Synergies and trade-offs between insect and pathogen resistance in maize leaves and roots

Determining links between plant defence strategies is important to understand plant evolution and to optimize crop breeding strategies. Although several examples of synergies and trade-offs between defence traits are known for plants that are under attack by multiple organisms, few studies have attempted to measure correlations of defensive strategies using specific single attackers. Such links are hard to detect in natural populations because they are inherently confounded by the evolutionary history of different ecotypes. We therefore used a range of 20 maize inbred lines with considerable differences in resistance traits to determine if correlations exist between leaf and root resistance against pathogens and insects. Aboveground resistance against insects was positively correlated with the plant's capacity to produce volatiles in response to insect attack. Resistance to herbivores and resistance to a pathogen, on the other hand, were negatively correlated. Our results also give first insights into the intraspecific variability of root volatiles release in maize and its positive correlation with leaf volatile production. We show that the breeding history of the different genotypes (dent versus flint) has influenced several defensive parameters. Taken together, our study demonstrates the importance of genetically determined synergies and trade-offs for plant resistance against insects and pathogens.     

Correlations between leaf structural traits and the densities of herbivorous insect guilds

The functional composition of herbivorous insect assemblages was correlated with aspects of new and mature leaf surface features, anatomy and morphology across 18 co‐occurring plant species. Multivariate analyses of insects and leaf traits revealed that the functional composition of the herbivore assemblage was more strongly correlated with leaf structural traits than with leaf constituents. Leaf traits were more strongly correlated with the functional composition of the herbivore assemblage than with its taxonomic composition. Densities of sessile phloem feeders, ­rostrum chewers, and all herbivores were significantly negatively correlated with specific leaf weight, lamina and cuticle thickness, vascular tissue depth and stomate length, and were significantly positively correlated with stomate density. External chewer densities were significantly negatively correlated with percent lignified vein area, and significantly positively correlated with leaf surface area and the distance between lignified tissues. Spine‐like leaves were associated with significantly lower densities of sessile phloem feeders, external chewers and all herbivores compared to kite leaves (kite leaves are comprised of unfortified leaf tissue supported by a framework of vascular tissue). The presence of a thickened leaf hypodermis was associated with significantly lower densities of external chewers and rostrum chewers, while midrib protection was associated with significantly lower densities of external chewers. Leaf structural traits may not be the proximal factors influencing herbivorous insects, as leaf structural traits are correlated with many other plant traits such as photosynthetic rate, relative growth rate and leaf life‐span. Nonetheless, these results indicate that certain leaf structural traits may potentially be used to predict the functional structure of herbivorous insect assemblages. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 77 , 43–65.     

An endophyte‐rich diet increases ant predation on a specialist herbivorous insect

1. All plants form symbioses with microfungi, known as endophytes, which live within plant tissues. Numerous studies have documented endophyte–herbivore antagonism in grass systems, but plant–endophyte–insect interactions are highly variable for forbs and woody plants. 2. The net effect of endophytes on insect herbivory may be modified by their interactions with higher trophic levels, such as predators. Including these multitrophic dynamics may explain some of the variability among endophyte studies of non‐grass plants, which are currently based exclusively on bitrophic studies. 3. The abundance of natural foliar endophytes in a Neotropical vine was manipulated and beetles were fed high or low endophyte diets. Experimental assays assessed whether dietary endophyte load affected beetle growth, leaf consumption, and susceptibility to ant predation. 4. Beetles feeding on high‐ versus low‐endophyte plants had almost identical growth and leaf consumption rates. 5. In a field bioassay, however, it was discovered that feeding on an endophyte‐rich diet increased a beetle's odds of capture by predatory ants nine‐fold. 6. Endophytes could thus provide an indirect, enemy‐mediated form of plant defence that operates even against specialist herbivores. We argue that a multitrophic approach is necessary to untangle the potentially diverse types of endophyte defence among plants.     

