Timing of induced resistance in a clonal plant network

After local herbivory, plants can activate defense traits both at the damaged site and in undamaged plant parts such as in connected ramets of clonal plants. Since defense induction has costs, a mismatch in time and space between defense activation and herbivore feeding might result in negative consequences for plant fitness. A short time lag between attack and defense activation is important to ensure efficient protection of the plant. Additionally, the duration of induced defense production once the attack has stopped is also relevant in assessing the cost–benefit balance of inducible defenses, which will depend on the absence or presence of subsequent attacks. In this study we quantified the timing of induced responses in ramet networks of the stoloniferous herb Trifolium repens after local damage by Mamestra brassicae larvae. We studied the activation time of systemic defense induction in undamaged ramets and the decay time of the response after local attack. Undamaged ramets became defense‐induced 38–51 h after the initial attack. Defense induction was measured as a reduction in leaf palatability. Defense induction lasted at least 28 days, and there was strong genotypic variation in the duration of this response. Ramets formed after the initial attack were also defense‐induced, implying that induced defense can extend to new ramet generations, thereby contributing to protection of plant tissue that is both very vulnerable to herbivores and most valuable in terms of future plant growth and fitness.     

Short-term damage-induced increases in tobacco alkaloids protect plants

Summary Leaf damage significantly increases the alkaloid content in undamaged leaves on damaged field-grown wild tobacco plants. Although field-grown pot-bound plants fail to exhibit the same damage-induced increase in alkaloid content, the ability to respond to leaf damage is restored 6 days after removing plants from their pots. Freshly hatched Manduca sexta larvae reared individually in the laboratory on the high-alkaloid foliage of damaged plants released from their pots gain less weight and eat less (57.2% and 45.7% of controls, respectively) than larvae fed low-alkaloid foliage from undamaged released plants. Moreover, larvae grow equally well on the foliage of damaged and undamaged pot-bound plants. The higher chlorophyll contents characteristic of damaged released plants did not negate the effects of the increased alkaloid contents on larval growth. Undamaged leaves from undamaged field-grown plants stem-fed nicotine solutions had elevated leaf nicotine and nornicotine contents. Larvae reared on these artificially induced leaves gain only 38.5% of the weight gained by larvae reared on low-alkaloid foliage. These results demonstrate that damage-induced increases in leaf alkaloids protect induced foliage from attack and are sufficient to explain the decreased growth of caterpillars on the foliage of damaged plants.     

Interference among cotton neighbours after differential reproductive damage

In indeterminate plant species, the rate of vegetative growth usually declines during the stage of active reproductive growth. Fruit shedding, as induced by insect herbivores, could counteract this decline. Due to the relative increase in vegetative growth, plants that have suffered reproductive damage could be better able to intercept light and acquire soil resources than undamaged plants. If so, plants with damaged neighbours might grow less than their counterparts with smaller, undamaged neighbours. This hypothesis was tested in high- and low-density cotton crops subjected to three treatments: (i) undamaged controls; (ii) uniformly damaged, in which all plants were damaged; (iii) non-uniformly damaged, in which every second plant was damaged. Damaged plants had their flowerbuds and young fruits manually removed at 85 days after sowing to simulate shedding as induced by Helicoverpa spp. (Lepidoptera) and mirid bugs (Hemiptera). As expected, damaged plants had greater leaf area and more vegetative dry matter than undamaged ones. This was most pronounced at high plant density. Neighbour status did not affect vegetative growth but it had a substantial, asymmetric effect on the reproductive growth of target plants. Damaged targets recovered to the level of undamaged controls in terms of total fruit number but had a large reduction in the mass of mature fruit due to the limited time available for recovery. The effect of neighbour status, if any, on the production of mature fruit in damaged targets was overridden by the limit imposed to recovery by the duration of the growing season. In contrast, neighbour status affected the production of mature fruit of undamaged targets: undamaged targets with damaged neighbours had 34% (low density) and 56% (high density) less mature fruit mass than their counterparts with undamaged neighbours. This was because (i) reproductive allocation and (ii) the proportion of total fruit that reached maturity in target plants declined with increasing neighbour interference. Most studies dealing with changes in competitive relationships among plants subjected to differential herbivory have shown how undamaged plants may benefit from herbivores that feed on their neighbours. This study shows that differential reproductive damage can cause the opposite effect, as undamaged plants may have a significant reduction in productivity due to the influence of neighbours whose vegetative growth was stimulated by the loss of reproductive organs. Received: 2 June 1996 / Accepted: 8 September 1996     

