Leaf compensatory growth as a tolerance strategy to resist herbivory in Pancratium sickenbergeri

We examined the effects of leaf herbivory by the dorcas gazelle, Gazella dorcas, on the compensatory growth of the geophyte Pancratium sickenbergeri (Amaryllidaceae) in the Negev desert, Israel. In three populations exposed to different levels of herbivory, we removed different amounts of photosynthetic leaf area from plants in five clipping treatments: 0, 25, 50%-dispersed over all leaves, 50%-entire area of half the leaves, 100%. The population with the lowest level of herbivory showed the lowest relative regrowth rate after clipping. In the population with a constantly high level of herbivory, plants in intermediate-clipping treatments overcompensated in leaf area after clipping. For all the populations, clipped plants produce more new leaves than unclipped plants. In the population with the highest level of herbivory, clipping treatments did not have a significant effect on the number of fruits per plant. In addition, we did not find a trade-off between investments in growth and reproduction in this population. Our results indicated that, in the desert lily, herbivores may select for plant mechanisms that compensate after damage as a tolerant strategy to maintain fitness.     

On quantifying tolerance of herbivory for comparative analyses

As the evolutionary importance of plant tolerance of herbivory is increasingly appreciated, more and more studies are not just measuring a plant's tolerance, but are comparing tolerance among plant genotypes, populations, species, and environments. Here, we suggest that caution must be taken in such comparative studies in the choice of measurement scales (and data transformations) for damage levels and plant performance. We demonstrate with a simple scenario of two plant groups of equal tolerance how the choice of scales can lead one to infer that the first group is more tolerant, the second group is more tolerant, or the two groups are equally tolerant-using the identical dataset. We conclude that to make reliable, logically consistent inferences when comparing tolerances among groups of plants, damage and performance should both be on an additive scale or both on a multiplicative scale.     

A field enclosure apparatus for measuring crop photosynthesis

The field enclosure is a transparent box covering a soil area of 1.5 m². It is a semi-closed system in which concentrations of water vapour and carbon dioxide are maintained constant: the required rate of input of carbon dioxide being a measure of the photosynthesis rate, and the rate of condensation of water, on cooling coils, a measure of transpiration. The air within the enclosure is circulated rapidly by fans to decrease concentration gradients, and under steady radiation inputs the air temperature is controlled to ±0.5 °C. Both photosynthesis and transpiration rates are corrected for air exchange with the surroundings, as measured through the injection of the inert gas, nitrous oxide.     

Ontogenetic changes in tolerance to herbivory in Arabidopsis

Tolerance to herbivory—the ability of plants to maintain fitness despite herbivore damage—is expected to change during the life cycle of plants because the physiological mechanisms underlying tolerance to herbivory are linked to growth, and resource allocation to growth changes throughout ontogeny. We used the model plant Arabidopsis thaliana to test two hypotheses: that tolerance increases as plants grow, and that tolerance decreases at the onset of reproduction. We chose three accessions previously reported to vary for resistance to herbivory in order to explore whether tolerance and resistance are inversely related. Cabbage looper (Trichoplusia ni) larvae were allowed to feed on plants at either the four-leaf, six-leaf, or 1st-flower developmental stage until 50% of the leaf area was removed. Overall, we found a trend for increased tolerance with ontogenetic stage, but there were important differences among accessions in their response to herbivory at different stages. Tolerance did not decrease with the onset of flowering, nor did we find any correlation between resistance and tolerance levels. Three main plant traits correlated strongly with tolerance: stem mass, an earlier onset of reproduction and a longer fruiting period. This study suggests there may be considerable variation in ontogenetic patterns of tolerance in natural populations of A. thaliana, and warrants further investigations with more accessions or natural populations, and detailed measurements of traits purported to contribute to tolerance in our quest to understand the mechanisms of tolerance to herbivory.     

