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.     

Responses of Caragana korshinskii to different aboveground shoot removal: combining defence and tolerance strategies

BACKGROUND AND AIMS: It is generally assumed that plants respond to natural enemies by either allocating resources to resistance traits or compensating for damage. This study evaluated how different methods of artificial shoot removal influence two alternative strategies (i.e. tolerance and defence) of Caragana korshinskii in the semi-arid area of China. METHODS: Zero per cent (control), 30% (30%) and 60% (60%) of the main shoot length and 25% (25%), 50% (50%) and 100% (100%) of the numbers of main shoots were removed from shrubs. KEY RESULTS: Moderate clipping treatments [30% removal of partial shoot length (RSL), 25% removal of shoot number (RSN) and 50% RSN] improved seed production, whereas the most intensive clipping treatments (60% RSL and 100% RSN) with most or total removal of potential flower buds reduced current reproduction fitness compared with controls. All treatments produced a similar leaf phenolic content, with the exception of 100% RSN which resulted in a low leaf phenolic content. In spite of a substantial investment in regrowth, clipped plants increased biomass allocation to physical defence. Control plants almost did not grow, had lower levels of physical defence and a lower photosynthetic rate, mobilized fewer carbohydrates from roots and produced more flowers. However, their current fitness was lower than that of plants undergoing clipping treatments (30% RSL, 25% RSN and 50% RSN) because of the high level of abortion of flowers and fruits. CONCLUSIONS: Caragana korshinskii responded to aboveground shoot removal through combining defence and tolerance strategies.     

The effects of herbivory and resource variability on the production of a second inflorescence by the desert lily, Pancratium sickenbergeri

We investigated the effects of herbivory by the dorcas gazelle, Gazella dorcas, on the production of a second inflorescence in a desert lily, Pancratium sickenbergeri (Amaryllidaceae), after the first inflorescence was eaten. In three populations exposed to different levels of herbivory, we conducted an inflorescence-clipping experiment in the flowering seasons of 1997, 1998 and 1999. The experiment was performed on inflorescences at both the emerging stage and the anthesis stage. Plants in each control group were undamaged. Clipped plants had a greater probability of producing a second inflorescence stalk than unclipped plants. In all the populations, the probability of producing a second inflorescence was greater when the first inflorescence was cut in the emerging stage than when it was cut in anthesis, indicating that there was a cost of compensation. In the population with the highest level of herbivory, the production of a second inflorescence stalk was related to resource availability in all 3 years. Plants produced as many flowers or fruits on the second stalk as on the first, indicating that potential reproductive output is double that usually achieved. Although we found no evidence for a trade-off between investment in first and second inflorescence stalks, the lower probability of producing a second inflorescence if heavy investment had been made in the first inflorescence indicates that compensation is costly. These results contradict the mutualism hypothesis that herbivory is beneficial to plants and provide support for the trade-off hypothesis that benefits of herbivory are proximal and are attained at an evolutionary cost.     

Plant defence signals and Batesian mimicry

In a game theory context, we investigated conditions for an evolutionarily stable equilibrium of defended, signalling plants, and plants mimicking these signals – that is, conditions for a stable mimicry complex. We modelled this in three steps. First, we analysed conditions for selection for defended, signalling plants, in a population of undefended plants. Second, we analysed conditions for when mimicking plants can invade a population of defended, signalling plants, leading to a stable equilibrium between the two strategies. Third, we analysed how sampling of signalling plants by herbivores affects the equilibrium between the strategies. The predictions show that mimicry of plant defence signals may be common, and even imperfect mimics could invade a population of defended, signalling plants. Whether the latter prediction holds or not depends on how herbivores generalize over signals, and on the length of their avoidance sequence'. The length of the avoidance sequence is the number of signalling plants that a herbivore avoids to attack, after attacking a defended plant. If herbivores always sample signalling plants, then mimicry cannot evolve, whereas if herbivores have a long avoidance sequence, this may allow selection even for imperfect mimics.     