Recovery of evergreen clonal dwarf shrubVaccinium vitis-idaea after simulated microtine herbivory in a boreal forest

The evergreen dwarf shrub lingonberry (Vaccinium vitis-idaea L.) was subjected to microtine herbivory simulations to investigate its recovery in a boreal forest. Beside the control (A), the study included three levels of herbivory: clipping of half the annual branches from 50% of ramets (B), removal of 50% of ramets (C), and removal of 100% of ramets (D). Density, growth, and fecundity of the ramets were monitored during the study. New ramets emerged rapidly from dormant basal buds at the base of the removed ramets in groups C and D. After three growth seasons, 60–117% and 42–112% of density and biomass, respectively, had been regained in the groups damaged relative to the control, the difference being insignificant between the treated groups apparently because of the small sample size. Survival, fecundity and net growth of ramets were not affected by the treatment. Mean dry weight of annual branches in new ramets was lower in the damaged groups than the control. The recovery of the lingonberry was unexpectedly good. The results suggest that, since natural herbivory seldom is as heavy as in this work, the time between population density peaks of microtine rodents is usually long enough for the lingonberry to recover in boreal ecosystems.     

Induced plant responses to multiple damagers: differential effects on an herbivore and its parasitoid

Herbivore-induced plants responses can affect the preference and performance of herbivores and their natural enemies. These responses may vary depending on the identity and number of herbivore species feeding on the plant so that when herbivores from different guilds feed on plants, the interactions between plants, herbivores, and natural enemies may be disrupted. Tomato plants were damaged either by the caterpillar Spodoptera exigua, or the aphid Macrosiphum euphorbiae, or damaged by both herbivores, or undamaged controls. We measured the preference and performance of S. exigua and its parasitoid Cotesia marginiventris, and activity of proteinase inhibitors (PI) as an indicator of induced resistance. Compared to undamaged plants, caterpillar damage reduced the number of eggs laid by S. exigua adults, reduced growth, consumption, and survival of larval S. exigua and C. marginiventris, and increased activity of PIs 43%; but did not increase attraction of C. marginiventris. While pupal mass of S. exigua was not affected, the pupal mass of C. marginiventris decreased on caterpillar-damaged plants compared to controls. In contrast, plants damaged by aphids were preferred for oviposition by S. exigua, and had increased larval consumption and survival, compared to controls. Aphid feeding did not affect the preference or performance of C. marginiventris, or PI activity, compared to controls. While oviposition was deterred on caterpillar-damaged plants, plants damaged by both herbivores received the same amount of oviposition as controls. The attraction of C. marginiventris to plants damaged by caterpillars and aphids was increased compared to controls. However, plants damaged by both herbivores had similar PI activity, larval growth and survival of S. exigua and C. marginiventris, as plants singly damaged by caterpillars. Overall, the preference component for both the herbivore and parasitoid was more strongly affected by damage due to multiple herbivores than the performance component.     

Defoliation effects on isoprene emission from Populus deltoides

Isoprene emission from plants is one of the principal ways in which plant processes alter atmospheric chemistry. Despite the importance of this process, few long-term controls over basal emission rates have been identified. Stress-induced changes in carbon allocation within the entire plant, such as those produced by defoliation, have not been examined as potential mechanisms that may control isoprene production and emission. Eastern cottonwood (Populus deltoides) saplings were partially defoliated and physiological and growth responses were measured from undamaged and damaged leaves 7 days following damage. Defoliation reduced isoprene emission from undamaged and damaged leaves on partially defoliated plants. Photosynthetic rates and leaf carbon and nitrogen pools were unaffected by damage. Photosynthetic rate and isoprene emission were highly correlated in undamaged leaves on undamaged plants and damaged leaves on partially defoliated plants. There was no correlation between photosynthetic rate and isoprene emission in undamaged leaves on partially defoliated plants. Isoprene emission was also highly correlated with the number of source leaves on the apical shoot in damage treatments. Increased carbon export from source leaves in response to defoliation may have depleted the amount of carbon available for isoprene synthesis, decreasing isoprene emission. These results suggest that while isoprene emission is controlled at the leaf level in undamaged plants, emission from leaves on damaged plants is controlled by whole-branch allocation patterns. Received: 12 May 1998 / Accepted: 9 November 1998     

