Abstract:Animals' foraging behavior and dietary choices are, in part, driven by their ultimate function: to meet nutritional demands. However, depending on their degree of dietary specialization and the availability and distribution of food resources in their environment, species may utilize different nutritional strategies. With shifting plant phenology, increasing unpredictability of fruiting, and declining food quality in response to anthropogenic climate change, existing nutritional constraints may become exacerbat… Show more
“…The AP : NPE ratio in the diets of wild diademed sifaka lemurs (Propithecus diadema) remained remarkably constant across seasons and habitats (intact versus disturbed), suggesting macronutrient balancing [43]. Beeby et al [44] inferred nutrient balancing in another lemur, the black-and-white ruffed lemur (Varecia variegata), whose diet varied in AP : NPE across seasons but, as the authors had predicted, across the year the AP : NPE was maintained more tightly. Johnson et al [45] reported that guerezas (Colobus guereza) maintained a consistent AP : NPE when feeding across foraging patches, and the ratio was a good indicator of time spent foraging within patches.…”
Section: (A) Laboratory Experimentsmentioning
confidence: 93%
“…Beeby et al . [44] inferred nutrient balancing in another lemur, the black-and-white ruffed lemur ( Varecia variegata ), whose diet varied in AP : NPE across seasons but, as the authors had predicted, across the year the AP : NPE was maintained more tightly. Johnson et al .…”
Section: Nutrient Balancing In the Laboratory And Fieldmentioning
confidence: 99%
“…Most primates studied to date are reported to show protein prioritization, in which AP intake is maintained within narrower boundaries than NPE (figure 1). These include spider monkeys [37], black howler monkeys [46], Kenyan blue monkeys [47], capuchins [48], golden snub-nose monkeys [23] (figure 4 b ), orang-outans [49], black-and-white ruffed lemurs [44], small-bodied lemurs [50] and chimpanzees [51]. There are three known exceptions.…”
Section: Nutrient Balancing In the Laboratory And Fieldmentioning
Diet and nutrition comprise a complex, multi-faceted interface between animal biology and food environments. With accumulating information on the many facets of this association arises a need for systems-based approaches that integrate dietary components and their links with ecology, feeding, post-ingestive processes and the functional and ecological consequences of these interactions. We briefly show how a modelling approach, nutritional geometry, has used the experimental control afforded in laboratory studies to begin to unravel these links. Laboratory studies, however, have limited ability to establish whether and how the feeding and physiological mechanisms interface with realistic ecological environments. We next provide an overview of observational field studies of free-ranging primates that have examined this, producing largely correlative data suggesting that similar feeding mechanisms operate in the wild as in the laboratory. Significant challenges remain, however, in establishing causal links between feeding, resource variation and physiological processes in the wild. We end with a more detailed account of two studies of temperate primates that have capitalized on the discrete variation provided by seasonal environments to strengthen causal inference in field studies and link patterns of intake to dynamics of nutrient processing.
This article is part of the theme issue ‘Food processing and nutritional assimilation in animals’.
“…The AP : NPE ratio in the diets of wild diademed sifaka lemurs (Propithecus diadema) remained remarkably constant across seasons and habitats (intact versus disturbed), suggesting macronutrient balancing [43]. Beeby et al [44] inferred nutrient balancing in another lemur, the black-and-white ruffed lemur (Varecia variegata), whose diet varied in AP : NPE across seasons but, as the authors had predicted, across the year the AP : NPE was maintained more tightly. Johnson et al [45] reported that guerezas (Colobus guereza) maintained a consistent AP : NPE when feeding across foraging patches, and the ratio was a good indicator of time spent foraging within patches.…”
Section: (A) Laboratory Experimentsmentioning
confidence: 93%
“…Beeby et al . [44] inferred nutrient balancing in another lemur, the black-and-white ruffed lemur ( Varecia variegata ), whose diet varied in AP : NPE across seasons but, as the authors had predicted, across the year the AP : NPE was maintained more tightly. Johnson et al .…”
Section: Nutrient Balancing In the Laboratory And Fieldmentioning
confidence: 99%
“…Most primates studied to date are reported to show protein prioritization, in which AP intake is maintained within narrower boundaries than NPE (figure 1). These include spider monkeys [37], black howler monkeys [46], Kenyan blue monkeys [47], capuchins [48], golden snub-nose monkeys [23] (figure 4 b ), orang-outans [49], black-and-white ruffed lemurs [44], small-bodied lemurs [50] and chimpanzees [51]. There are three known exceptions.…”
Section: Nutrient Balancing In the Laboratory And Fieldmentioning
Diet and nutrition comprise a complex, multi-faceted interface between animal biology and food environments. With accumulating information on the many facets of this association arises a need for systems-based approaches that integrate dietary components and their links with ecology, feeding, post-ingestive processes and the functional and ecological consequences of these interactions. We briefly show how a modelling approach, nutritional geometry, has used the experimental control afforded in laboratory studies to begin to unravel these links. Laboratory studies, however, have limited ability to establish whether and how the feeding and physiological mechanisms interface with realistic ecological environments. We next provide an overview of observational field studies of free-ranging primates that have examined this, producing largely correlative data suggesting that similar feeding mechanisms operate in the wild as in the laboratory. Significant challenges remain, however, in establishing causal links between feeding, resource variation and physiological processes in the wild. We end with a more detailed account of two studies of temperate primates that have capitalized on the discrete variation provided by seasonal environments to strengthen causal inference in field studies and link patterns of intake to dynamics of nutrient processing.
