Recent advances in the integrative nutrition of arthropods.

In this review we highlight recent advances in four areas in which nutrition shapes the relationships between organisms: between plants and herbivores, between hosts and their microbiota, between individuals within groups and societies, and between species within food webs. We demonstrate that taking an explicitly multidimensional view of nutrition and employing the logic of the geometric framework for nutrition provide novel insights and offer a means of integration across different levels of organization, from individuals to ecosystems.

Insect herbivores can choose microclimates to achieve nutritional homeostasis.

The interaction between temperature and diet quality can affect the life history of ectotherms. The rate and ratio at which protein and carbohydrate are obtained from food are important aspects of diet quality, and insects have a well-developed capacity to adjust their feeding behaviour and post-ingestive physiology to regulate intake and allocation of these nutrients. If the supply of protein and carbohydrate varies with temperature (e.g. via effects on intake, digestion or metabolism), then herbivorous insects can use thermoregulatory behaviour to help achieve nutritional homeostasis. When fed the host grass Triticum aestivum, Locusta migratoria nymphs absorbed and allocated protein and carbohydrate to growth with the same efficiency at 38°C as at 32°C; however, at the higher temperature, they ingested more food. In contrast, when feeding on Themeda triandra, the nymphs absorbed carbohydrate with higher efficiency at 32°C, and protein at 38°C. Using synthetic diets, we induced either a protein or a carbohydrate deficiency in experimental insects and showed that locusts placed in a thermal gradient following a meal of T. triandra selected 32°C when deprived of carbohydrate, and 38°C when deprived of protein. This capacity to use thermoregulatory behaviour to redress an imposed nutritional imbalance improved with experience of feeding on T. triandra. As predicted, locusts fed T. aestivum always chose higher temperatures, irrespective of nutritional state. Our results have consequences for understanding host-plant choice by herbivores and interpreting the effects of changed environmental temperatures and microclimate on animal-plant interactions.

Protein-induced mass increase of the gastrointestinal tract of locusts improves net nutrient uptake via larger meals rather than more efficient nutrient absorption.

Increasing the tissue biomass and/or volume of the gastrointestinal tract (GIT) is commonly seen when animals feed on poor-quality diets. This increase can simply permit larger meal sizes, but may also rebalance nutritionally imbalanced ingesta by allowing selective absorption of limiting nutrients. In an insect herbivore, the migratory locust, a synthetic diet with a high ratio of protein to carbohydrate was found to induce mass enhancement of the GIT. When normalised for sex and overall body size, increases to the mass of the foregut and midgut caeca resulted in higher absorption (20-30%) of both protein and carbohydrate when subsequently feeding on three chemically and structurally different grasses. Greater net absorption of macronutrients occurred because these locusts ate larger meals that transited at the same time and with the same digestive efficiency as locusts in which the GIT was not enlarged. Thus, plasticity of the GIT did not improve nutritional homeostasis, but increased the rate of nutrient uptake.

Optimal foraging for specific nutrients in predatory beetles.

Evolutionary theory predicts that animals should forage to maximize their fitness, which in predators is traditionally assumed equivalent to maximizing energy intake rather than balancing the intake of specific nutrients. We restricted female predatory ground beetles (Anchomenus dorsalis) to one of a range of diets varying in lipid and protein content, and showed that total egg production peaked at a target intake of both nutrients. Other beetles given a choice to feed from two diets differing only in protein and lipid composition selectively ingested nutrient combinations at this target intake. When restricted to nutritionally imbalanced diets, beetles balanced the over- and under-ingestion of lipid and protein around a nutrient composition that maximized egg production under those constrained circumstances. Selective foraging for specific nutrients in this predator thus maximizes its reproductive performance. Our findings have implications for predator foraging behaviour and in the structuring of ecological communities.

Global patterns of leaf mechanical properties.

Leaf mechanical properties strongly influence leaf lifespan, plant-herbivore interactions, litter decomposition and nutrient cycling, but global patterns in their interspecific variation and underlying mechanisms remain poorly understood. We synthesize data across the three major measurement methods, permitting the first global analyses of leaf mechanics and associated traits, for 2819 species from 90 sites worldwide. Key measures of leaf mechanical resistance varied c. 500-800-fold among species. Contrary to a long-standing hypothesis, tropical leaves were not mechanically more resistant than temperate leaves. Leaf mechanical resistance was modestly related to rainfall and local light environment. By partitioning leaf mechanical resistance into three different components we discovered that toughness per density contributed a surprisingly large fraction to variation in mechanical resistance, larger than the fractions contributed by lamina thickness and tissue density. Higher toughness per density was associated with long leaf lifespan especially in forest understory. Seldom appreciated in the past, toughness per density is a key factor in leaf mechanical resistance, which itself influences plant-animal interactions and ecosystem functions across the globe.