Plant defence and stochastic risk of herbivory

Summary The influence of risk of herbivory and its variation in time on the optimal defence strategy in plants is analysed by a simple optimization model. We contrast two possible defence strategies; a constitutive defence with an invariant defence level in time and an idealized induced defence, that is, a strategy that adjusts the defence level to the prevailing risk of herbivory. We also take into account effects of the efficiency of the defence. If there is no variation in risk of herbivory over years, constitutive and induced defence should have the same expected optimal defence level and both strategies are equally fit. The optimal defence level increases as the maximum fecundity and the adult to juvenile survival ratio of the plants both increase. If the risk of herbivory varies stochastically, the expected optimal level of the constitutive defence is either increased or unaffected by the variation, whereas the induced defence strategy may result in both higher or lower expected optimal defence levels as variance increases. This outcome is dependent on the mean risk of herbivory. It also depends on the defence efficiency, i.e. the shape (convex, concave or linear) of the defence function that relates the probability of survival if encountered by a herbivore to defence level. Thus, the defence level of plants interacting with variable herbivore populations cannot be unambiguously predicted unless the defence strategy (constitutive or induced), mean risk of herbivory, the form of the defence function and plant life history are known.     

Phytoplankton defence mechanisms: traits and trade‐offs

In aquatic ecosystems, unicellular algae form the basis of the food webs. Theoretical and experimental studies have demonstrated that one of the mechanisms that maintain high diversity of phytoplankton is through predation and the consequent evolution of defence mechanisms. Proposed defence mechanisms in phytoplankton are diverse and include physiological (e.g. toxicity, bioluminescence), morphological (e.g. silica shell, colony formation), and behavioural (e.g. escape response) traits. However, the function of many of the proposed defence mechanisms remains elusive, and the costs and benefits (trade‐offs) are often unquantified or undocumented. Here, we provide an overview of suggested phytoplankton defensive traits and review their experimental support. Wherever possible we quantify the trade‐offs from experimental evidence and theoretical considerations. In many instances, experimental evidence suggests that defences are costless. However, we argue that (i) some costs materialize only under natural conditions, for example, sinking losses, or dependency on the availability of specific nutrients, and (ii) other costs become evident only under resource‐deficient conditions where a rivalry for limiting resources between growth and defence occurs. Based on these findings, we suggest two strategies for quantifying the costs of defence mechanisms in phytoplankton: (i) for the evaluation of defence costs that are realized under natural conditions, a mechanistic understanding of the hypothesized component processes is required; and (ii) the magnitude of the costs (i.e. growth reduction) must be assessed under conditions of resource limitation.     

Responses to simulated herbivory and water stress in two tropical C4 grasses

Summary The African grass Hyparrhenia rufa has established itself successfully in South American savannas (Llanos) and displaced dominant native grasses such as Trachypogon plumosus from the wetter and more fertile habitats. Several ecophysiological traits have been related to the higher competitive capacity of H. rufa. To further analyze the behavior of both species, their growth, biomass allocation, physiological and architectural responses to defoliation and water stress were compared under controlled conditions. Although total, aerial and underground biomass decreased under defoliation in both grasses, increases in clipped-leaf biomass and area compensated for defoliation in H. rufa but not in T. plumosus. This difference was due mainly to a higher proportion of assimilates being directed to leaf and tiller production and a higher leaf growth rate in the African grass as compared to T. plumosus, which showed incrased senescence under frequent defoliation. In both species, water stress ameliorated the effects of defoliation. The ability to compensate for defoliated biomass in H. rufa is possibly related to its long coevolution with large herbivores in its original African habitat and is apparently one of the causes of its success in Neotropical savannas.     

Silicon as a plant defence against insect herbivory: response to Massey, Ennos and Hartley

1. Silicon (Si) has received increased attention as a nutrient capable of providing some measure of defence for plants against fungal pathogens, and insect and mammalian herbivores. 2. On the basis of a study including two generalist insect folivores and a phloem feeder, Massey, Ennos & Hartley (2006; Journal of Animal Ecology, 75, 595-603) have drawn attention to a putative distinction between the effects of plant Si in defending against folivorous and phloem-feeding insects. On the basis of their results they imply that phloem feeders are less likely to be adversely affected by increased plant Si than folivores. 3. However, in making this suggestion, Massey et al. have ignored many previous studies demonstrating a clear effect of plant Si on a range of phloem-feeding and some xylem-feeding insects, and that this effect stems not only from leaf mechanical properties based on opaline silica, but also from induced chemical defences seemingly mediated by soluble Si. 4. Furthermore, Massey et al. cannot claim that their study was the first demonstration of a direct effect of Si on insect herbivore preference and performance; there have been numerous earlier studies demonstrating this from folivores, stem borers, and phloem and xylem feeders. 5. We contend that current evidence indicates that Si is likely to be involved to a similar extent in enhancing resistance to all four insect feeding guilds and that any conclusion to the contrary is, at this stage, premature.     

