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Complementarity effects through dietary mixing enhance the performance of a generalist insect herbivore.

ABSTRACT: The ontogenetic niche concept predicts that resource use depends on an organism's developmental stage. This concept has been investigated primarily in animals that show differing resource use strategies as juveniles and as adults, such as amphibians. We studied resource use and performance in the grasshopper Chorthippus parallelus (Orthoptera, Acrididae) provided with food plant mixtures of either one, three or eight plant species throughout their development. C. parallelus survival and fecundity was highest in the food plant mixture with eight plant species and lowest in the treatments where only one single plant species was offered as food. C. parallelus' consumption throughout its ontogeny depended on sex, and feeding on different plant species was dependent on a grasshopper's developmental stage. To depict grasshopper foraging in food plant mixtures compared to foraging on single plant species, we introduce the term "relative forage total" (RFT) based on an approach used in biodiversity research by Loreau and Hector (Nature 413:548-274, 2001). RFT of grasshoppers in food plant mixtures was always higher than what would have been expected from foraging in monocultures. The increase in food consumption was due to an overall increase in feeding on plant species in mixtures compared to consumption of the same species offered as a single diet. Thus we argue that grasshopper foraging exhibits complementarity effects. Our results reinforce the necessity to consider development-related changes in insect herbivore feeding. Thorough information on the feeding ontogeny of insect herbivores could not only elucidate their nutritional ecology but also help to shed light on their functional role in plant communities.

SUBMITTER: Unsicker SB

PROVIDER: S-EPMC2757592 | biostudies-literature | 2008 May

REPOSITORIES: biostudies-literature

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Complementarity effects through dietary mixing enhance the performance of a generalist insect herbivore.

Unsicker Sybille B SB Oswald Anett A Köhler Günter G Weisser Wolfgang W WW

Oecologia 20080501 2

The ontogenetic niche concept predicts that resource use depends on an organism's developmental stage. This concept has been investigated primarily in animals that show differing resource use strategies as juveniles and as adults, such as amphibians. We studied resource use and performance in the grasshopper Chorthippus parallelus (Orthoptera, Acrididae) provided with food plant mixtures of either one, three or eight plant species throughout their development. C. parallelus survival and fecundit ...[more]

PMID: 18301924

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Project description:When facing a food shortage, generalist herbivores can respond by expanding their dietary species richness (DSR) to maximize energy collection, regardless of whether forages are preferred or not. Higher DSR usually indicates higher nutrient adequacy and better health. However, the high-DSR diet containing a large proportion of preferred species or a large proportion of less-preferred species means different things to an animal. It is still unknown how different shift patterns in DSR would affect distinctly the performance of animals via altering gut microbiota. We examined the gut microbial composition, diversity, community assembly processes, and performance of a generalist herbivore, Lasiopodomys brandtii, in a feeding experiment with increased levels of simulated DSR shifting from preferred plant species to less preferred ones. We found the survival rate and body growth of Brandt's voles showed a dome-shaped association with DSR: species performance increased initially with the increase of preferred plant species but declined with the increase of less-preferred food items. Several microbial taxa and functions closely related to the metabolism of amino acids and short-chain fatty acids also showed a dome-shaped association with DSR, which is consistent with the observation of performance change. However, the alpha diversities of gut microbiota increased linearly with DSR. The null model and phylogenetic analysis suggested that stochastic processes dominate at low DSR diets, whereas deterministic processes prevail at high DSR diets. These results suggest that the role of DSR in regulating animal performance by gut microbiota depends on the number of preferred forage items. IMPORTANCE The plant species diversity varies greatly under the influence of both climate change and human disturbance, which may negatively affect the productivity as well as the variability of organisms (e.g., small herbivores) at the next trophic level. It is still unknown how gut microbiota of small herbivores respond to such changes in dietary species richness. Our manipulative food experiment revealed that dietary species richness can affect the composition, functions, and community assembly of gut microbiota of Brandt's vole in a nonlinear way. Given the fast-growing interest in therapeutic diets to treat dysbiosis and to improve health conditions, our study highlights the need to consider not just the variety of consumed food but also the principles of rational nutrition.