Corymbia leaf oils,latitude, hybrids and herbivory: A test using common‐garden field trials

Foliar oils, particularly monoterpenes, can influence the susceptibility of plants to herbivory. In plants, including eucalypts, monoterpenes are often associated with plant defence. A recent analysis revealed an increase in foliar oil content with increasing latitudinal endemism, and we tested this pattern using three eucalypt taxa comprising a latitudinal replacement cline. We also examined the relative concentrations of two monoterpenes (α‐pinene and 1,8‐cineole), for which meta‐analyses also showed latitudinal variation, using hybrids of these three taxa with Corymbia torelliana. These, and pure C. torelliana, were then assessed in common‐garden field plots for the abundance and distribution of herbivory by four distinct herbivore taxa. Differing feeding strategies among these herbivores allowed us to test hypotheses regarding heritability of susceptibility and relationships to α‐pinene and 1,8‐cineole. We found no support for an increase in foliar oil content with increasing latitude, nor did our analysis support predictions for consistent variation in α‐pinene and 1,8‐cineole contents with latitude. However, herbivore species showed differential responses to different taxa and monoterpene contents. For example, eriophyid mites, the most monophagous of our censused herbivores, avoided the pure species, but fed on hybrid taxa, supporting hypotheses on hybrid susceptibility. The most polyphagous herbivore (leaf blister sawfly Phylacteophaga froggatti) showed no evidence of response to plant secondary metabolites, while the distribution and abundance patterns of Paropsis atomaria showed some relationship to monoterpene yields.     

A test of the compensatory continuum: fertilization increases and below-ground competition decreases the grazing tolerance of tall wormseed mustard (Erysimum strictum)

Contrary to the general expectation, the compensatory continuum hypothesis proposes that grazing may not always affect plant performance adversely. Instead, the effects may vary from negative (undercompensation) to positive (overcompensation), depending on the local availability of resources and the intensity of competition experienced by individual plants. We tested this hypothesis in a common garden experiment by growing tall wormseed mustard, Erysimum strictum, under a factorial design involving simulated grazing (0, 10, or 50% of the main stem clipped), supplemental fertilization and below-ground competition. The results supported the hypothesis. On an average, fertilization increased and competition decreased plant performance. Overcompensation was only observed among the fertilized plants growing free of competition. Simulated grazing increased seed yield 1.6 (10% clipping) and 1.4 times (50% clipping) as compared to unclipped plants when the plants were grown with fertilization and without competition. In contrast, clipping did not significantly increase seed yield in the plants grown without fertilization and/or with competition. The breakage of apical dominance provides a proximate mechanism of these regrowth responses. This is consistent with the fact that most plants (85%) had an unbranched shoot architecture in our study population. However, it is not clear why E. strictum has a relatively unbranched architecture in natural populations. We briefly discuss the alternative ecological factors – competition for light, adaptation to herbivory and optimal timing of flowering as a bet-hedging strategy in monocarpic plants – which might maintain unbranched architecture in this species. This revised version was published online in July 2006 with corrections to the Cover Date.     

Optimal distribution of herbivory and localized compensatory responses within a plant

Because the impact of induced resistance on herbivores is often too small to have a considerable impact on herbivore populations, it has been suggested that the function of defenses is not necessarily to affect herbivore densities per se, but to spread the damage evenly throughout a plant. Some observations suggest that evenly-distributed herbivory results in a smaller decrease in growht and reproduction than the same level of herbivory concentrated on only one part of the canopy. One possible reason for this is that plant parts are able to compensate for small amounts of local damage spread all over the plant but not for larger concentrated damage of the same extent because of the of resource distribution patterns in a plant.Models were constructed to analyze how to optimally distribute damage among modules so that the total performance (growth, subsequent reproduction) of a plant, measured as the sum of the module performances, is maximized. According to the models, spreading damage is profitable when the performance of all or most modules decreases slowly with small damage levels and then faster as damage increases. In addition, the pattern of resource movement between modules must be tolerant to damage. It is proposed a hypothesis that the resource distribution system is often tolerant to at least small or moderate total damage levels, since there are several alternative pathways of movement for assimilates and water through the plant's structure.It has been suggested that defense and compensatory growth are alternative strategies for a plant in the struggle against herbivores. The present models suggest that they can also work together to increase fitness under herbivore pressure.     