WATER SHARING AMONG RAMETS IN A DESERT POPULATION OF DISTICHLIS SPICATA (POACEAE)

Clonal growth enables plants to transport resources among separately rooted but connected ramets, a potential advantage in patchy or unpredictable habitats. Nevertheless, clonal plants are relatively scarce in deserts. To test whether clonal integration of water relations can increase plant performance under natural conditions in a desert species, water movement was traced and connection among ramets was manipulated in the rhizomatous grass Distichlis spicata in Death Valley, California. To examine potential costs of clonal growth form, connections were mapped and analyzed for dry mass and nitrogen content. Movement of dye showed potential transport of water among five ramets up to 1.4 m apart. Severance of connecting rhizomes increased mortality and decreased water potential of individual ramets within 36 hr, indicating that water sharing among ramets could be of significant benefit. However, plants had a high investment of mass and nitrogen in underground organs, which might be a cost of clonal growth associated with desert environments.     

Grazing tolerance of Gentianella amarella and other monocarpic herbs: why is tolerance highest at low damage levels?

Plants have adapted to compensate for the loss of vegetative biomass and reproductive potential caused by grazing. Shoot damage breaks down the correlative inhibition maintained by apical dominance. The consequent increased branching may lead to increased production of flowers and fruits in damaged plants, provided that enough resources, both in terms of meristems and nutrients, are available. In Gentianella amarella, the removal of the apex of the main stem (10% clipping) had no pronounced effect on branching and plant performance. In one of the two study populations, however, apically damaged plants produced more fruits than undamaged control plants. The plants also fully compensated for 50% removal of the main stem in terms of above-ground biomass, but their fruit production was reduced compared to control and apically damaged plants. After 75% clipping, fruit production was not significantly reduced compared to 50% clipping. Consequently, G. amarella showed highest tolerance in the presence of minor shoot damage. The pattern is qualitatively similar in some other monocarpic species (Gentianella campestris, Erysimum strictum and Rhinanthus minor). Multiple constraints as well as selective forces may shape these compensatory responses: (1) A lack of basal meristems may constrain tolerance of high damage levels. (2) Species with basal meristems may have a potential to tolerate major damage, but a shortage of resources or otherwise unfavourable growth conditions may constrain their compensatory ability. (3) It may be adaptive to have maximum tolerance of low and moderate damage levels if chemical defences reduce the risk of extensive shoot damage as well as the risk of repeated grazing. (4) The compensatory ability of monocarpic species may be affected by selective forces that favour fast vertical growth early in the season and unbranched architecture in undamaged conditions. Therefore, it is not the mere grazing history, but also other factors associated with growth conditions that are required to explain the variation in grazing tolerance.     

Hurricane-induced modification of nitrogen and phosphorus resorption in an aspen clone: an example of diffuse disturbance

Summary On 27 September 1985, Hurricane Gloria intersected the Rhode Island land mass and disrupted normal autumnal element resorption in 20 ramets of a trembling aspen clone (Populus tremuloides). No mechanical injury to the plants was observed, but in contrast to undamaged aspens, the wind/salt-damaged aspens did not withdraw nitrogen (N) or phosphorus (P) from senescing leaves. There was actually 17% more N in abscising leaves than in presenescent, pre-hurricane leaves.     