Asymmetric effects of a leaf‐chewing herbivore on aphid population growth

1. Plant responses to herbivory are often specific to the feeding guild of the attacking herbivore. These phytochemical responses to herbivore damage can affect herbivore performance and activity. Comprehensive studies on the ecological consequences of multi‐herbivore plant interactions are key to understanding plant–herbivore community dynamics. 2. This study examined how feeding damage by co‐occurring herbivores from separate feeding guilds, Myzus persicae (Sulzer), a sucking herbivore, and Leptinotarsa decemlineata (Say), a chewing herbivore, alter plant chemistry and indirectly affect herbivore performance. Performance was measured when each insect fed on plants individually, sequentially, or simultaneously in laboratory and field experiments. Phytohormone and glycoalkaloid content were measured for each feeding sequence to evaluate plant responses to herbivory by each guild. Mid‐season and end‐of‐season tuber yield were evaluated in the field study. 3. Damage by L. decemlineata negatively impacted M. persicae performance in both laboratory and field settings. Damage by M. persicae did not affect L. decemlineata performance in laboratory assays. However, L. decemlineata performance was positively affected by M. persicae herbivory in the field, but this effect was temporary. Although phytohormones and plant defences varied across treatments, they provide little resolution on interaction outcomes. 4. These results confirm that the presence of multiple feeding guilds on a single plant can affect these chewing and sucking herbivores differentially, but given the variability in our phytochemical analyses compared with other studies, the mechanism remains unclear. The study's findings show that aphids are negatively affected by chewing herbivores across systems, while aphids temporarily affected beetles positively.     

Mutual interplay between phytopathogenic powdery mildew fungi and other microorganisms

Powdery mildew is a common and widespread plant disease of considerable agronomic relevance. It is caused by obligate biotrophic fungal pathogens which, in most cases, epiphytically colonize aboveground plant tissues. The disease has been typically studied as a binary interaction of the fungal pathogen with its plant hosts, neglecting, for the most part, the mutual interplay with the wealth of other microorganisms residing in the phyllo- and/or rhizosphere and roots. However, the establishment of powdery mildew disease can be impacted by the presence/absence of host-associated microbiota (epi- and endophytes) and, conversely, plant colonization by powdery mildew fungi might disturb indigenous microbial community structures. In addition, other (foliar) phytopathogens could interact with powdery mildews, and mycoparasites may affect the outcome of plant–powdery mildew interactions. In this review, we discuss the current knowledge regarding the intricate and multifaceted interplay of powdery mildew fungi, host plants and other microorganisms, and outline current gaps in our knowledge, thereby setting the basis for potential future research directions.     

Interguild interactions between a non-native phloem feeder and a native outbreaking defoliator

1. Competitive and synergistic interactions directly or indirectly drive community dynamics of herbivorous insects. Novel interactions between non-native and native insects are unpredictable and not fully understood. 2. We used manipulative experiments on mature red spruce trees to test interactions between a non-native phloem feeding insect, the brown spruce longhorn beetle (BSLB), and an outbreaking native defoliator, the spruce budworm. We subjected treatment trees to defoliation by three densities of spruce budworm larvae. Treatment trees were: stressed by (i) girdling (to mimic beetle feeding) or (ii) girdling + BSLB before spruce budworm larvae were introduced on branches in sleeve cages. Budworm larvae then fed on foliage and developed to pupation. We assessed all branches for budworm performance, defoliation, shoot production and shoot growth. 3. Shoot length did not differ in response to stress from girdling or BSLB infestation. Neither stress from girdling, nor interactions with BSLB feeding affected spruce budworm performance or defoliation. Intraspecific impacts on performance and defoliation in relation to budworm density were stronger than the effects of tree stress. 4. Prior infestation of red spruce by BSLB in our experimental set-up did not influence spruce budworm performance. BSLB is a successful invader that has blended into its novel ecological niche because of ecological and phylogenetic similarities with a native congener, Tetropium cinnamopterum. 5. Outbreaks by BSLB will not likely impede or facilitate spruce budworm outbreaks if they co-occur. It would be useful to evaluate the reverse scenario of BSLB success after defoliation stress by spruce budworm.     