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.     

Latitudinal variation in resistance and tolerance to herbivory in the perennial herb Lythrum salicaria is related to intensity of herbivory and plant phenology

Both the length of the growing season and the intensity of herbivory often vary along climatic gradients, which may result in divergent selection on plant phenology, and on resistance and tolerance to herbivory. In Sweden, the length of the growing season and the number of insect herbivore species feeding on the perennial herb Lythrum salicaria decrease from south to north. Previous common‐garden experiments have shown that northern L. salicaria populations develop aboveground shoots earlier in the summer and finish growth before southern populations do. We tested the hypotheses that resistance and tolerance to damage vary with latitude in L. salicaria and are positively related to the intensity of herbivory in natural populations. We quantified resistance and tolerance of populations sampled along a latitudinal gradient by scoring damage from natural herbivores and fitness in a common‐garden experiment in the field and by documenting oviposition and feeding preference by specialist leaf beetles in a glasshouse experiment. Plant resistance decreased with latitude of origin, whereas plant tolerance increased. Oviposition and feeding preference in the glasshouse and leaf damage in the common‐garden experiment were negatively related to damage in the source populations. The latitudinal variation in resistance was thus consistent with reduced selection from herbivores towards the northern range margin of L. salicaria. Variation in tolerance may be related to differences in the timing of damage in relation to the seasonal pattern of plant growth, as northern genotypes have developed further than southern have when herbivores emerge in early summer.     

Maize seedling morphology and defence hormone profiles,but not herbivory tolerance,were mediated by domestication and modern breeding

We addressed whether Zea seedling morphology relevant to performance, defence hormone profiles and tolerance of a phloem‐feeding, specialist herbivore were affected by two processes, plant domestication and modern breeding. Domestication effects were inferred through comparisons between Balsas teosintes (Zea mays parviglumis) and landrace maizes (Z. mays mays), and modern breeding effects through comparisons between landrace maizes and inbred maize lines. Specifically, we compared seedling forms (a composite measure of leaf length, average stem diameter, shoot wet weight, shoot dry weight, total root length, root wet weight, and root dry weight), shapes (forms scaled by seedling dry weight, a proxy for seedling size), and defence hormone profiles among Balsas teosinte and landrace and inbred line maizes, exposed or unexposed to feeding by Dalbulus maidis. Our results suggested that domestication as well as modern breeding strongly mediated both seedling form and shape. Form was more similar between landrace and inbred maize than between Balsas teosinte and landrace maize, suggesting that domestication affected seedling form more than modern breeding. In contrast, shape was more similar between Balsas teosinte and landrace maize than between landrace and inbred maizes, suggesting that modern breeding affected seedling shape more than domestication. Additionally, seedling shoot : root ratios appeared to have been mediated by domestication, but not by modern breeding. In broad terms, individual seedling structures relevant to seedling ecology in wild or managed environments, such as leaf and root lengths, and shoot and root masses, were enlarged with domestication and reduced with modern breeding. Herbivory did not affect seedling shape, but had a weak effect on form so that seedlings were slightly larger in the absence versus presence of D. maidis. Also, both domestication and modern breeding seem to have mediated seedling hormone profiles, with breeding more strongly mediating profiles than domestication. Jasmonic acid isoleucine (JA‐Ile) and salicylic acid (SA) were induced by herbivory in both teosinte and maize. The hormone profiles assays collectively suggested that domestication and modern breeding altered constitutive levels of SA, abscisic acid and JA‐related (JA‐Ile and oxo‐phytodienoic acid) hormone levels in seedlings, particularly by increasing the levels of SA and decreasing those of JA‐related hormones. Altogether, our results suggested that maize domestication and modern breeding significantly altered seedling form, shape, ecologically relevant morphological traits (e.g. leaf and root lengths, and shoot and root masses) and hormonal defences, but not tolerance of D. maidis herbivory.     