Locusts use dynamic thermoregulatory behaviour to optimize nutritional outcomes.

Because key nutritional processes differ in their thermal optima, ectotherms may use temperature selection to optimize performance in changing nutritional environments. Such behaviour would be especially advantageous to small terrestrial animals, which have low thermal inertia and often have access to a wide range of environmental temperatures over small distances. Using the locust, Locusta migratoria, we have demonstrated a direct link between nutritional state and thermoregulatory behaviour. When faced with chronic restrictions to the supply of nutrients, locusts selected increasingly lower temperatures within a gradient, thereby maximizing nutrient use efficiency at the cost of slower growth. Over the shorter term, when locusts were unable to find a meal in the normal course of ad libitum feeding, they immediately adjusted their thermoregulatory behaviour, selecting a lower temperature at which assimilation efficiency was maximal. Thus, locusts use fine scale patterns of movement and temperature selection to adjust for reduced nutrient supply and thereby ameliorate associated life-history consequences.

Lifespan and reproduction in Drosophila: New insights from nutritional geometry.

Modest dietary restriction (DR) prolongs life in a wide range of organisms, spanning single-celled yeast to mammals. Here, we report the use of recent techniques in nutrition research to quantify the detailed relationship between diet, nutrient intake, lifespan, and reproduction in Drosophila melanogaster. Caloric restriction (CR) was not responsible for extending lifespan in our experimental flies. Response surfaces for lifespan and fecundity were maximized at different protein-carbohydrate intakes, with longevity highest at a protein-to-carbohydrate ratio of 1:16 and egg-laying rate maximized at 1:2. Lifetime egg production, the measure closest to fitness, was maximized at an intermediate P:C ratio of 1:4. Flies offered a choice of complementary foods regulated intake to maximize lifetime egg production. The results indicate a role for both direct costs of reproduction and other deleterious consequences of ingesting high levels of protein. We unite a body of apparently conflicting work within a common framework and provide a platform for studying aging in all organisms.

Cost of a naturally occurring two-amino acid deletion in cytochrome c oxidase subunit 7A in Drosophila simulans.

This study aimed to determine whether a naturally occurring (DeltaTrp85, DeltaVal86) deletion from a protein subunit of cytochrome c oxidase (complex IV) influenced cytochrome c oxidase activity, mRNA expression levels of electron transport chain genes, and aspects of adult female fitness in the fly Drosophila simulans. We modeled the tertiary structure of D. simulans cox7A containing the deletion by homology to the bovine cox7A structure and predicted that it would decrease the function of complex IV. This prediction led to the hypothesis that flies with the deletion would have lower cytochrome c oxidase activity and higher levels of mRNA expression from cox7A. This result was observed, but unexpectedly, elevated levels of mRNA expression were also observed in genes encoding subunits of complexes I, III, and IV. Together these data suggest that the deletion causes a high bioenergetic cost to the organism. To investigate the predicted cost at a physiological level, we assayed aspects of adult female fitness. Starvation sensitivity but not feeding rate was significantly influenced by the two-amino acid deletion. Further, we observed that carbohydrate and protein levels but not lipid levels were higher in the mutant flies. Together, these data show that quaternary structure modeling and biochemistry can be used to link the genotype with the organismal phenotype.

The gastrointestinal tract as a nutrient-balancing organ.

Failure to provision tissues with an appropriate balance of nutrients engenders fitness costs. Maintaining nutrient balance can be achieved by adjusting the selection and consumption of foods, but this may not be possible when the nutritional environment is limiting. Under such circumstances, rebalancing of an imbalanced nutrient intake requires post-ingestive mechanisms. The first stage at which such post-ingestive rebalancing might occur is within the gastrointestinal tract (GIT), by differential release of digestive enzymes-releasing less of those enzymes for nutrients present in excess while maintaining or boosting levels of enzymes for nutrients in deficit. Here, we use an insect herbivore, the locust, to show for the first time that such compensatory responses occur within the GIT. Furthermore, we show that differential release of proteases and carbohydrases in response to nutritional state translate into differential extraction of macronutrients from host plants. The prevailing view is that physiological and structural plasticity in the GIT serves to maximize the rate of nutrient gain in relation to costs of maintaining the GIT; our findings show that GIT plasticity is integral to the maintenance of nutrient balance.

Speed over efficiency: locusts select body temperatures that favour growth rate over efficient nutrient utilization.

