Highly unsaturated fatty acids in nature: what we know and what we need to learn

The supply and demand of omega‐3 highly unsaturated fatty acids (ω‐3 HUFA) in natural ecosystems may lead to resource limitation in a diverse array of animal taxa. Here, we review why food quality in terms of ω‐3 HUFAs is important, particularly for neural tissue, across a diversity of animal taxa ranging from invertebrate zooplankton to vertebrates (including humans). Our review is focused on ω‐3 HUFAs rather than other unsaturated fatty acids because these compounds are especially important biochemically, but scarce in nature. We discuss the dichotomy between ω‐3 HUFA availability between aquatic primary producers, which are often rich in these compounds, and terrestrial primary producers, which are contain little to none of them. We describe the use of fatty acids as qualitative and quantitative tracers for reconstructing animal diets in natural ecosystems. Next, we discuss both direct and indirect ecological implications of ω‐3 HUFA limitation at the individual, population, food web, and ecosystem scales, which include: changes in behavior, species composition, secondary production rates, trophic transfer efficiency and cross‐ecosystem subsidies. We finish by highlighting future research priorities including a need for more research on ω‐3 HUFAs in terrestrial systems, more research their importance for higher order consumers, and more research on the food web and ecosystem‐scale effects of ω‐3 HUFA limitation. Synthesis Mismatches between the supply of and demand for omega‐3 highly unsaturated fatty acids (ω‐3 HUFA) in natural ecosystems have the potential to result in resource limitation across a diverse array of ecosystems. We combined perspectives from ecology and nutritional science to develop a unified synthesis of ω‐3 HUFA ecology. We reviewed the importance of ω‐3 HUFAs for animals, the striking differences in ω‐3 HUFA availability at the base of terrestrial versus aquatic food webs, and the implications of ω‐3 HUFA limitation for food webs. We finished by highlighting research priorities in the field including more research on ω‐3 HUFAs in terrestrial systems, on higher order consumers, and at the food web and ecosystem‐scales.     

Oligotrophication of a large,deep lake alters food quantity and quality constraints at the primary producer–consumer interface

To assess nutritional consequences associated with lake oligotrophication for aquatic consumers, we analyzed the elemental and biochemical composition of natural seston and concomitantly conducted laboratory growth experiments in which the freshwater key herbivore Daphnia was raised on natural seston of the nowadays (2008) oligotrophic Lake Constance throughout an annual cycle. Food quality mediated constraints on Daphnia performance were assessed by comparing somatic growth rates with seston characteristics (multiple regression analysis) and by manipulating the elemental and biochemical composition of natural seston experimentally (nutrient supplementation). Results were compared to similar experiments carried out previously (1997) during a mesotrophic phase of the lake. In the oligotrophic phase, particulate carbon and phosphorus concentrations were lower, fatty acid concentrations were higher, and the taxonomic composition of phytoplankton was less diverse, with a more diatom‐ and cryptophytes‐dominated community, compared to the previous mesotrophic phase. Multiple regression analysis indicated a shift from a simultaneous limitation by food quantity (in terms of carbon) and quality (i.e. α‐linolenic acid) during the mesotrophic phase to a complex multiple nutrient limitation mediated by food quantity, phosphorus, and omega‐3 fatty acids in the following oligotrophic phase. The concomitant supplementation experiments also revealed seasonal changes in multiple resource limitations, i.e. the prevalent limitation by food quantity was accompanied by a simultaneous limitation by either phosphorus or omega‐3 fatty acids, and thus confirmed and complemented the multiple regression approach. Our results indicate that seasonal and annual changes in nutrient availabilities can create complex co‐limitation scenarios consumers have to cope with, which consequently may also affect the efficiency of energy transfer in food webs.     