This article is part of the theme issue ‘Food processing and nutritional assimilation in animals’.
“…Many species of non-human primates, for example, maintain daily protein intakes within narrow limits, allowing fat and carbohydrate to vary more widely with ecologically imposed variation in the macronutrient ratios of available diets—a pattern of macronutrient regulation termed ‘protein prioritization’ ( figure 1 a , b ). Known instances include spider monkeys [ 19 ], black howler monkeys [ 20 ], golden snub-nosed monkeys [ 17 ] ( figure 1 d ), Kenyan blue monkeys [ 18 ] ( figure 1 d ), black-and-white ruffed lemurs [ 21 ], orangutans [ 22 ] and chimpanzees [ 23 ]. Figure 1 Theoretical depiction of the protein prioritization pattern of macronutrient regulation and empirical examples from non-human primates.…”
Despite the large volume and extensive range of obesity research, there is substantial disagreement on the causes and effective preventative strategies. We suggest the field will benefit from greater emphasis on integrative approaches that examine how various potential contributors interact, rather than regarding them as competing explanations. We demonstrate the application of nutritional geometry, a multi-nutrient integrative framework developed in the ecological sciences, to obesity research. Such studies have shown that humans, like many other species, regulate protein intake more strongly than other dietary components, and consequently if dietary protein is diluted there is a compensatory increase in food intake—a process called protein leverage. The protein leverage hypothesis (PLH) proposes that the dilution of protein in modern food supplies by fat and carbohydrate-rich highly processed foods has resulted in increased energy intake through protein leverage. We present evidence for the PLH from a variety of sources (mechanistic, experimental and observational), and show that this mechanism is compatible with many other findings and theories in obesity research.
This article is part of a discussion meeting issue ‘Causes of obesity: theories, conjectures and evidence (Part II)’.
“…Several studies have shown the behavioral impacts of seasonal resource availability on these lemurs (Balko, 1998;Balko & Brian Underwood, 2005;Beeby & Baden, 2021;Britt, 2000;Ratsimbazafy, 2002Ratsimbazafy, , 2006Rigamonti, 1993); fewer have investigated the physiological impacts of this seasonality (Morland, 1993;Vasey, 2004Vasey, , 2005. Due to their adaptations to frugivory, in combination with declines in calorie intakes during fruit-lean seasons (Beeby et al, 2023), ruffed lemurs may be at high risk of experiencing negative energy balance (expending more energy than they consume) during sustained periods of fruit scarcity. Moreover, the ability to maintain energetic conditions throughout lean seasons may be a driver of certain ruffed lemur life history traits, such as their "boom-bust" reproduction (Ratsimbazafy, 2002) and communal nesting (Baden, 2011;Baden et al, 2013).…”
Measuring energy balance and energy metabolism can provide crucial information for understanding the ecological and behavioral drivers of an animal's energetic and physiological condition. Both urinary C‐peptide (uCP) of insulin and urinary total triiodothyronine (uTT3) have been validated as noninvasive biomarkers of energy balance and metabolic activity in haplorrhine primates. This study attempts to validate uCP and uTT3 measures in strepsirrhines, a phylogenetically distinct primate clade, using the ruffed lemur (genus Varecia) as a model. We experimentally manipulated the diet of captive black‐and‐white (Varecia variegata) and red (Varecia rubra) ruffed lemurs at Duke Lemur Center across a 4‐week period. We collected urine samples from subjects (n = 5) each day during 1 week of control diet, 2 weeks of calorie‐restricted diet and 1 week of refeeding, designed to temporarily reduce energy balance and metabolism. We also tested the outcome of filter paper as a storage method by comparing to controls (frozen at −20°C) to assess its suitability for studies of wild populations. We successfully measured uCP and uTT3 levels in frozen urine samples using commercial enzyme immunoassay kits and found that both biomarkers were excreted at lower concentrations (C‐peptide: 1.35 ng/mL, 54% reduction; TT3: 1.5 ng/mL, 37.5% reduction) during calorie‐restricted periods compared to normal diet periods. Filter paper recovery for uCP was 19%, though values were significantly positively correlated with frozen control samples. uTT3 could not be recovered at measurable concentrations using filter paper. These methods enable noninvasive measurement of energetic conditions in wild strepsirrhines and subsequent assessment of relationships between energy balance and numerous socioecological drivers in primate populations.
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