Ectotherms have evolved preferences for particular body temperatures, but the nutritional and life-history consequences of such temperature preferences are not well understood. We measured thermal preferences in Locusta migratoria (migratory locusts) and used a multi-factorial experimental design to investigate relationships between growth/development and macronutrient utilization (conversion of ingesta to body mass) as a function of temperature. A range of macronutrient intake values for insects at 26, 32 and 38 degrees C was achieved by offering individuals high-protein diets, high-carbohydrate diets or a choice between both. Locusts placed in a thermal gradient selected temperatures near 38 degrees C, maximizing rates of weight gain; however, this enhanced growth rate came at the cost of poor protein and carbohydrate utilization. Protein and carbohydrate were equally digested across temperature treatments, but once digested both macronutrients were converted to growth most efficiently at the intermediate temperature (32 degrees C). Body temperature preference thus yielded maximal growth rates at the expense of efficient nutrient utilization.

Gross vs. net income: How plant toughness affects performance of an insect herbivore.

Leaf biomechanical properties are thought to impose a significant obstacle to herbivores and as such influence patterns of herbivory more than leaf chemistry. However, evidence for the role of structural traits in influencing herbivore food choice and performance has come from correlative studies, whereas the underlying mechanisms have been given little attention. By manipulating the biomechanical properties of a host grass species through a combination of lyophilization and milling, and providing water separately, we were able to compare behavioral, physiological, and developmental responses of the Australian plague locust, Chortoicetes terminifera, to the biomechanical properties of plant food (exemplified by toughness) independently of the food's macronutrient content and the insect's demand for water. Increasing leaf toughness was associated with reduced rates of locust growth and prolonged development, with potential ecological consequences. Poorer performance on the tougher foods was primarily a consequence of a reduced rate of nutrient supply, which occurred as a result of (1) smaller meals being eaten more slowly, (2) slowed gut passage rates, which limited how quickly the next meal could be taken, and (3) reduced efficiency of assimilation of nutrients from food in the gut. In addition, there were deleterious changes in the ratio of protein to carbohydrate assimilated from the gut. Prolonged development time was associated with increased total nutrient demands throughout the extended developmental period. Because these demands could not be met by increased consumption, there was a decreased efficiency of conversion of assimilated nutrients to growth. By disentangling the effects of biomechanical properties from macronutrient and water content we have shown that leaf biomechanical traits can influence chewing herbivores independently of leaf chemical traits.

Correlations between leaf toughness and phenolics among species in contrasting environments of Australia and New Caledonia.

BACKGROUND AND AIMS: Plants are likely to invest in multiple defences, given the variety of sources of biotic and abiotic damage to which they are exposed. However, little is known about syndromes of defence across plant species and how these differ in contrasting environments. Here an investigation is made into the association between carbon-based chemical and mechanical defences, predicting that species that invest heavily in mechanical defence of leaves will invest less in chemical defence. METHODS: A combination of published and unpublished data is used to test whether species with tougher leaves have lower concentrations of phenolics, using 125 species from four regions of Australia and the Pacific island of New Caledonia, in evergreen vegetation ranging from temperate shrubland and woodland to tropical shrubland and rainforest. Foliar toughness was measured as work-to-shear and specific work-to-shear (work-to-shear per unit leaf thickness). Phenolics were measured as 'total phenolics' and by protein precipitation (an estimate of tannin activity) per leaf dry mass. KEY RESULTS: Contrary to prediction, phenolic concentrations were not negatively correlated with either measure of leaf toughness when examined across all species, within regions or within any plant community. Instead, measures of toughness (particularly work-to-shear) and phenolics were often positively correlated in shrubland and rainforest (but not dry forest) in New Caledonia, with a similar trend suggested for shrubland in south-western Australia. The common feature of these sites was low concentrations of soil nutrients, with evidence of P limitation. CONCLUSIONS: Positive correlations between toughness and phenolics in vegetation on infertile soils suggest that additive investment in carbon-based mechanical and chemical defences is advantageous and cost-effective in these nutrient-deficient environments where carbohydrate may be in surplus.

Collective foraging in spatially complex nutritional environments.

Nutrition impinges on virtually all aspects of an animal's life, including social interactions. Recent advances in nutritional ecology show how social animals often trade-off individual nutrition and group cohesion when foraging in simplified experimental environments. Here, we explore how the spatial structure of the nutritional landscape influences these complex collective foraging dynamics in ecologically realistic environments. We introduce an individual-based model integrating key concepts of nutritional geometry, collective animal behaviour and spatial ecology to study the nutritional behaviour of animal groups in large heterogeneous environments containing foods with different abundance, patchiness and nutritional composition. Simulations show that the spatial distribution of foods constrains the ability of individuals to balance their nutrient intake, the lowest performance being attained in environments with small isolated patches of nutritionally complementary foods. Social interactions improve individual regulatory performances when food is scarce and clumpy, but not when it is abundant and scattered, suggesting that collective foraging is favoured in some environments only. These social effects are further amplified if foragers adopt flexible search strategies based on their individual nutritional state. Our model provides a conceptual and predictive framework for developing new empirically testable hypotheses in the emerging field of social nutrition.This article is part of the themed issue 'Physiological determinants of social behaviour in animals'.