Nutrigenomics: a case study in the measurement of insect response to nutritional quality

Recent developments in the area of nutrigenomics hold the promise of providing valuable information about the impact of nutrition on a wide range of biochemical parameters by investigating how nutrition alters global gene expression patterns. Our goal is to use a nutrigenomics approach to identify insect molecular markers that could be used as early indicators of insect responses to different nutritional sources. Such molecular markers could be chosen for degree of expression and evaluated for suitability as nutritional biomarkers by examining developmental and generational expression. Ideal markers would be highly expressed, manifested in the first generation within one developmental stage, and consistent over many generations. Our objective for the current study was to illustrate the potential discovery of molecular markers using Perillus bioculatus (F.) (Heteroptera: Pentatomidae), when reared on an optimal vs. suboptimal diet, and analyze the presence of differentially expressed genes resulting from those treatments. In this paper we present preliminary results of microarray and subtractive hybridization experiments that represent the feasibility of using nutrigenomics to assist in analyzing insect responses to nutritional changes and dietary quality with the intent of stimulating further studies in this area.     

Biofluid 1H NMR-based metabonomic techniques in nutrition research - metabolic effects of dietary isoflavones in humans

A metabonomic approach to nutrition research may provide an insight into in vivo mechanisms of action following nutritional intervention. This approach was applied to investigate changes in the (1)H NMR spectral profile of urine collected from controlled dietary intervention studies conducted in premenopausal women before and following soy or miso consumption. The aim of the study was to identify the biochemical effects of a diet rich in soy isoflavones, phytochemicals which are receiving significant attention because of their potential importance to human health and wide bioactivity in vitro. By applying various chemometric techniques to the data the biochemical effects of conjugated and unconjugated isoflavones were determined. The biochemical changes observed suggest that soy isoflavone ingestion had significant effects on several metabolic pathways associated with osmolyte fluctuation and energy metabolism. These biochemical changes were more significant following ingestion of the unconjugated soy isoflavone (miso) diet suggesting that the chemical composition of the isoflavones present in soy-based foods may have an effect on their biological efficacy in vivo. This study describes a novel application for (1)H NMR analysis by determining subtle differences in biochemical profiles following dietary intervention and providing further insight into the mechanisms of action of phytochemicals in vivo.     

Is regional species diversity bounded or unbounded?

Two conflicting hypotheses have been proposed to explain large‐scale species diversity patterns and dynamics. The unbounded hypothesis proposes that regional diversity depends only on time and diversification rate and increases without limit. The bounded hypothesis proposes that ecological constraints place upper limits on regional diversity and that diversity is usually close to its limit. Recent evidence from the fossil record, phylogenetic analysis, biogeography, and phenotypic disparity during lineage diversification suggests that diversity is constrained by ecological processes but that it is rarely asymptotic. Niche space is often unfilled or can be more finely subdivided and still permit coexistence, and new niche space is often created before ecological limits are reached. Damped increases in diversity over time are the prevalent pattern, suggesting the need for a new ‘damped increase hypothesis'. The damped increase hypothesis predicts that diversity generally increases through time but that its rate of increase is often slowed by ecological constraints. However, slowing due to niche limitation must be distinguished from other possible mechanisms creating similar patterns. These include sampling artifacts, the inability to detect extinctions or declines in clade diversity with some methods, the distorting effects of correlated speciation‐extinction dynamics, the likelihood that opportunities for allopatric speciation will vary in space and time, and the role of undetected natural enemies in reducing host ranges and thus slowing speciation rates. The taxonomic scope of regional diversity studies must be broadened to include all ecologically similar species so that ecological constraints may be accurately inferred. The damped increase hypothesis suggests that information on evolutionary processes such as time‐for‐speciation and intrinsic diversification rates as well as ecological factors will be required to explain why regional diversity varies among times, places and taxa.     