Use of gaseous 13NH3 administered to intact leaves of Nicotiana tabacum to study changes in nitrogen utilization during defence induction

Nitrogen‐13 (t_1/2 9.97 m), a radioactive isotope of nitrogen, offers unique opportunities to explore plant nitrogen utilization over short time periods. Here we describe a method for administering ¹³N as gaseous ¹³NH₃ to intact leaves of Nicotiana tabacum L. (cv Samsun), and measuring the labelled amino acids using radio high‐performance liquid chromatography (HPLC) on tissue extract. We used this method to study the effects of defence induction on plant nitrogen utilization by applying treatments of methyl jasmonate (MeJA), a potent defence elicitor. MeJA caused a significant increase relative to controls in key [¹³N]amino acids, including serine, glycine and alanine by 4 h post‐treatment, yet had no effect on ¹³NH₃ incorporation, a process that is primarily under the control of the glutamine synthatase/glutamate synthase pathway (GS/GOGAT) in cellular photorespiration. We suggest that the reconfiguration of nitrogen metabolism may reflect induction of non‐photorespiratory sources of nitrogen to better serve the plant's defences.     

Silicon-augmented resistance of plants to herbivorous insects: a review

Silicon (Si) is one of the most abundant elements in the earth's crust, although its essentiality in plant growth is not clearly established. However, the importance of Si as an element that is particularly beneficial for plants under a range of abiotic and biotic stresses is now beyond doubt. This paper reviews progress in exploring the benefits at two‐ and three‐trophic levels and the underlying mechanism of Si in enhancing the resistance of host plants to herbivorous insects. Numerous studies have shown an enhanced resistance of plants to insect herbivores including folivores, borers, and phloem and xylem feeders. Silicon may act directly on insect herbivores leading to a reduction in insect performance and plant damage. Various indirect effects may also be caused, for example, by delaying herbivore establishment and thus an increased chance of exposure to natural enemies, adverse weather events or control measures that target exposed insects. A further indirect effect of Si may be to increase tolerance of plants to abiotic stresses, notably water stress, which can in turn lead to a reduction in insect numbers and plant damage. There are two mechanisms by which Si is likely to increase resistance to herbivore feeding. Increased physical resistance (constitutive), based on solid amorphous silica, has long been considered the major mechanism of Si‐mediated defences of plants, although there is recent evidence for induced physical defence. Physical resistance involves reduced digestibility and/or increased hardness and abrasiveness of plant tissues because of silica deposition, mainly as opaline phytoliths, in various tissues, including epidermal silica cells. Further, there is now evidence that soluble Si is involved in induced chemical defences to insect herbivore attack through the enhanced production of defensive enzymes or possibly the enhanced release of plant volatiles. However, only two studies have tested for the effect of Si on an insect herbivore and third trophic level effects on the herbivore's predators and parasitoids. One study showed no effect of Si on natural enemies, but the methods used were not favourable for the detection of semiochemical‐mediated effects. Work recently commenced in Australia is methodologically and conceptually more advanced and an effect of Si on the plants' ability to generate an induced response by acting at the third trophic level was observed. This paper provides the first overview of Si in insect herbivore resistance studies, and highlights novel, recent hypotheses and findings in this area of research. Finally, we make suggestions for future research efforts in the use of Si to enhance plant resistance to insect herbivores.     