Field evidence for indirect interactions between foliar‐feeding insect and root‐feeding nematode communities on Nicotiana tabacum

Abstract 1. As herbivory often elicits systemic changes in plant traits, indirect interactions via induced plant responses may be a pervasive feature structuring herbivore communities. Although the importance of this phenomenon has been emphasised for herbivorous insects, it is unknown if and how induced responses contribute to the organisation of other major phytoparasitic taxa. 2. Survey and experimental field studies were used to investigate the role of plants in linking the dynamics of foliar‐feeding insects and root‐feeding nematodes on tobacco, Nicotiana tabacum. 3. Plant‐mediated interactions between insects and nematodes could largely be differentiated by insect feeding guild, with positive insect–nematode interactions predominating with leaf‐chewing insects (caterpillars) and negative interactions occurring with sap‐feeding insects (aphids). For example, insect defoliation was positively correlated with the abundance of root‐feeding nematodes, but aphids and nematodes were negatively correlated. Experimental field manipulations of foliar insect and nematode root herbivory also tended to support this outcome. 4. Overall, these results suggest that plants indirectly link the dynamics of divergent consumer taxa in spatially distinct ecosystems. This lends support to the growing perception that plants play a critical role in propagating indirect effects among a diverse assemblage of consumers.     

Finish line plant–insect interactions mediated by insect feeding mode and plant interference: a case study of Brassica interactions with diamondback moth and turnip aphid

There are gaps in our understanding of plant responses under different insect phytophagy modes and their subsequent effects on the insect herbivores’ performance at late season. Here we compared different types of insect feeding by an aphid, Lipaphis erysimi, and a lepidopteran, Plutella xylostella, and how this affected defensive metabolites in leaves of 2 Brassica species when plants gain maturity. Thiocyanate concentrations after P. xylostella and L. erysimi feeding activities were the same. Total phenolics was higher after the phloem feeder feeding than the folivore activity. The plants compensatory responses (i.e., tolerance) to L. erysimi feeding was significantly higher than the responses to P. xylostella. This study showed that L. erysimi had higher carbon than P. xylostella whereas nitrogen in P. xylostella was 1.42 times that in L. erysimi. Population size of the phloem feeder was not affected by plant species or insect coexistence. However, there was no correlation between plant defensive metabolites and both insects’ population size and biomass. This suggests that plant root biomass and tolerance index after different insect herbivory modes are not necessarily unidirectional. Importantly, the interaction between the folivore and the phloem feeder insects is asymmetric and the phloem feeder might be a trickier problem for plants than the folivore. Moreover, as both plants’ common and special defenses decreased under interspecific interference, we suggest that specialist insect herbivores can be more challenged in ecosystems in which plants are not involved in interspecific interference.     

Impact of plant nutrients on the relationship between a herbivorous insect and its symbiotic bacteria

The interactions between herbivorous insects and their symbiotic micro-organisms can be influenced by the plant species on which the insects are reared, but the underlying mechanisms are not understood. Here, we identify plant nutrients, specifically amino acids, as a candidate factor affecting the impact of symbiotic bacteria on the performance of the phloem-feeding aphid Aphis fabae. Aphis fabae grew more slowly on the labiate plant Lamium purpureum than on an alternative host plant Vicia faba, and the negative effect of L. purpureum on aphid growth was consistently exacerbated by the bacterial secondary symbionts Regiella insecticola and Hamiltonella defensa, which attained high densities in L. purpureum-reared aphids. The amino acid content of the phloem sap of L. purpureum was very low; and A. fabae on chemically defined diets of low amino acid content also grew slowly and had elevated secondary symbiont densities. It is suggested that the phloem nutrient profile of L. purpureum promotes deleterious traits in the secondary symbionts and disturbs insect controls over bacterial abundance.     

Bryophytes as food: comparative consumption and utilization of mosses by a generalist insect herbivore