Ontogenetic patterns in the mechanisms of tolerance to herbivory in Plantago

Background and Aims

Herbivory and plant defence differ markedly among seedlings and juvenile and mature plants in most species. While ontogenetic patterns of chemical resistance have been the focus of much research, comparatively little is known about how tolerance to damage changes across ontogeny. Due to dramatic shifts in plant size, resource acquisition, stored reserves and growth, it was predicted that tolerance and related underlying mechanisms would differ among ontogenetic stages.

Methods

Ontogenetic patterns in the mechanisms of tolerance were investigated in Plantago lanceolata and P. major (Plantaginaceae) using the genetic sib-ship approach. Pot-grown plants were subjected to 50 % defoliation at the seedling, juvenile and mature stages and either harvested in the short-term to look at plasticity in growth and photosynthesis in response to damage or allowed to grow through seed maturation to measure phenology, shoot compensation and reproductive fitness.

Key Results

Tolerance to defoliation was high in P. lanceolata, but low in P. major, and did not vary among ontogenetic stages in either species. Mechanisms underlying tolerance did vary across ontogeny. In P. lanceolata, tolerance was significantly related to flowering (juveniles) and pre-damage shoot biomass (mature plants). In P. major, tolerance was significantly related to pre-damage root biomass (seedlings) and induction of non-photochemical quenching, a photosynthetic parameter (juveniles).

Conclusions

Biomass partitioning was very plastic in response to damage and showed associations with tolerance in both species, indicating a strong role in plant defence. In contrast, photosynthesis and phenology showed weaker responses to damage and were related to tolerance only in certain ontogenetic stages. This study highlights the pivotal role of ontogeny in plant defence and herbivory. Additional studies in more species are needed to determine how seedlings tolerate herbivory in general and whether mechanisms vary across ontogeny in consistent patterns.     

Variation in Arundo donax stem and leaf strength: Implications for herbivory

We determined leaf and stem strength for Arundo donax from plants grown in different geographic areas and at different times within their growing cycle. Mean leaf strength for plants collected within California was 1.72 Newtons (N) and ranged from 0.36 to 6.32 N, based on 1170 individual determinations. For leaves collected from 30 plants within four states between July 11 and 20, 2007, mean leaf strength was 1.58 N based on 936 determinations. Values ranged from 0.24 to 4.90 N. Overall, leaf strength showed statistically significant changes depending on the sampling date, sampling location, type of leaf sampled, and position within the leaf where the measurement was taken. In general leaf strength was greater near the base of the leaf and decreased with distance away from the base; leaf strength changed as the growing season progressed; and first year leaves had leaf strength values about 25% greater than leaves produced on stems >1-year old. This represents two of the three age categories of leaves which may be present on giant reed at any one time. Stem strength and stem wall thickness were strongly correlated (Kendall's Tau b = 0.92, P < 0.0001, N = 26). Linear regression indicated that mean stem strength decreased by approximately 6.8% (95% confidence limits 5.8-7.7%) from one node to the successive node progressing from the stem base to the shoot tip. These results imply that the ability of biological control agents to damage A. donax leaves may not be the same across the locations this plant occurs or at all times during the growing season within a given location.     

Importance of tolerance to herbivory for plant survival in a British grassland

Question: Is plant capacity to regrow under different herbivore treatments related to herbivore increaser/decreaser plant status? Location: Grassland in Southeast England (GR 41/944691). Methods: A field experiment was established in order to understand the role of plant tolerance to herbivory in explaining the abundance of nine grassland species previously known as herbivore increasers or decreasers. Tolerance was measured as a plant's capacity to regrow after exposure to herbivores. The experiment was designed to measure the impact of rabbits, molluscs, insects and clipping (artificial damage). Plants were propagated by stolons, exposed to different treatments in the field and then allowed to recover in the greenhouse for a month. Results: Previous studies have stated that plants that are able to persist in a herbivore environment could be tolerant or resistant, in agreement with the later our results showed that rabbit increaser plants were tolerant to herbivory in terms of biomass regrowth. Nonetheless, insect and mollusc increasers did not show any particular pattern related to plant compensation and some decreaser species were intolerant. Conclusions: This study shows that tolerance to herbivory could be an important mechanism for rabbit increaser species survival in grazed ecosystems.     