Temperature, food quality and life history traits of herbivorous insects.

Population dynamics of herbivorous insects are strongly influenced by temperature and host plant quality; an interaction generally thought to be mediated via effects of temperature on metabolic rate and altered energy requirements. However, recent research suggests the relationship between nutrition, temperature, host plant quality and life history traits that influence insect fitness are more complex than appreciated to date. In the laboratory, rates of development are most strongly influenced by temperature, while growth, body composition, and reproductive output are greatly affected by nutrition, notably the uptake of protein and carbohydrate. However, individual outcomes and consequently population responses in the field are not readily predicted from data on ambient temperatures and host plant chemical composition. The relative amounts of protein and carbohydrate gained from a host plant depends on complex interactions between plant cell structure and leaf chemistry, combined with plasticity in feeding behaviour, microclimate selection, digestive and assimilative physiology. For example, grasshoppers can exploit the temperature dependence of host plant quality to maintain nutritional homeostasis. Consequently, understanding environmental interactions such as leaf defences and patterns of foraging, and predicting the effects of climate change on insect populations, will be complex.

Regulation of water and macronutrients by the Australian plague locust, Chortoicetes terminifera.

Nutritional outcomes for animals are best understood when the intake of multiple nutrients are considered together. The requirements for protein and carbohydrate and the consequences for development, growth and fitness when confined to sub-optimal amounts and ratios of these nutrients are well known for many herbivorous insects. Water is also essential for life, and it is known that herbivorous insects will actively ingest free water, have physiological mechanisms controlling thirst, and suffer fitness consequences if water is excessive or deficient in the diet. As herbivorous insects are thought to obtain the majority of their water from foliage, which can vary in protein, carbohydrate and water content, we investigated if the Australian plague locust, Chortoicetes terminifera, can select among complementary foods to attain a target intake across these three nutrient dimensions. Locusts demonstrated selection behaviour for protein, carbohydrate and water by eating non-randomly from different combinations of complementary foods. A ratio of P:C:H2O of 1:1.13:13.2 or 1(P+C): 6.2 H2O was ingested. Given that locusts strongly regulate water intake, and its importance as an essential resource, we suggest future studies consider the single and interactive influences of water, protein and carbohydrate, when evaluating herbivorous insect host choice and foraging decisions.

Modelling nutritional interactions: from individuals to communities.

Nutrient acquisition is a major context for ecological interactions among species but ecologists and nutritionists have developed theory in isolation from each other. Developments in agent-based modelling, state-space modelling of nutrition and multi-scale modelling of landscape ecology provide the components for a new synthesis in nutritional ecology linking the nutritional biology of individual organisms to population- and community-level processes across multiple scales within an evolutionary context. We review the core elements for such a synthesis and set out the principles for a generic modelling framework that could be used to test specific ecological hypotheses.

Behavioural phase polyphenism in the Australian plague locust (Chortoicetes terminifera).

Swarming and the expression of phase polyphenism are defining characteristics of locust species. Increases in local population density mediate morphological, physiological and behavioural changes within individuals, which correlate with mass marching of juveniles in migratory bands and flying swarms of adults. The Australian plague locust (Chortoicetes terminifera) regularly forms migratory bands and swarms, but is claimed not to express phase polyphenism and has accordingly been used to argue against a central role for phase change in locust swarming. We demonstrate that juvenile C. terminifera express extreme density-dependent behavioural phase polyphenism. Isolated-reared juveniles are sedentary and repelled by conspecifics, whereas crowd-reared individuals are highly active and are attracted to conspecifics. In contrast to other major locust species, however, behavioural phase change does not accumulate across generations, but shifts completely within an individual's lifetime in response to a change in population density.

Sex differences in nutrient-dependent reproductive ageing.

Evolutionary theories of aging predict that fitness-related traits, including reproductive performance, will senesce because the strength of selection declines with age. Sexual selection theory predicts, however, that male reproductive performance (especially sexual advertisement) will increase with age. In both bodies of theory, diet should mediate age-dependent changes in reproductive performance. In this study, we show that the sexes exhibit dramatic, qualitative differences in age-dependent reproductive performance trajectories and patterns of reproductive ageing in the cricket Teleogryllus commodus. In females, fecundity peaked early in adulthood and then declined. In contrast, male sexual advertisement increased across the natural lifespan and only declined well beyond the maximum field lifespan. These sex differences were robust to deviations from sex-specific dietary requirements. Our results demonstrate that sexual selection can be at least as important as sex-dependent mortality in shaping the signal of reproductive ageing.