Effects of plant quality and ant defence on herbivory rates in a neotropical ant‐plant

1. Understanding the degree to which populations and communities are limited by both bottom‐up and top‐down effects is still a major challenge for ecologists, and manipulation of plant quality, for example, can alter herbivory rates in plants. In addition, biotic defence by ants can directly influence the populations of herbivores, as demonstrated by increased rates of herbivory or increased herbivore density after ant exclusion. The aim of this study was to evaluate bottom‐up and top‐down effects on herbivory rates in a mutualistic ant‐plant. 2. In this study, the role of Azteca alfari ants as biotic defence in individuals of Cecropia pachystachya was investigated experimentally with a simultaneous manipulation of both bottom‐up (fertilisation) and top‐down (ant exclusion) factors. Four treatments were used in a fully factorial design, with 15 replicates for each treatment: (i) control plants, without manipulation; (ii) fertilised plants, ants not manipulated; (iii) unfertilised plants and excluded ants and (iv) fertilised plants and ants excluded. 3. Fertilisation increased the availability of foliar nitrogen in C. pachystachya, and herbivory rates by chewing insects were significantly higher in fertilised plants with ants excluded. 4. Herbivory, however, was more influenced by bottom‐up effects – such as the quality of the host plant – than by top‐down effects caused by ants as biotic defences, reinforcing the crucial role of leaf nutritional quality for herbivory levels experienced by plants. Conditionality in ant defence under increased nutritional quality of leaves through fertilisation might explain increased levels of herbivory in plants with higher leaf nitrogen.     

Below‐ground herbivory and root toughness: a potential model system using lignin‐modified tobacco

Plants exploit an array of defences against insect herbivores based on chemical and biomechanical properties. There is increasing evidence that plant toughness comprises a particularly effective defence against herbivory, yet studies to date have focussed exclusively on leaf toughness and folivore behaviour. The relationship between root mechanical properties and the chewing behaviour of a root‐feeding insect, the Agriotes spp. wireworm (Coleoptera: Elateridae L.), feeding on tobacco (Nicoiana tabacum) is investigated. Root toughness is manipulated using introduced transgenes for the down‐regulation of key enzymes in the lignin biosynthesis pathway: cinnamoyl‐CoA reductase (CCR line) and caffeate O‐methyltransferase and cinnamyl alcohol dehydrogenase (CO line). Two biomechanical analyses (i.e. conventional cutting and notched tensile) are conducted to quantify root toughness on both lines. Roots from the CO line are significantly tougher than those of the CCR line in terms of fracture toughness and fracture energy, although not for cutting energy or stiffness. Bioassays that compel wireworms to chew through roots demonstrate that only 30% can penetrate roots of the CO line compared with 90% on the CCR line. It takes wireworms over twice as long to penetrate roots from the CO line (8 h) compared with CCR roots (3.5 h). There is a statistically significant positive relationship between penetration time and fracture toughness evaluated with tensile tests, although not with cutting energy from cutting tests. Using this exploratory model system, it is concluded that root toughness derived from tensile tests is a practical indicator of the ability of root‐feeding insects to penetrate roots.     

Responses of morphological and physiological traits to herbivory by snails of three invasive and native submerged plants

3种入侵和本地沉水植物形态和生理性状对螺类牧食的响应 沉水植物水盾草(Cabomba caroliniana)已成为中国太湖流域的优势入侵水生植物。与外来物种的原产地环境相比,引入地新环境中存在的专食性天敌较少。外来物种可能会逃避其原产地环境中的天敌牧食,又因为它们的适口性相对较差,从而导致在引入地外来物种通常比本地物种遭受的牧食者影响更低(天敌逃逸假说)。本研究的目的是比较水盾草与共生的本地沉水植物对本地牧食者的响应。我们进行了一个中宇宙尺度实验,研究了水盾草和两种共生的本地沉水植物黑藻(Hydrilla verticillata)和穗花狐尾藻(Myriophyllum spicatum)对两种本地广食性腹足纲螺类萝卜螺(Radix swinhoei)和环棱螺(Sinotaia quadrata)的牧食响应。记录了它们的形态性状指标(总生物量、冠根比和相对生长率)和生理性状指标(叶片总非结构性碳、木质素和纤维素)。研究结果表明,环棱螺对3种沉水植物性状指标的影响较少。随着本地广食性螺类萝卜螺数量的增加,黑藻和穗花狐尾藻大部分植物性状发生了改变,而水盾草的植物性状表现出相对稳定的趋势。水盾草对萝卜螺的牧食更具抵抗力,这与天敌逃逸假说的假设一致。这一发现说明牧食性螺类促进了水盾草的入侵,这可能会改变沉水植物群落中的物种组成。