Project description:Herbivores must overcome a variety of plant defenses, including coping with plant secondary compounds (PSCs). To help detoxify these defensive chemicals, several insect herbivores are known to harbor gut microbiota with the metabolic capacity to degrade PSCs. Leaf-cutter ants are generalist herbivores, obtaining sustenance from specialized fungus gardens that act as external digestive systems and which degrade the diverse collection of plants foraged by the ants. There is in vitro evidence that certain PSCs harm Leucoagaricus gongylophorus, the fungal cultivar of leaf-cutter ants, suggesting a role for the Proteobacteria-dominant bacterial community present within fungus gardens. In this study, we investigated the ability of symbiotic bacteria present within fungus gardens of leaf-cutter ants to degrade PSCs. We cultured fungus garden bacteria, sequenced the genomes of 42 isolates, and identified genes involved in PSC degradation, including genes encoding cytochrome P450 enzymes and genes in geraniol, cumate, cinnamate, and α-pinene/limonene degradation pathways. Using metatranscriptomic analysis, we showed that some of these degradation genes are expressed in situ Most of the bacterial isolates grew unhindered in the presence of PSCs and, using gas chromatography-mass spectrometry (GC-MS), we determined that isolates from the genera Bacillus, Burkholderia, Enterobacter, Klebsiella, and Pseudomonas degrade α-pinene, β-caryophyllene, or linalool. Using a headspace sampler, we show that subcolonies of fungus gardens reduced α-pinene and linalool over a 36-h period, while L. gongylophorus strains alone reduced only linalool. Overall, our results reveal that the bacterial communities in fungus gardens play a pivotal role in alleviating the effect of PSCs on the leaf-cutter ant system.IMPORTANCE Leaf-cutter ants are dominant neotropical herbivores capable of deriving energy from a wide range of plant substrates. The success of leaf-cutter ants is largely due to their external gut, composed of key microbial symbionts, specifically, the fungal mutualist L. gongylophorus and a consistent bacterial community. Both symbionts are known to have critical roles in extracting energy from plant material, yet comparatively little is known about their roles in the detoxification of plant secondary compounds. In this study, we assessed if the bacterial communities associated with leaf-cutter ant fungus gardens can degrade harmful plant chemicals. We identify plant secondary compound detoxification in leaf-cutter ant gardens as a process that depends on the degradative potential of both the bacterial community and L. gongylophorus Our findings suggest that the fungus garden and its associated microbial community influence the generalist foraging abilities of the ants, underscoring the importance of microbial symbionts in plant substrate suitability for herbivores.

Project description:BACKGROUND: Hormesis is a biphasic biological response characterized by the stimulatory effect at relatively low amounts of chemical compounds which are otherwise detrimental at higher concentrations. A hormetic response in larval growth rates has been observed in cotton-feeding insects in response to increasing concentrations of gossypol, a toxic metabolite found in the pigment glands of some plants in the family Malvaceae. We investigated the developmental effect of gossypol in the cotton bollworm, Helicoverpa armigera, an important heliothine pest species, by exposing larvae to different doses of this metabolite in their diet. In addition, we sought to determine the underlying transcriptional responses to different gossypol doses. RESULTS: Larval weight gain, pupal weight and larval development time were measured in feeding experiments and a hormetic response was seen for the first two characters. On the basis of net larval weight gain responses to gossypol, three concentrations (0%, 0.016% and 0.16%) were selected for transcript profiling in the gut and the rest of the body in a two-color double reference design microarray experiment. Hormesis could be observed at the transcript level, since at the low gossypol dose, genes involved in energy acquisition such as ?-fructofuranosidases were up-regulated in the gut, and genes involved in cell adhesion were down-regulated in the body. Genes with products predicted to be integral to the membrane or associated with the proteasome core complex were significantly affected by the detrimental dose treatment in the body. Oxidoreductase activity-related genes were observed to be significantly altered in both tissues at the highest gossypol dose. CONCLUSIONS: This study represents the first transcriptional profiling approach investigating the effects of different concentrations of gossypol in a lepidopteran species. H. armigera's transcriptional response to gossypol feeding is tissue- and dose-dependent and involves diverse detoxifying mechanisms not only to alleviate direct effects of gossypol but also indirect damage such as pH disturbance and oxygen radical formation. Genes discovered through this transcriptional approach may be additional candidates for understanding gossypol detoxification and coping with gossypol-induced stress. In a generalist herbivore that has evolved transcriptionally-regulated responses to a variety of different plant compounds, hormesis may be due to a lower induction threshold of growth-promoting, stress-coping responses and a higher induction threshold of detoxification pathways that are costly and cause collateral damage to the cell.

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Complementarity effects through dietary mixing enhance the performance of a generalist insect herbivore.

Publications

Complementarity effects through dietary mixing enhance the performance of a generalist insect herbivore.

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