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Nutrition has long been considered more the domain of medicine and agriculture than of the biological sciences, yet it touches and shapes all aspects of the natural world. The need for nutrients determines whether wild animals thrive, how populations evolve and decline, and how ecological communities are structured.The Nature of Nutritionis the first book to address nutrition's enormously complex role in biology, both at the level of individual organisms and in their broader ecological interactions. Stephen Simpson and David Raubenheimer provide a comprehensive theoretical approach to the analysis of nutrition--the Geometric Framework. They show how it can help us to understand the links between nutrition and the biology of individual animals, including the physiological mechanisms that determine the nutritional interactions of the animal with its environment, and the consequences of these interactions in terms of health, immune responses, and lifespan. Simpson and Raubenheimer explain how these effects translate into the collective behavior of groups and societies, and in turn influence food webs and the structure of ecosystems. Then they demonstrate how the Geometric Framework can be used to tackle issues in applied nutrition, such as the problem of optimizing diets for livestock and endangered species, and how it can also help to address the epidemic of human obesity and metabolic disease Drawing on a wealth of examples from slime molds to humans,The Nature of Nutritionhas important applications in ecology, evolution, and physiology, and offers promising solutions for human health, conservation, and agriculture.

Temperature and nutrition are amongst the most common environmental challenges faced by organisms and will become increasingly so with ongoing climate change. While we have learnt a great deal about how temperature and nutrition affect life‐history traits on their own, we know very little about their combined effect on animal performance. Given that animals in the wild are likely to experience changes in both their thermal and nutritional conditions, we need to understand how interactions between these conditions shape an animal's response if we hope to mitigate the effects of environmental change. In the present research, we investigated the combined effects of nutrition and temperature on key life‐history traits in Drosophila melanogaster. Using nutritional geometry, developing larvae were exposed to a range of diets varying in their protein and carbohydrate content and to one of two developmental temperature regimes (25°C and 28°C). We then examined key life‐history traits: development time, viability, and two estimates of body size—wing and femur size. We found that developmental temperature significantly changed the response to nutrition for all traits. Increased temperature led to more restricted trait optima for all traits and exacerbated the negative effects of carbohydrate‐rich diets, resulting in harsher trade‐offs between life‐history traits. For example, at 25°C there were more diets that led to high viability, fast development and large body size than at 28°C. However, for the diets that produced the best outcomes for each trait, temperature had less of an effect. These findings highlight the importance of studying the effects of combined stressors when assessing animals' responses to changing environmental conditions. A free Plain Language Summary can be found within the Supporting Information of this article. A free Plain Language Summary can be found within the Supporting Information of this article.

Nutritional geometry has shown the benefits of viewing nutrition in a multidimensional context, in which foraging is viewed as a process of balancing the intake and use of multiple nutrients. New insights into nutrient regulation have been generated in studies performed in a laboratory context, where accurate measures of amounts (e.g. eaten, converted to body mass, excreted) can be made and analysed using amounts-based nutritional geometry. In most field situations, however, proportional compositions (e.g. of foods, diets, faeces) are the only measures readily available, and in some cases are more relevant to the problem at hand. For this reason, a complementary geometric method was recently introduced for analysing multi-dimensional data on proportional compositions in nutritional studies, called the right-angled mixture triangle (RMT). We use literature data from field studies of primates to demonstrate how the RMT can provide insight into a variety of important concepts in nutritional ecology. We first compare the compositions of foods, using as an example primate milks collected in both the wild and the laboratory. We next compare the diets of different species of primates from the same habitat and of the same species (mountain gorillas) from two distinct forests. Subsequently, we model the relationships between the composition of gorilla diets in these two habitats and the foods that comprise these diets, showing how such analyses can provide evidence for active nutrient-specific regulation in a field context. We provide a framework to relate concepts developed in laboratory studies with field-based studies of nutrition.