Cotton compensatory growth after loss of reproductive organs as affected by availability of resources and duration of recovery period

Damaged cotton plants in which reproductive organs were manually removed to simulate shedding induced by Helicoverpa spp. (Lepidoptera) were compared with undamaged controls grown under contrasting availability of resources. Plant growth and partitioning were analysed and fruit mass was taken as a measure of compensation. Under high availability of resources (low plant density, high fertility) damaged plants had a large potential compensatory capacity due to increased vegetative growth that enhanced their ability to assimilate carbon and nitrogen with respect to undamaged controls. These plants shifted from vegetative to reproductive growth when they were allowed to set fruit in the recovery period. Actual compensation was complete, however, only when the duration and conditions of the recovery period were favourable. Under multiple stresses (high plant density, low fertility, low temperature), damage triggered a marked increase in the allocation of biomass to roots which was not reversed when plants were allowed to set fruit. The apparent shift in the allocation pattern of damaged plants under stress-which matches well the survival strategy described for many perennials-probably restricted compensatory fruit growth.     

An analysis of the costs and benefits of physiological integration between ramets in the clonal perennial herb Glechoma hederacea

Summary The costs and benefits, measured in terms of dry weight, of physiological integration between clonal ramets, were analysed in two experiments conducted on the clonal herb Glechoma hederacea. Firstly, integration between consecutively-produced ramets was examined in an experiment in which stolons grew from one set of growing conditions (either unshaded or shaded and either nutrient-rich or nutrient-poor) into conditions in which light or nutrient level was altered. Comparisons were made between the dry weight of the parts of the clones produced before and after growing conditions were changed, and the dry weights of the corresponding part of control clones subjected to constant growing conditions. In a second experiment, integration between two distinct parts of G. hederacea clones was investigated. In this experiment clones were grown from two connected parent ramets and the parts of the clone produced by each parent ramet were subjected independently to either nutrient-rich or nutrient-poor conditions. Ramets in resource-rich conditions provided considerable physiological support to those in resource-poor conditions. This was measured as a dry weight gain compared with the weight of the corresponding part of the control clones growing in resource-poor conditions. However, when stolons grew from resource-poor conditions into resource-rich conditions, there was no similar evidence of the resourcepoor ramtes receiving support from resource-rich ramets. Physiological integration did not result in dry weight gains when this would have necessitated basipetal translocation of resources.Because of the predominantly acropedal direction of movement of translocates in G. hederacea, the structure of the clone was important in determining the effectiveness of integration between ramets. Where physiological integration was effective, the cost to the supporting ramets in terms of dry weight was insignificant. Physiological integration allows clones to maintain a presence in less favourable sites with insignificant cost to ramets in favourable sites, thereby reducing the probability of invasion by other plants, and providing the potential for rapid clonal growth if conditions improve. Integrated support of ramets in unfavourable conditions also enables the clone to grow through unfavourable sites, thus increasing the probability of encountering more favourable conditions by wider foraging.     

Reciprocal transport between ramets increases growth of Fragaria chiloensis when light and nitrogen occur in separate patches but only if patches are rich

Summary Fragaria chiloensis is a stoloniferous perennial herb that grows on coastal sand dunes where scattered shrubs create small patches of lower photon flux density (PFD) but higher soil nitrogen availability. The potential effects of resource transport between ramets when PFD and soil nitrogen are negatively associated in space were tested by comparing the growth of pairs of ramets in which the vascular connection between ramets was either severed or left intact. One ramet in each pair was given high PFD but a low level of soil nitrogen and the other ramet was given low PFD but high N. The analogous effects of resource transport likely to be realized in nature were tested by substituting a more realistic medium soil nitrogen level in place of the high level. Results suggested that connected ramets exchanged carbon and nitrogen under both regimes of soil nitrogen heterogeneity. In the low versus high nitrogen regime, connected ramets had higher combined dry biomass and different patterns of dry mass partitioning from those of severed ramets; effect of connection was greater on ramets given low PFD and high N and on younger ramets. In the low versus medium nitrogen regime, connected ramets had different patterns of partitioning only. Apparent reciprocal resource transport between ramets can enhance the growth of ramets with complementary resource deficiencies, but may affect growth in dry mass only when maximum resource levels are high.     