Legume biofortification is an underexploited strategy for combatting hidden hunger

Legumes are the world's primary source of dietary protein and are particularly important for those in developing economies. However, the biofortification potential of legumes remains underexploited. Legumes offer a diversity of micronutrients and amino acids, exceeding or complementing the profiles of cereals. As such, the enhancement of legume nutritional composition presents an appealing target for addressing the “hidden hunger” of global micronutrient malnutrition. Affecting ~2 billion people, micronutrient malnutrition causes severe health effects ranging from stunted growth to reduced lifespan. An increased availability of micronutrient‐enriched legumes, particularly to those in socio‐economically deprived areas, would serve the dual functions of ameliorating hidden hunger and increasing the positive health effects associated with legumes. Here, we give an updated overview of breeding approaches for the nutritional improvement of legumes, and crucially, we highlight the importance of considering nutritional improvement in a wider ecological context. Specifically, we review the potential of the legume microbiome for agronomic trait improvement and highlight the need for increased genetic, biochemical, and environmental data resources. Finally, we state that such resources should be complemented by an international and multidisciplinary initiative that will drive crop improvement and, most importantly, ensure that research outcomes benefit those who need them most.     

Detecting spatial regimes in ecosystems

Research on early warning indicators has generally focused on assessing temporal transitions with limited application of these methods to detecting spatial regimes. Traditional spatial boundary detection procedures that result in ecoregion maps are typically based on ecological potential (i.e. potential vegetation), and often fail to account for ongoing changes due to stressors such as land use change and climate change and their effects on plant and animal communities. We use Fisher information, an information theory‐based method, on both terrestrial and aquatic animal data (U.S. Breeding Bird Survey and marine zooplankton) to identify ecological boundaries, and compare our results to traditional early warning indicators, conventional ecoregion maps and multivariate analyses such as nMDS and cluster analysis. We successfully detected spatial regimes and transitions in both terrestrial and aquatic systems using Fisher information. Furthermore, Fisher information provided explicit spatial information about community change that is absent from other multivariate approaches. Our results suggest that defining spatial regimes based on animal communities may better reflect ecological reality than do traditional ecoregion maps, especially in our current era of rapid and unpredictable ecological change.     

Bridging factorial and gradient concepts of resource co‐limitation: towards a general framework applied to consumers

Organism growth can be limited either by a single resource or by multiple resources simultaneously (co‐limitation). Efforts to characterise co‐limitation have generated two influential approaches. One approach uses limitation scenarios of factorial growth assays to distinguish specific types of co‐limitation; the other uses growth responses spanned over a continuous, multi‐dimensional resource space to characterise different types of response surfaces. Both approaches have been useful in investigating particular aspects of co‐limitation, but a synthesis is needed to stimulate development of this recent research area. We address this gap by integrating the two approaches, thereby presenting a more general framework of co‐limitation. We found that various factorial (co‐)limitation scenarios can emerge in different response surface types based on continuous availabilities of essential or substitutable resources. We tested our conceptual co‐limitation framework on data sets of published and unpublished studies examining the limitation of two herbivorous consumers in a two‐dimensional resource space. The experimental data corroborate the predictions, suggesting a general applicability of our co‐limitation framework to generalist consumers and potentially also to other organisms. The presented framework might give insight into mechanisms that underlie co‐limitation responses and thus can be a seminal starting point for evaluating co‐limitation patterns in experiments and nature.     

The role of natural plant products in modulating the immune system: An adaptable approach for combating disease in grazing animals

Plants provide herbivores with an array of chemicals with the potential to improve health and well-being. For instance, phytochemicals, known as secondary compounds, which protect plants from consumers and pests can adversely affect cellular and metabolic processes in herbivores, but at low doses and in appropriate mixtures, they can have beneficial effects on animal nutrition and health, though the latter has not been explored in great breadth or depth. In this review, we summarize the potential impact of natural plant products on immunomodulation and other therapeutic effects in herbivores. Development of preventative strategies to help animals resist disease would be a more economical, ecological and socially effective long-term healthcare strategy than treating diseases. In this realm, immunomodulation promoted by forages emerges as an interesting alternative and complement to chemotherapy. The challenge for feeding systems will be to incorporate mixes of plants with bioactive properties in ways that enhance health without compromising animal production and well-being. A solution to this challenge may involve developing management programs that acknowledge the ability of animals to learn about the beneficial effects of diverse foods.     

