Plant nutrient supply determines competition between phytophagous insects

Division of Biology, Department of Life Sciences, Imperial College London, Ascot, Berkshire, UK.
Proceedings of the Royal Society B: Biological Sciences (Impact Factor: 5.05). 03/2011; 278(1706):718-24. DOI: 10.1098/rspb.2010.1593
Source: PubMed


Indirect competition is often mediated by plant responses to herbivore feeding damage and is common among phytophagous insect species. Plant-mediated responses may be altered by abiotic conditions such as nutrient supply, which can affect plant growth, morphology, and the concentration of primary and secondary metabolites. Nutrient supply can be manipulated by the type and amount of fertilizer applied to a plant. Brassica oleracea plants were grown in several types of fertilizer, including those commonly used in sustainable and conventional agricultural systems. The occurrence of indirect competition between two phytophagous species from different feeding guilds (a phloem-feeder and leaf-chewer) was assessed. The leaf-chewer reduced aphid populations on plants growing in most fertilizer treatments, but not on those in the ammonium nitrate fertilizer treatment, which caused the highest concentration of foliar nitrogen. The potential consequences of our findings are discussed for phytophagous species in conventional and sustainable agricultural systems.


Available from: Simon Robert Leather
    • "Further downstream, a limited availability of mineral N can cause pronounced qualitative and quantitative changes in primary plant metabolites such as amino acids (Tschoep et al., 2009) and organic acids (Tschoep et al., 2009), but also in secondary plant metabolites such as flavonoids (Lillo et al., 2008) and terpenoids (Kleine and Müller, 2013). Nutrient-related changes of the plant metabolome can be critical to the outcome of multitrophic interactions between plants and other organisms (Kutyniok and Müller, 2013; Staley et al., 2011). Intra-and interspecific competition can also lead to the depletion of essential macronutrients such as N, phosphate and potassium in the soil, and at the same time, might reduce photosynthesis and carbon (C) assimilation rates of the target plants due to shading. "
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    ABSTRACT: Iridoid glycosides are plant defence compounds with potentially detrimental effects on non-adapted herbivores. Some plant species possess β-glucosidases that hydrolyse iridoid glycosides and thereby release protein-denaturing aglycones. To test the hypothesis that iridoid glycosides and plant β-glucosidases form a dual defence system, we used Plantago lanceolata and a polyphagous caterpillar species. To analyse the impact of leaf-age dependent differences in iridoid glycoside concentrations and β-glucosidase activities on insect performance, old or young leaves were freeze-dried and incorporated into artificial diets or were provided freshly to the larvae. We determined larval consumption rates and the amounts of assimilated nitrogen. Furthermore, we quantified β-glucosidase activities in artificial diets and fresh leaves and the amount of iridoid glycosides that larvae feeding on fresh leaves ingested and excreted. Compared to fresh leaves, caterpillars grew faster on artificial diets, on which larval weight gain correlated positively to the absorbed amount of nitrogen. When feeding fresh young leaves, larvae even lost weight and excreted only minute proportions of the ingested iridoid glycosides intact with the faeces, indicating that the hydrolysis of these compounds might have interfered with nitrogen assimilation and impaired larval growth. To disentangle physiological effects from deterrent effects of iridoid glycosides, we performed dual choice feeding assays. Young leaves, their methanolic extracts and pure catalpol reduced larval feeding in comparison to the respective controls, while aucubin had no effect on larval consumption. We conclude that the dual defence system of P. lanceolata consisting of iridoid glycosides and β-glucosidases interferes with the nutrient utilisation via the hydrolysis of iridoid glycosides and also mediates larval feeding behaviour in a concentration- and substance-specific manner. Copyright © 2015. Published by Elsevier Ltd.
    Journal of insect physiology 08/2015; 82. DOI:10.1016/j.jinsphys.2015.08.006 · 2.47 Impact Factor
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    • "As indigenous or endemic species respond spatially and temporally to populations of alien insects, they may be affected negatively or positively in complex ways (Gandhi and Herms, 2010). Furthermore, abiotic factors may influence the manner in which multiple phytophagous insects compete (Staley et al., 2011). If the presence of one insect species or an abiotic factor increases or decreases damage by a second insect species, this knowledge may improve management decisions. "