Behavior of the tachinid parasitoid <Emphasis Type="Italic">Exorista japonica</Emphasis> (Diptera: Tachinidae) on herbivore-infested plants

Odors from corn plants infested with the larvae of the noctuid herbivore Mythimna separata (Walker) attract tachinid fly, Exorista japonica Townsend, females; and odors from corn plants artificially damaged also attract this fly. We investigated the responses of flies to herbivore-infested, artificially damaged, and undamaged plants before and after arrival at the target plants to measure timing of the behavioral sequence. The behavior of the flies for 10 min after takeoff from a release point was observed in a wind-tunnel bioassay. The percentage of flies attracted to the plants was higher in infested and artificially damaged plants than in undamaged plants. Latency before takeoff was longer in undamaged plants, and time from takeoff to arrival at the plant was also longer in undamaged plants. Moreover, flies stayed longer on infested and artificially damaged plants. Flies walked longer on infested plants than on artificially damaged and undamaged plants. In this paper, we summarize the behavioral data and discuss the host-searching behavior of E. japonica females.     

Population-biomass dynamics and the absence of - 3/2 self-thinning in the clonal weed Salvinia molesta

Abstract In the field, the population density (n) of crowded, living ramets of Salvinia molesta ranged from 2500 m ^?2 in nutrient-poor water to more than 30 000 m^?2 in nutrient-rich water. Biomass of living shoots (B) in some localities exceeded 600 gm^?2 dry weight (150 tonnes ha^?1 fresh weight) and shoots plus roots of living and floating dead material exceeded 1600 gm^?2 dry weight (400 tonnes ha^?1 fresh weight). The ultimate limit B= 10⁵n^0.5 suggested by previous authors was not exceeded. The highest n and smallest ramets occurred in nutrient-rich water and B was a linear function of n. Field experiments confirmed no effect of n, but a strong effect of nutrient availability, on ramet weight. In a glasshouse experiment, ramet populations did not ‘self-thin’ along the log log B-n trajectory of slope -0.5, which has been suggested for aclonal plants, but followed trajectories having slopes closer to +1.0 before halting at the ambient B-n limit. Nutrient concentrations in the plants increased during the experiment, causing ramet size to decrease and slopes of log log B-n trajectories to depart from +1.0 by amounts which reflected the degree to which nutrient concentration had changed. Under constant conditions, mean ramet size is expected to remain constant and log log B-n trajectories to travel in a straight line of slope +1.0 to the ambient B-n limit. This behaviour of salvinia, whose ramets consist of a single structural module, is contrasted with that expected of clonal plants whose ramets are made up of multiple structural modules. A logistic model explained the increases in n and biomass of living and dead ramets when ramets were assumed to have constant longevity, constant time to decay, and when both the B-n limit and size of ramets were dependent on nitrogen content of the plant. There was no indication that physiological integration within phenets halted production of new ramets when carrying capacity was reached and new ramets continued to be produced on top of older ramets. Rates of ramet mortality were equal to, and dependent on, rates of ramet natality.     

Response of Salvinia molesta to insect damage: changes in nitrogen,phosphorus and potassium content

Summary When adults and larvae of the weevil Cyrtobagous salviniae destroyed buds and tunnelled through rhizomes of Salvinia molesta, the plant responded by producting new growth which contained higher concentrations of nitrogen than in undamaged plants or in the older parent tissue of the same plant. Damage to leaves by the moth, Samea multiplicalis did not induce the same response. C. salviniae fed on the new growth and the higher nitrogen intake would have increased its reproductive capacity and enhanced its action as a biological control agent.Damage by both insects resulted in potassium leaching from the plant but no change in concentrations of phosphorus. The results support earlier suggestions that damage by C. salviniae might improve the qualtity of the host plant for this herbivore.     

Samea multiplicalis [Lep.: Pyralidae], for biological control of two water weeds,Salvinia molesta andPistia stratiotes in Australia

The biology and host specificity ofSamea multiplicalis (Guenée) were studied in quarantine in Australia. Immature stages completed development onSalvinia molesta Mitchell,Pistia stratiotes L. andAzolla pinnata R.Br. In starvation tests, although larvae which had first fed onS. molesta produced minor leaf scarring on some other plants, they were unable to complete development. Damage toS. molesta andP. stratiotes indicated thatS. multiplicalis may be a valuable biological control agent for these weeds in Australia.S. multiplicalis was first liberated in northern Queensland in 1981 where it has become established onS. molesta.     