Homeostatic responses of animals to environmentally induced changes in nutrient requirements provide a powerful basis for predictive ecological models, and yet, such responses are virtually unstudied in the wild. We tested for macronutrient‐specific compensatory feeding responses by free‐ranging golden snub‐nosed monkeys (Rhinopithecus roxellana) inhabiting high altitude temperate forests, where they experience a substantial difference in ambient temperature in cold winters vs. warmer springs. The monkeys had free access to natural foods throughout the year, and to ensure that any seasonal differences in nutrient intake were due to homeostatic compensation and not constraints on food availability, we studied the monkeys during periods in which they were provisioned with the same amount of supplementary foods in winter and spring. Thermoregulatory energy costs in winter and spring were calculated using partitional calorimetric estimations of convective and radiative heat loss obtained from thermal imaging of free‐ranging monkeys in situ. Daily nutrient intakes were measured using continuous focal follows (average 6.9 hr/day) of free‐ranging individuals (27 days in spring and 28 days in winter). We used a nutritional geometry framework to integrate these data and test three predictions: (a) In order to remain thermoneutral (balance heat loss with heat expenditure), golden snub‐nosed monkeys increase daily energy consumption during the winter compared to spring; (b) this increase is achieved specifically by increasing intake of the primary energetic nutrients, carbohydrate and lipid, relative to protein; and (c) the seasonal increase in ingested fat and carbohydrate calories will quantitatively match the additional thermoregulatory costs in winter compared with spring. Our results showed that daily metabolisable energy intake in winter (721.5 kJ/mbm) was 1.8 times that in spring (399 kJ/mbm). As predicted, this difference was specific to fat and carbohydrate, whereas seasonal protein intake did not differ significantly. Winter consumption of fat and carbohydrate was 326 kJ/mbm per day greater than in spring, a value that closely matched the seasonal difference in the daily energetic costs of thermoregulation (329 kJ/mbm). This is the first study to test for a match between nutrient‐specific homeostatic compensation and environmentally induced perturbations in nutrient requirements in free‐ranging animals and underpins the potential for the homeostasis framework to provide predictive power to ecological models. Foreign Language 动物应对环境改变而寻求营养上平衡可以基于稳健的生态模型进行预测,然而这种预测在野外研究上却很少实现 秦岭金丝猴生活在高寒高海拔山区,其环境温度在冬春两季差异剧烈。于是,我们对一个自由活动的金丝猴种群进行常量营养成分摄入进行研究,来分析常量营养成分摄入应对环境变化的补偿性的应答机制。为了保证我们的研究结果是由于动物自我平衡所致,而非是环境资源限制所致,我们让金丝猴全年都在自然食物环境中采食,只有在冬季和春季开展研究时段,我们才给研究对象提供等质等量的人工食物补充 根据我们采集的热成像照片,我们测量动物体表不同部位的温度,并依据金丝猴不同姿态下体表暴露的部位比例,来计算身体热对流和辐射导致的热损失。我们平均每天连续跟踪6.9小时的目标个体,来计算其每日能量摄入。冬季跟踪28天,春季跟踪27天 我们用营养几何模型整合分析了以上数据,对3种预测结果进行验证:1.金丝猴为了保证其体温的稳定(也就是平衡热损失和热收益),将在冬季增加能量摄入;2.在三种基础常量营养成分中,金丝猴在冬季预期将增加碳水化合物和脂类养分的摄入,而保持蛋白质稳定;3. 金丝猴对碳水化合物和脂类两种常量养分的能量摄入在冬春两季的差值,预期将等于其在冬春两季体表热能量损失的差值 我们的研究结果显示,金丝猴冬季代谢能摄入(721.5千焦/公斤体重)是春季的(399千焦/公斤体重) 1.8倍。正如预期所示,金丝猴的冬春能量摄入变异主要来源于碳水化合物和脂类产生的能量差异,蛋白质能量摄入在两个季节保持稳定不变。金丝猴摄入的碳水化化合物和脂类能量在冬季比春季每天多326 千焦/公斤体重, 而这个值恰恰与它们的每天在冬春两季体表热能损失的差值329千焦/公斤体重极为接近 该研究首次验证了自由活动的野生动物在对环境干扰时,具有营养摄入的自我平衡能力。对于自我平衡理论体系而言,该研究成果充分证明该体系下的生态模型的确具有预测能力 A plain language summary is available for this article. Plain Language Summary

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 individualbased 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'.

It is commonly assumed that because males produce many, tiny sperm, they are cheap to produce. Recent work, however, suggests that sperm production is not cost-free. If sperm are costly to produce, sperm number and/or viability should be influenced by diet, and this has been documented in numerous species. Yet few studies have examined the exact nutrients responsible for mediating these effects. Here, we quantify the effects of protein (P) and carbohydrate (C) intake on sperm number and viability in the cockroach Nauphoeta cinerea, as well as the consequences for male fertility. We found the intake of P and C influenced sperm number, being maximized at a high intake of diets with a P : C ratio of 1 : 2, but not sperm viability. The nutritional landscapes for male fertility and sperm number were closely aligned, suggesting that sperm number is the major determinant of male fertility in N. cinerea. Under dietary choice, males regulate nutrient intake at a P : C ratio of 1 : 4.95, which is midway between the ratios needed to maximize sperm production and pre-copulatory attractiveness in this species. This raises the possibility that males regulate nutrient intake to balance the trade-off between pre- and post-copulatory traits in this species.