Describing and understanding behavioral responses to multiple stressors and multiple stimuli

Understanding the effects of environmental change on natural ecosystems is a major challenge, particularly when multiple stressors interact to produce unexpected “ecological surprises” in the form of complex, nonadditive effects that can amplify or reduce their individual effects. Animals often respond behaviorally to environmental change, and multiple stressors can have both population‐level and community‐level effects. However, the individual, not combined, effects of stressors on animal behavior are commonly studied. There is a need to understand how animals respond to the more complex combinations of stressors that occur in nature, which requires a systematic and rigorous approach to quantify the various potential behavioral responses to the independent and interactive effects of stressors. We illustrate a robust, systematic approach for understanding behavioral responses to multiple stressors based on integrating schemes used to quantitatively classify interactions in multiple‐stressor research and to qualitatively view interactions between multiple stimuli in behavioral experiments. We introduce and unify the two frameworks, highlighting their conceptual and methodological similarities, and use four case studies to demonstrate how this unification could improve our interpretation of interactions in behavioral experiments and guide efforts to manage the effects of multiple stressors. Our unified approach: (1) provides behavioral ecologists with a more rigorous and systematic way to quantify how animals respond to interactions between multiple stimuli, an important theoretical advance, (2) helps us better understand how animals behave when they encounter multiple, potentially interacting stressors, and (3) contributes more generally to the understanding of “ecological surprises” in multiple stressors research.     

Gender‐Specific Effects of Early Nutritional Restriction on Adult Obesity Risk: Evidence From Quasi‐Experimental Studies

In countries undergoing nutrition transition and historically poor minority groups in wealthy countries, obesity tends to be more common in women than men. A potential contributor to this female excess of obesity is a mismatch between perinatal nutritional restriction and a later calorie‐rich environment. Several epidemiologic and quasi‐experimental studies support a gender‐differential effect of early nutritional deprivation on adult obesity. The quasi‐experimental studies are of particular interest because results of quasi‐experimental studies are typically less vulnerable to confounding bias than observational studies. Four quasi‐experimental studies—exploiting 20th century famines that occurred in Europe, Africa, and Asia—provide evidence that perinatal nutritional restriction followed by relative caloric abundance may increase adult obesity risk to a greater extent in women than men. If the findings are accurate and generalizable to contemporary food environments, they suggest that the female offspring of poor, or otherwise nutritionally restricted, women in rapidly developing and wealthy countries may be at particularly high risk of adult obesity. Research into gender‐specific effects of early life nutritional deprivation and its interactions with later environmental exposures may provide insight into global gender differences in obesity prevalence.     

Assessing nutritional diversity of cropping systems in African villages

Background

In Sub-Saharan Africa, 40% of children under five years in age are chronically undernourished. As new investments and attention galvanize action on African agriculture to reduce hunger, there is an urgent need for metrics that monitor agricultural progress beyond calories produced per capita and address nutritional diversity essential for human health. In this study we demonstrate how an ecological tool, functional diversity (FD), has potential to address this need and provide new insights on nutritional diversity of cropping systems in rural Africa.

Methods and Findings

Data on edible plant species diversity, food security and diet diversity were collected for 170 farms in three rural settings in Sub-Saharan Africa. Nutritional FD metrics were calculated based on farm species composition and species nutritional composition. Iron and vitamin A deficiency were determined from blood samples of 90 adult women. Nutritional FD metrics summarized the diversity of nutrients provided by the farm and showed variability between farms and villages. Regression of nutritional FD against species richness and expected FD enabled identification of key species that add nutrient diversity to the system and assessed the degree of redundancy for nutrient traits. Nutritional FD analysis demonstrated that depending on the original composition of species on farm or village, adding or removing individual species can have radically different outcomes for nutritional diversity. While correlations between nutritional FD, food and nutrition indicators were not significant at household level, associations between these variables were observed at village level.

Conclusion

This study provides novel metrics to address nutritional diversity in farming systems and examples of how these metrics can help guide agricultural interventions towards adequate nutrient diversity. New hypotheses on the link between agro-diversity, food security and human nutrition are generated and strategies for future research are suggested calling for integration of agriculture, ecology, nutrition, and socio-economics.     