Compared with angiosperms, bryophytes are seldom fed upon by insects, despite being commonly used for shelter. Bryophytes are assumed to be unpalatable, and three classes of mechanisms have been suggested as possible barriers to bryophagy: chemical defenses, low digestibility, and low nutrient content. However, very few studies have tested these hypotheses. The present study examines pre‐ and post‐ingestive defenses of mosses. The acceptability and quality of four species of moss –Bryum argenteum Hedw. (Bryales: Bryaceae), Climacium americanum Brid. (Leucodontales: Climaciaceae), Leucobryum glaucum (Hedw.) (Dicranales: Leucobryaceae), and Sphagnum warnstorfii Russ. (Sphagnales: Sphagnaceae) – were compared with two control diets using the generalist caterpillar, Trichoplusia ni Hübner (Lepidoptera: Noctuidae: Plusiinae). In no‐choice trials, caterpillars consumed much less of any of the mosses than lettuce or wheat germ. The only moss consumed in sufficient quantities to evaluate post‐ingestive responses was C. americanum. Digestibility, assimilation, and overall utilization efficiency of C. americanum did not differ from that of lettuce, although C. americanum and lettuce were both less digestible than artificial diet. Choice assays using leaf discs showed that ethanol extract of L. glaucum, the least consumed moss, was deterrent, implying that chemical defenses play a major role in deterring feeding on L. glaucum. This study suggested that pre‐ingestive mechanisms are more important than post‐ingestive mechanisms in discouraging herbivory on mosses, and offered evidence that mosses are not simply nutrient poor.     

Interspecific variation and elevated CO2 influence the relationship between plant chemical resistance and regrowth tolerance

To understand how comprehensive plant defense phenotypes will respond to global change, we investigated the legacy effects of elevated CO₂ on the relationships between chemical resistance (constitutive and induced via mechanical damage) and regrowth tolerance in four milkweed species (Asclepias). We quantified potential resistance and tolerance trade‐offs at the physiological level following simulated mowing, which are relevant to milkweed ecology and conservation. We examined the legacy effects of elevated CO₂ on four hypothesized trade‐offs between the following: (a) plant growth rate and constitutive chemical resistance (foliar cardenolide concentrations), (b) plant growth rate and mechanically induced chemical resistance, (c) constitutive resistance and regrowth tolerance, and (d) regrowth tolerance and mechanically induced resistance. We observed support for one trade‐off between plant regrowth tolerance and mechanically induced resistance traits that was, surprisingly, independent of CO₂ exposure. Across milkweed species, mechanically induced resistance increased by 28% in those plants previously exposed to elevated CO_2. In contrast, constitutive resistance and the diversity of mechanically induced chemical resistance traits declined in response to elevated CO₂ in two out of four milkweed species. Finally, previous exposure to elevated CO₂ uncoupled the positive relationship between plant growth rate and regrowth tolerance following damage. Our data highlight the complex and dynamic nature of plant defense phenotypes under environmental change and question the generality of physiologically based defense trade‐offs.     

Interactive direct and plant‐mediated effects of elevated atmospheric [CO2] and temperature on a eucalypt‐feeding insect herbivore

Understanding the direct and indirect effects of elevated [CO₂] and temperature on insect herbivores and how these factors interact are essential to predict ecosystem‐level responses to climate change scenarios. In three concurrent glasshouse experiments, we measured both the individual and interactive effects of elevated [CO₂] and temperature on foliar quality. We also assessed the interactions between their direct and plant‐mediated effects on the development of an insect herbivore of eucalypts. Eucalyptus tereticornis saplings were grown at ambient or elevated [CO₂] (400 and 650 μmol mol^?1 respectively) and ambient or elevated ( + 4 °C) temperature for 10 months. Doratifera quadriguttata (Lepidoptera: Limacodidae) larvae were feeding directly on these trees, on their excised leaves in a separate glasshouse, or on excised field‐grown leaves within the temperature and [CO₂] controlled glasshouse. To allow insect gender to be determined and to ensure that any sex‐specific developmental differences could be distinguished from treatment effects, insect development time and consumption were measured from egg hatch to pupation. No direct [CO₂] effects on insects were observed. Elevated temperature accelerated larval development, but did not affect leaf consumption. Elevated [CO₂] and temperature independently reduced foliar quality, slowing larval development and increasing consumption. Simultaneously increasing both [CO₂] and temperature reduced these shifts in foliar quality, and negative effects on larval performance were subsequently ameliorated. Negative nutritional effects of elevated [CO₂] and temperature were also independently outweighed by the direct positive effect of elevated temperature on larvae. Rising [CO₂] and temperature are thus predicted to have interactive effects on foliar quality that affect eucalypt‐feeding insects. However, the ecological consequences of these interactions will depend on the magnitude of concurrent temperature rise and its direct effects on insect physiology and feeding behaviour.     

