in planta that are sensed by herbivores either directly or indirectly, following its dismutation to H₂O₂.     

Leaf synchrony and insect herbivory among tropical tree habitat specialists

Growth defense tradeoff theory predicts that plants in low-resource habitats invest more energy in defense mechanisms against natural enemies than growth, whereas plants in high-resource habitats can afford higher leaf loss rates. A less-studied defense against herbivores involves the synchrony of leaf production, which can be an effective defense strategy if leaf biomass production exceeds the capacity of consumption by insects. The aim of this study was to determine whether leaf synchrony varied across habitats with different available resources and whether insects were able to track young leaf production among tree habitat specialists in a tropical forest of French Guiana. We predicted that high-resource habitats would exhibit more synchrony in leaf production due to the low cost and investment to replace leaf tissue. We also expected closer patterns of leaf synchrony and herbivory within related species, assuming that they shared herbivores. We simultaneously monitored leaf production and herbivory rates of five pairs of tree species, each composed of a specialist of terra firme or white-sand forests within the same lineage. Our prediction was not supported by the strong interaction of habitat and lineage for leaf synchrony within individuals of the same species; although habitat specialists differed in leaf synchrony within four of five lineages, the direction of the effect was variable. All species showed short time lags for the correlation between leaf production and herbivory, suggesting that insects are tightly tracking leaf production, especially for the most synchronous species. Leaf synchrony may provide an important escape defense against herbivores, and its expression appears to be constrained by both evolutionary history and environmental factors.     

Population differentiation related to climate of origin affects the intensity of plant–herbivore interactions in a clonal grass

With ongoing climate change, it is likely that shifts in species distribution ranges will lead to changes in the type and intensity of plant–herbivore interactions. Plants currently exposed to lower levels of herbivory could have less developed defensive mechanisms and therefore could suffer in case of increased herbivore pressure.We performed a common garden experiment using clones of Festuca rubra originating from four populations experiencing contrasting temperature and precipitation regimes. Clones of identical genotype were subjected to both the control and the herbivory treatment using larvae of the nymphalid butterfly Coenonympha pamphilus, a generalist herbivore feeding on several grass species. Various measures of constitutive and induced defence as well as growth response to herbivory were assessed, compared between populations of different climatic origin and related to herbivore performance (larval survival).The four F. rubra populations significantly differed in constitutive defence (content of Si and total phenols), nutritional quality (content of C) and inducibility of defence (change in total phenols), but not in growth response to herbivory. Herbivores survived better on populations from colder climate and better survival was generally related to lower Si content and lower initial plant size.We demonstrated population differentiation in both constitutive and induced defence against insect herbivory, which directly affected survival of a generalist herbivore. Our findings confirmed the expectation that plants from higher elevations are more prone to herbivory. Moreover, differences in various aspects of plant defence between populations from the same altitude stresses the need of considering multiple factors when assessing the effect of climate on plant–herbivore interactions.     

Herbivore‐induced plant responses in Brassica oleracea prevail over effects of constitutive resistance and result in enhanced herbivore attack

1. Plant responses to herbivore attack may have community‐wide effects on the composition of the plant‐associated insect community. Thereby, plant responses to an early‐season herbivore may have profound consequences for the amount and type of future attack. 2. Here we studied the effect of early‐season herbivory by caterpillars of Pieris rapae on the composition of the insect herbivore community on domesticated Brassica oleracea plants. We compared the effect of herbivory on two cultivars that differ in the degree of susceptibility to herbivores to analyse whether induced plant responses supersede differences caused by constitutive resistance. 3. Early‐season herbivory affected the herbivore community, having contrasting effects on different herbivore species, while these effects were similar on the two cultivars. Generalist insect herbivores avoided plants that had been induced, whereas these plants were colonised preferentially by specialist herbivores belonging to both leaf‐chewing and sap‐sucking guilds. 4. Our results show that community‐wide effects of early‐season herbivory may prevail over effects of constitutive plant resistance. Induced responses triggered by prior herbivory may lead to an increase in susceptibility to the dominant specialists in the herbivorous insect community. The outcome of the balance between contrasting responses of herbivorous community members to induced plants therefore determines whether induced plant responses result in enhanced plant resistance.     

Distributions of coral reef macroalgae in a back reef habitat in Moorea,French Polynesia

On tropical reefs where macroalgae are subjected to continuous herbivore pressure, spatial refuges typically are identified as large-scale, landscape interfaces that limit foraging behavior. However, algal distributions and community assemblages may also rely on the availability of smaller scale spatial refuges within the reef. The results of this study demonstrate that the patterns of macroalgal distribution across the back reef of Moorea, French Polynesia, are maintained by herbivores interacting with the small-scale structural complexities of the coral reef landscape. Although the majority of space available for colonization is composed of exposed surfaces, macroalgae rarely are found in the open. Instead, macroalgal occurrence is highest in the protected narrow crevices and hole microhabitats provided by massive Porites spp. coral heads. These distributions are determined initially by post-settlement mortality of young algal recruits in exposed habitats. Rates of consumption for two of the most common macroalgal species found in refuges across the back reef, Halimeda minima and Amansia rhodantha, indicate that algal recruits in exposed habitats are limited by herbivory. While algal abundance and community structure are highly dependent upon herbivore grazing, the availability of small-scale spatial refuges ultimately shapes the distinct community patterns and distributional boundaries of coral reef macroalgae in the back reefs of Moorea.