The effect of developmental nutrition on life span and fecundity depends on the adult reproductive environment in Drosophila melanogaster

Both developmental nutrition and adult nutrition affect life‐history traits; however, little is known about whether the effect of developmental nutrition depends on the adult environment experienced. We used the fruit fly to determine whether life‐history traits, particularly life span and fecundity, are affected by developmental nutrition, and whether this depends on the extent to which the adult environment allows females to realize their full reproductive potential. We raised flies on three different developmental food levels containing increasing amounts of yeast and sugar: poor, control, and rich. We found that development on poor or rich larval food resulted in several life‐history phenotypes indicative of suboptimal conditions, including increased developmental time, and, for poor food, decreased adult weight. However, development on poor larval food actually increased adult virgin life span. In addition, we manipulated the reproductive potential of the adult environment by adding yeast or yeast and a male. This manipulation interacted with larval food to determine adult fecundity. Specifically, under two adult conditions, flies raised on poor larval food had higher reproduction at certain ages – when singly mated this occurred early in life and when continuously mated with yeast this occurred during midlife. We show that poor larval food is not necessarily detrimental to key adult life‐history traits, but does exert an adult environment‐dependent effect, especially by affecting virgin life span and altering adult patterns of reproductive investment. Our findings are relevant because (1) they may explain differences between published studies on nutritional effects on life‐history traits; (2) they indicate that optimal nutritional conditions are likely to be different for larvae and adults, potentially reflecting evolutionary history; and (3) they urge for the incorporation of developmental nutritional conditions into the central life‐history concept of resource acquisition and allocation.     

Genotype‐by‐environment interactions underlie the expression of pre‐ and post‐copulatory sexually selected traits in guppies

The role that genotype‐by‐environment interactions (GEIs) play in sexual selection has only recently attracted the attention of evolutionary biologists. Yet GEIs can have profound evolutionary implications by compromising the honesty of sexual signals, maintaining high levels of genetic variance underlying their expression and altering the patterns of genetic covariance among fitness traits. In this study, we test for GEIs in a highly sexually dimorphic freshwater fish, the guppy Poecilia reticulata. We conducted an experimental quantitative genetic study in which male offspring arising from a paternal half‐sibling breeding design were assigned to differing nutritional ‘environments’ (either high or low feed levels). We then determined whether the manipulation of diet quantity influenced levels of additive genetic variance and covariance for several highly variable and condition‐dependent pre‐ and post‐copulatory sexual traits. In accordance with previous work, we found that dietary limitation had strong phenotypic effects on numerous pre‐ and post‐copulatory sexual traits. We also report evidence for significant GEI for several of these traits, which in some cases (area of iridescence and sperm velocity) reflected a change in the rank order of genotypes across different nutritional environments (i.e. ecological crossover). Furthermore, we show that genetic correlations vary significantly between nutritional environments. Notably, a highly significant negative genetic correlation between iridescent coloration and sperm viability in the high food treatment broke down under dietary restriction. Taken together, these findings are likely to have important evolutionary implications for guppies; ecological crossover may influence sexual signal reliability in unstable (nutritional) environments and contribute towards the extreme levels of polymorphism in sexual traits typically reported for this species. Furthermore, the presence of environment‐specific genetic covariance suggests that trade‐offs measured in one environment may not be indicative of genetic constraints in others.     

Parent-offspring conflict theory,signaling of need,and weight gain in early life

Human growth in early life has major implications for fitness. During this period, the mother regulates the growth of her offspring through placental nutrition and lactation. However, parent-offspring conflict theory predicts that offspring are selected to demand more resources than the mother is selected to provide. This general issue has prompted the development of begging theory, which attempts to find the optimal levels of offspring demand and parental provisioning. Several models have been proposed to account for begging behavior, whether by biochemical or behavioral pathways, including: (1) blackmail of parents; (2) scramble competition between multiple offspring; (3) honest signaling of nutritional need; and (4) honest signaling of offspring worth. These models are all supported by data from nonhuman animals, with species varying according to which model is relevant. This paper examines the evidence that human suckling and crying signal nutritional demand, need, and worth to the mother. While suckling provides hormonal stimulation of breast milk production and signals hunger, crying fulfills a different role, with evidence suggesting that it signals both worth and need for resources (nutrition and thermoregulation). The role of signaling in nutritional demand is examined in the context of three common health problems that have traditionally been assumed to have physiological rather than behavioral causes: excess weight gain, failure to thrive, and colic. The value of such an evolutionary approach lies in its potential to enhance behavioral management of these conditions.     