The relationship between cabbage root fly (Delia radicum) larval feeding and the freeze-dried matter and sugar content of Brassica roots

Five genotypes of swede (Brassica napus var. napobrassica), two genotypes of kale (B. oleracea var. acephala), and two genotypes of rape (B. napus var. napus) were each inoculated at the 8–10 true leaf stage with five cabbage root fly (Delia radicum) eggs. The percentage pupation after larval feeding on individual plant genotypes ranged from 45 to 78%, and the mean pupal weight from 6.5 to 13.0 mg. After 5 weeks, larval feeding damage had reduced root weight by up to 47%, compared with uninoculated plants. The dry matter content of undamaged roots was higher in the kales and rapes than in the swedes. Whilst the dry matter content of the rapes and swedes were not changed by D. radicum damage, that of the kales was elevated. The ethanol-soluble sugar content of the root was reduced in all cases by D. radicum larval damage. However, the effect of D. radicum damage on the concentrations of individual sugars (glucose, fructose and sucrose) was crop- and genotype-dependent. In the roots of kales and rapes, the glucose and fructose concentrations were either very low or unaffected by D. radicum damage, whilst both glucose and fructose were generally reduced in swede roots by D. radicum damage. The root sucrose concentration was either reduced or not significantly affected by D. radicum damage in all of the crop types tested. The percentage pupation and the mean pupal weight of D. radicum were inversely correlated to root freeze-dried matter content. D. radicum pupal weight was positively correlated with root fructose, glucose and ethanol-soluble sugar contents.     

Plant compensation, natural biological control, and herbivory by Aphis gossypii on pre-reproductive cotton: the anatomy of a non-pest

Crop plant compensation for herbivory and the population dynamics of herbivores are two key elements in defining an herbivore's pest status. We studied the dynamics of natural, unmanipulated populations of the aphid Aphis gossypii on seedling plantings of cotton, Gossypium hirsutum and Gossypium barbadense, over a 4-year period in California's Central Valley. Aphid populations colonized all plantings, but reached densities in excess of 0.5 aphids/leaf during only one year (1991), when outbreaks occurred. Outbreak populations were, however, ephemeral; predation and parasitism suppressed aphid populations prior to the initiation of flower bud production, when cotton plant growth may become photosynthate-limited. Effective natural biological control was observed despite the action of hyperparasitoids and the heavy mortality of immature parasitoids that occurred when predators consumed parasitized aphids.We conducted manipulative experiments during 1991 and 1992 to quantify the ability of pre-reproductive G. hirsutum to compensate for aphid herbivory. In 1991 aphid populations in the high-damage treatment reached densities as high as any observed naturally during the past 37 years. Damage symptoms were severe: leaf area was reduced by up to 58% and total above-ground plant biomass was reduced by 45%. By the time of crop harvest, however, plants had compensated fully for the early damage in each of the three traits that define cotton's economic value: the timing of crop maturation, the yield of cotton fiber, and the quality of cotton fiber. Aphid feeding damage did, however, produce some changes in plant architecture that persisted throughout the growing season, including a decrease in the number of vegetative branches. In 1992 aphid populations and associated damage were much lighter, but the qualitative responses to herbivory were consistent with those observed in 1991. Plant compensation for early damage was complete for economically significant measures, and vegetative branch production was again suppressed in mature cotton plants. There was no evidence for a change in the suitability of G. hirsutum as a host plant for A. gossypii as a result of early damage (induced resistance).We conclude that pre-reproductive G. hirsutum, which has not yet begun strong allocations to reproductive structures or established architectural complexity, has retained effective means of compensating for herbivory. In contrast to other systems exhibiting strong compensation, G. hirsutum appears to compensate in part by enhancing apical dominance. The recognition of early-season A. gossypii as non-pests is critical to the sustainability of cotton production, because it will allow growers to forego pesticide applications that accelerate the evolution of pesticide-resistance and disrupt natural communities of predators and parasitoids.Deceased, formerly at the Shafter Research Station, 17053 Shafter Ave., Shafter, CA 93263, USA