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    ABSTRACT: Four phytophagous insects are among the major threats to Cycas micronesica K.D. Hill on Guam, and the temporal comparisons of infestation levels may inform horticultural and conservation decisions. Incidence of Aulacaspis yasumatsui Takagi, Erechthias Meyrick sp., Chilades pandava Horsfield, and Dihammus marianarum Aurivillius infestations on Cycas micronesica plants were recorded every 6 months from 2004 to 2013 to determine if the incidence of A. yasumatsui was related to patterns of the other three insects. Dihammus marianarum infestations reached ephemeral maximum and minimum levels ≈2 years after A. yasumatsui infestations reached maximum and minimum levels. Erechthias sp. infestations disappeared in early 2006 when Cycas micronesica leaves were being killed by acute A. yasumatsui infestations. Erechthias sp. infestations increased thereafter as A. yasumatsui incidence declined in response to biological control. Chilades pandava infestations appeared to increase and decrease inversely with A. yasumatsui infestations throughout the years. Aulacaspis yasumatsui may be indirectly affecting D. marianarum damage by direct control of changes in overall tree health. Aulacaspis yasumatsui may be indirectly influencing Erechthias sp. through direct control over leaf longevity. The C. pandava and A. yasumatsui populations appear to exhibit direct competition with inverse patterns of incidence.
    HortScience: a publication of the American Society for Horticultural Science 09/2013; 48(10):1334-1338. · 0.90 Impact Factor
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    • "Abiotic factors such as nutrient supply or drought can also determine whether the interaction between two herbivores results in competition or facilitation (Gange & Brown 1989; Staley et al. 2011). Interestingly, this can even occur between herbivores that are located above-and below-ground (Gange & Brown 1989; Staley et al. 2007; Erb et al. 2011). "
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    ABSTRACT: 1. Plants have a complex immune system that defends them against attackers (e.g. herbivores and microbial pathogens) but that also regulates the interactions with mutualistic organisms (e.g. mycorrhizal fungi and plant growth-promoting rhizobacteria). Plants have to respond to multiple environmental challenges, so they need to integrate both signals associated with biotic and abiotic stresses in the most appropriate response to survive. 2. Beneficial microbes such as rhizobacteria and mycorrhizal fungi can help plants to 'deal' with pathogens and herbivorous insects as well as to tolerate abiotic stress. Therefore, beneficial microbes may play an important role in a changing environment, where abiotic and biotic stresses on plants are expected to increase. The effects of beneficial microbes on herbivores are highly context-dependent, but little is known on what is driving such dependency. Recent evidence shows that abiotic stresses such as changes in soil nutrients, drought and salt stress, as well as ozone can modify the outcome of plant—microbe—insect interactions. 3. Here, we review how abiotic stress can affect plant—microbe, plant—insect and plant—microbe—insect interactions, and the role of the network of plant signal-transduction pathways in regulating such interactions. 4. Most of the studies on the effects of abiotic stress on plant—microbe—insect interactions show that the effects of microbes on herbivores (positive or negative) are strengthened under stressful conditions. We propose that, at least in part, this is due to the crosstalk of the different plant signalling pathways triggered by each stress individually. By understanding the cross-regulation mechanisms we may be able to predict the possible outcomes of plant-microbe—insect interactions under particular abiotic stress conditions. We also propose that microbes can help plants to deal with insects mainly under conditions that compromise efficient activation of plant defences. 5. In the context of global change, it is crucial to understand how abiotic stresses will affect species interactions, especially those interactions that are beneficial for plants. The final aim of this review is to stimulate studies unravelling when these 'beneficial' microbes really benefit a plant.
    Functional Ecology 02/2013; 27:574–586. DOI:10.2307/23481020 · 4.83 Impact Factor
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