Allocating nitrogen away from a herbivore: a novel compensatory response to root herbivory

Centaurea maculosa, an invasive North American plant species, shows a high degree of tolerance to the root-boring biocontrol herbivore, Agapeta zoegana. For example, infested individuals of C. maculosa often exhibit more rigorous growth and reproduction compared with their non-infested counterparts. Compensatory responses to aboveground herbivores often involve increases in leaf area and/or photosynthetic capacity, but considerably less is known about root system compensatory responses to belowground herbivory. We used a ¹⁵N labeling approach to evaluate whether compensatory adjustments in N acquisition via changes in root morphology and/or physiological uptake capacity could explain the ability of C. maculosa to tolerate root herbivory. Root herbivory reduced whole plant N uptake by more than 30% and root uptake capacity by about 50%. Despite a marked reduction in N procurement, herbivory did not affect total biomass or shoot N status. Infested plants maintained shoot N status by shifting more of the acquired N from the root to the shoot. To our knowledge, shifting N allocation away from a root herbivore has not been reported and provides a plausible mechanism for the host plant to overcome an otherwise devastating effect of a root herbivore-induced N deficit.     

A test method for pesticide tolerance in minute parasiticHymenoptera

In contrast to many pest species, important biological control agents have only rarely been found to be pesticide resistant. Biochemical and ecological mechanisms have been implicated, but lack of toxicological techniques suitable for the minute and fragile insects concerned may limit screening and research projects. Standard techniques are criticized, and a method utilizing controlled access to pesticidecontaining sucrose solutions is described. The method was used to test tolerance ofAphytis holoxanthus to malathion, and is suggested for screening and selection experiments with this and similar species.      

Indirect suppression of photosynthesis on individual leaves by arthropod herbivory

BACKGROUND: Herbivory reduces leaf area, disrupts the function of leaves, and ultimately alters yield and productivity. Herbivore damage to foliage typically is assessed in the field by measuring the amount of leaf tissue removed and disrupted. This approach assumes the remaining tissues are unaltered, and plant photosynthesis and water balance function normally. However, recent application of thermal and fluorescent imaging technologies revealed that alterations to photosynthesis and transpiration propagate into remaining undamaged leaf tissue. SCOPE AND CONCLUSIONS: This review briefly examines the indirect effects of herbivory on photosynthesis, measured by gas exchange or chlorophyll fluorescence, and identifies four mechanisms contributing to the indirect suppression of photosynthesis in remaining leaf tissues: severed vasculature, altered sink demand, defence-induced autotoxicity, and defence-induced down-regulation of photosynthesis. We review the chlorophyll fluorescence and thermal imaging techniques used to gather layers of spatial data and discuss methods for compiling these layers to achieve greater insight into mechanisms contributing to the indirect suppression of photosynthesis. We also elaborate on a few herbivore-induced gene-regulating mechanisms which modulate photosynthesis and discuss the difficult nature of measuring spatial heterogeneity when combining fluorescence imaging and gas exchange technology. Although few studies have characterized herbivore-induced indirect effects on photosynthesis at the leaf level, an emerging literature suggests that the loss of photosynthetic capacity following herbivory may be greater than direct loss of photosynthetic tissues. Depending on the damage guild, ignoring the indirect suppression of photosynthesis by arthropods and other organisms may lead to an underestimate of their physiological and ecological impacts.     

Snail herbivory on submerged macrophytes and nutrient release: Implications for macrophyte management

Radix swinhoei (H. Adams) is a freshwater snail commonly found in shallow regions of Lake Taihu. This research estimated, based on experiments, the consumption rates of R. swinhoei on three young submerged plants (Vallisneria spiralis, Hydrilla verticillata and Potamogeton malaianus) and its rates of nutrient release. Results showed that the snails consumed V. spiralis at the highest rate (23.34 mg g⁻¹ d⁻¹), P. malaianus at a lower rate (11.97 mg g⁻¹ d⁻¹), and H. verticillata at the lowest rate (7.04 mg g⁻¹ d⁻¹). The consumption rates on V. spiralis varied significantly, with snail size, ranging from 13.63 mg g⁻¹ d⁻¹ for large-size snails to 143.42 mg g⁻¹ d⁻¹ for small-size ones.The average nutrient release rates of snails grazing on different macrophytes were 45.93 μg PO₄-P and 0.58 mg NH₄-N g⁻¹ d⁻¹. The food species had a significant effect on NH₄-N release rates but not on PO₄-P. However, the snail size had a significant effect on PO₄-P release rates and not on NH₄-N. The present study indicates that through selective grazing and nutrient release, snails may impose a significant impact on the macrophyte community, which should be considered in managing the macrophytes of a lake.     