Variation in damage to cotton affecting larval feeding preference of Spodoptera littoralis

Feeding experiments with larvae of Spodoptera littoralis were performed with leaves from cotton plants subjected to damage and from undamaged plants. In the experiments, four different time intervals (1, 3, 7, and 14 days) after damage induction and two different levels (high and low) of herbivore damage were tested. Seven days after damage induction larvae fed less on the young top leaves from damaged plants for both levels of damage. At the high damage level, the larvae fed less on leaves from the damaged plants after just three days, and this effect still remained 14 days after damage infliction. When mature leaves from the middle of the plant were compared, no difference between treatments was observed.Two plant sizes were tested, small plants with 4–5 true leaves and large plants with 8–10 true leaves. In small plants the induced changes affecting larval feeding were found mainly in the youngest leaf at the top of the plant, while in large plants the induced effects were found in both the youngest and the second youngest leaves.In plants subjected to artificial damage, larvae fed less on top leaves of the damaged plants when compared to leaves from undamaged plants. When leaves from plants that had been artificially damaged were directly compared with leaves from plants damaged by herbivores, larvae fed more on the youngest leaves from artificially damaged plants when the plants were large. In small plants no significant difference was found when comparing artificial and herbivore damage.     

Temporal dynamics of herbivore‐induced responses in Brassica juncea and their effect on generalist and specialist herbivores

Herbivore feeding may induce an array of responses in plants, and each response may have its own temporal dynamics. Precise timing of these plant responses is vital for them to have optimal effect on the herbivores feeding on the plant. This study measured the temporal dynamics of various systemically induced responses occurring in Brassica juncea (L.) Czern. (Brassicaceae) leaves after insect herbivory in India and The Netherlands. Morphological (trichomes, leaf size) and chemical (glucosinolates, amino acids, sugars) responses were analysed. The effects of systemic responses were assessed using a specialist [Plutella xylostella L. (Lepidoptera: Plutellidae)] and a generalist [Spodoptera litura Fabricius (Lepidoptera: Noctuidae)] herbivore. We tested the hypotheses that morphological responses were slower than chemical responses and that generalist herbivores would be more affected by induced responses than specialists. Glucosinolates and trichomes were found to increase systemically as quickly as 4 and 7 days after herbivore damage, respectively. Amino acids, sugars, and leaf size remained unaffected during this period. The generalist S. litura showed a significant feeding preference for undamaged leaves, whereas the specialist herbivore P. xylostella preferred leaves that were damaged 9 days before. Performance bioassays on generalist S. litura revealed that larvae gained half the weight on leaves from damaged plants as compared to larvae feeding on leaves from undamaged plants. These studies show that although morphological responses are somewhat slower than chemical responses, they also contribute to induced plant resistance in a relatively short time span. We argue that before considering induced responses as resistance factors, their effect should be assessed at various points in time with both generalist and specialist herbivores.     

Population-level compensation after loss of vegetative buds: interactions among damaged and undamaged cotton neighbours

Population-level compensation occurs when herbivore attack on one individual allows another individual to grow more rapidly. This form of compensation was investigated in high and low density cotton crops subjected to three treatments: (i) undisturbed controls, (ii) uniformly damaged, in which all plants were damaged, and (iii) non-uniformly damaged, in which every second plant was damaged. Damaged plants had their vegetative buds manually removed to simulate damage by Helicoverpa spp. (Lepidoptera). Removal of vegetative buds did not reduce seed cotton production per unit ground area. In uniformly damaged crops, compensation was essentially the result of profuse branching after release of apical dominance and activation of axilary buds. In non-uniformly damaged crops, population level mechanisms acted that involved strong plant-plant interactions. At both plant densities, undamaged plants grown alongside damaged neighbours accumulated more root and shoot biomass and produced more seed cotton than undamaged plants in uniform crops. Different degrees of symmetry in the relationship between damaged and undamaged neighbours lead to different degrees of compensation, viz. seed cotton production of non-uniformly damaged crops ranged from 98 to 125% of that in controls. At high plant density, neighbour status also affected flowerbud initiation and/or retention. Changes in competitive relationships as well as early detection of and response to neighbour status were likely involved in these responses.