Wolbachia are maternally inherited bacterial endosymbionts that naturally infect a diverse array of arthropods. They are primarily known for their manipulation of host reproductive biology, and recently, infections with Wolbachia have been proposed as a new strategy for controlling insect vectors and subsequent human-transmissible diseases. Yet, Wolbachia abundance has been shown to vary greatly between individuals and the magnitude of the effects of infection on host life-history traits and protection against infection is correlated to within-host Wolbachia abundance. It is therefore essential to better understand the factors that modulate Wolbachia abundance and effects on host fitness. Nutrition is known to be one of the most important mediators of host–symbiont interactions. Here, we used nutritional geometry to quantify the role of macronutrients on insect–Wolbachia relationships in Drosophila melanogaster. Our results show fundamental interactions between diet composition, host diet selection, Wolbachia abundance and effects on host lifespan and fecundity. The results and methods described here open a new avenue in the study of insect–Wolbachia relationships and are of general interest to numerous research disciplines, ranging from nutrition and life-history theory to public health.

Phosphorus has been identified as an important determinant of nutrition-related biological variation. The macronutrients protein (P) and carbohydrates (C), both alone and interactively, are known to affect animal performance. No study, however, has investigated the importance of phosphorus relative to dietary protein or carbohydrates, or the interactive effects of phosphorus with these macronutrients, on fitness-related traits in animals. We used a nutritional geometry framework to address this question in adult field crickets (Gryllus veletis). Our results showed that lifespan, weight gain, acoustic mate signalling and egg production were maximized on diets with different P : C ratios, that phosphorus did not positively affect any of these fitness traits, and that males and females had different optimal macronutrient intake ratios for reproductive performance. When given a choice, crickets selected diets that maximized both lifespan and reproductive performance by preferentially eating diets with low P : C ratios, and females selected diets with a higher P : C ratio than males. Conversely, phosphorus intake was not regulated. Overall, our findings highlight the importance of disentangling the influences of different nutrients, and of quantifying both their individual and interactive effects, on animal fitness traits, so as to gain a more integrative understanding of their nutritional ecology.

Summary Herbivores face various nutritional challenges in their life cycles, challenges that may become increasingly acute under ongoing environmental changes. Here, focusing on calcium, phosphorus and nitrogen, we used nutritional geometry to analyse individual‐based data on foraging and extraction efficiencies, and combined these with data on reproduction and migratory behaviour to understand how a large herbivorous carnivore can complete its life cycle on a narrow and seemingly low quality bamboo diet. Behavioural results showed that pandas during the year switched between four main food categories involving the leaves and shoots of two bamboo species available. Nutritional analysis suggests that these diet shifts are related to the concentrations and balances of calcium, phosphorus and nitrogen. Notably, successive shifts in range use and food type corresponded with a transition to higher concentrations and/or a more balanced intake of these multiple key constituents. Our study suggests that pandas obligatorily synchronize their seasonal migration and reproduction with the disjunct nutritional phenologies of two bamboo species. This finding has potentially important implications for habitat conservation for this species and, more generally, draws attention to the need for understanding the nutritional basis of food selection in devising management plans for endangered species. Lay Summary

Animals make feeding decisions to simultaneously maximize fitness traits that often require different nutrients. Recent quantitative methods have been developed to characterize these nutritional trade-offs from performance landscapes on which traits are mapped on a nutrient space defined by two nutrients. This limitation constrains the broad applications of previous methods to more complex data, and a generalized framework is needed. Here, we build on previous methods and introduce a generalized vector-based approach—the vector of position approach—to study nutritional trade-offs in complex multidimensional spaces. The vector of position approach allows the estimate of performance variations across entire landscapes (peaks and valleys) and comparison of these variations between animals. Using landmark published data sets on life span and reproduction landscapes, we illustrate how our approach gives accurate quantifications of nutritional trade-offs in two- and three-dimensional spaces and can bring new insights into the underlying nutritional differences in trait expression between species. The vector of position approach provides a generalized framework for investigating nutritional differences in life-history trait expression within and between species, an essential step for the development of comparative research on the evolution of animal nutritional strategies.