Environmental dependency in the expression of costs of tolerance to deer herbivory

Plant tolerance to natural enemy damage is a defense strategy that minimizes the effects of damage on fitness. Despite the apparent benefits of tolerance, many populations exhibit intermediate levels of tolerance, indicating that constraints on the evolution of tolerance are likely. In a field experiment with the ivyleaf morning glory, costs of tolerance to deer herbivory in the form of negative genetic correlations between deer tolerance and fitness in the absence of damage were detected. However, these costs were detected only in the presence of insect herbivores. Such environmental dependency in the expression of costs of tolerance may facilitate the maintenance of tolerance at intermediate levels.     

The roots of defense: plant resistance and tolerance to belowground herbivory

Background

There is conclusive evidence that there are fitness costs of plant defense and that herbivores can drive selection for defense. However, most work has focused on above-ground interactions, even though belowground herbivory may have greater impacts on individual plants than above-ground herbivory. Given the role of belowground plant structures in resource acquisition and storage, research on belowground herbivores has much to contribute to theories on the evolution of plant defense. Pocket gophers (Geomyidae) provide an excellent opportunity to study root herbivory. These subterranean rodents spend their entire lives belowground and specialize on consuming belowground plant parts.

Methodology and Principal Findings

We compared the root defenses of native forbs from mainland populations (with a history of gopher herbivory) to island populations (free from gophers for up to 500,000 years). Defense includes both resistance against herbivores and tolerance of herbivore damage. We used three approaches to compare these traits in island and mainland populations of two native California forbs: 1) Eschscholzia californica populations were assayed to compare alkaloid deterrents, 2) captive gophers were used to test the palatability of E. californica roots and 3) simulated root herbivory assessed tolerance to root damage in Deinandra fasciculata and E. californica. Mainland forms of E. californica contained 2.5 times greater concentration of alkaloids and were less palatable to gophers than island forms. Mainland forms of D. fasciculata and, to a lesser extent, E. californica were also more tolerant of root damage than island conspecifics. Interestingly, undamaged island individuals of D. fasciculata produced significantly more fruit than either damaged or undamaged mainland individuals.

Conclusions and Significance

These results suggest that mainland plants are effective at deterring and tolerating pocket gopher herbivory. Results also suggest that both forms of defense are costly to fitness and thus reduced in the absence of the putative target herbivore.     

Attack frequency and the tolerance to herbivory of Neotropical savanna trees

Tolerance is the ability of a plant to regrow or reproduce following damage. While experimental studies typically measure tolerance in response to the intensity of herbivory (i.e., the amount of leaf tissue removed in one attack), the impact of how many times plants are attacked during a growing season (i.e., the frequency of damage) is virtually unexplored. Using experimental defoliations that mimicked patterns of attack by leaf-cutter ants (Atta spp.), we examined how the frequency of herbivory influenced plant tolerance traits in six tree species in Brazil’s Cerrado. For 2 years we quantified how monthly and quarterly damage influenced individual survivorship, relative growth rate, plant architecture, flowering, and foliar chemistry. We found that the content of leaf nitrogen (N) increased among clipped individuals of most species, suggesting that Atta influences the allocation of resources in damaged plants. Furthermore, our clipping treatments affected tree architecture in ways thought to promote tolerance. However, none of our focal species exhibited a compensatory increase in growth (increment in trunk diameter) in response to herbivory as relative growth rates were significantly lower in clipped than in unclipped individuals. In addition, the probability of survival was much lower for clipped plants, and lower for plants clipped monthly than those clipped quarterly. For plants that did survive, simulated herbivory dramatically reduced the probability of flowering. Our results were similar across a phylogenetically distinct suite of species, suggesting a potential extendability of these findings to other plant species in this system.