Ecological indicators for green building construction

Building construction is one of the largest final consumers of environmental resources as well as one of the largest emitters of greenhouse gas and other pollution. This paper aims to propose ecological indicators for green building construction by applying a slack-based data envelop analysis approach, in which resource conservation and environmental protection are both incorporated. We conduct an empirical analysis of ecological indicators for green building construction using China's regional panel dataset during 1995–2012, and use the analysis to further discuss the technological gaps across the regions. The findings show that: (i) half of China's provinces have a substantial potential increase of more than 60% in ecological performance for green building construction; (ii) the developed areas perform better than the developing areas; (iii) the 11th five-year plan period is a turning point for China's green building construction and development as the policies for green construction have significant effects.     

Gene expression profiling: opening the black box of plant ecosystem responses to global change

The use of genomic techniques to address ecological questions is emerging as the field of genomic ecology. Experimentation under environmentally realistic conditions to investigate the molecular response of plants to meaningful changes in growth conditions and ecological interactions is the defining feature of genomic ecology. Because the impact of global change factors on plant performance are mediated by direct effects at the molecular, biochemical, and physiological scales, gene expression analysis promises important advances in understanding factors that have previously been consigned to the 'black box' of unknown mechanism. Various tools and approaches are available for assessing gene expression in model and nonmodel species as part of global change biology studies. Each approach has its own unique advantages and constraints. A first generation of genomic ecology studies in managed ecosystems and mesocosms have provided a testbed for the approach and have begun to reveal how the experimental design and data analysis of gene expression studies can be tailored for use in an ecological context.     

Egg limitation and individual variation in parasitization risk among hosts in host–parasitoid dynamics

Egg limitation is known to destabilize host–parasitoid dynamics. This study reexamines the effect of egg limitation in light of the individual variation in parasitization risk among hosts (e.g., some hosts are more likely to be parasitized than others). Previous studies have considered egg limitation (predicted as a destabilizing factor) and individual variation among hosts (predicted as a stabilizing factor) in isolation; however, their interaction is not known. An individual‐based model was used to examine the effects of each factor and their interaction. The model‐based analysis shows a clear interaction between egg limitation and individual variation in risk among hosts. Egg limitation can both stabilize and destabilize host–parasitioid dynamics depending on the presence and absence of the risk variation. The result suggests that the population‐dynamic consequences of egg limitation are more complex than previously thought and emphasizes the importance of the simultaneous consideration of multiple ecological factors (with individual‐level details) to uncover potential interactions among them.     

Simultaneous effects of light intensity and phosphorus supply on the sterol content of phytoplankton

Sterol profiles of microalgae and their change with environmental conditions are of great interest in ecological food web research and taxonomic studies alike. Here, we investigated effects of light intensity and phosphorus supply on the sterol content of phytoplankton and assessed potential interactive effects of these important environmental factors on the sterol composition of algae. We identified sterol contents of four common phytoplankton genera, Scenedesmus, Chlamydomonas, Cryptomonas and Cyclotella, and analysed the change in sterol content with varying light intensities in both a high-phosphorus and a low-phosphorus approach. Sterol contents increased significantly with increasing light in three out of four species. Phosphorus-limitation reversed the change of sterol content with light intensity, i.e., sterol content decreased with increasing light at low phosphorus supply. Generally sterol contents were lower in low-phosphorus cultures. In conclusion, both light and phosphorus conditions strongly affect the sterol composition of algae and hence should be considered in ecological and taxonomic studies investigating the biochemical composition of algae. Data suggest a possible sterol limitation of growth and reproduction of herbivorous crustacean zooplankton during summer when high light intensities and low phosphorus supply decrease sterol contents of algae.