David Mayntz

Protein-leverage in Mice : The Geometry of Macronutrient Balancing and Consequences for Fat Deposition

Objective: The Protein‐Leverage Hypothesis proposes that humans regulate their intake of macronutrients and that protein intake is prioritized over fat and carbohydrate intake, causing excess energy ingestion when diets contain low %protein. Here we test in a model animal, the mouse: (i) the extent to which intakes of protein and carbohydrate are regulated; (ii) if protein intake has priority over carbohydrates so that unbalanced foods low in %protein leads to increased energy intake; and (iii) how such variations in energy intake are converted into growth and storage.

The Life of a Dead Ant: The Expression of an Adaptive Extended Phenotype

Specialized parasites are expected to express complex adaptations to their hosts. Manipulation of host behavior is such an adaptation. We studied the fungus Ophiocordyceps unilateralis, a locally specialized parasite of arboreal Camponotus leonardi ants. Ant‐infecting Ophiocordyceps are known to make hosts bite onto vegetation before killing them. We show that this represents a fine‐tuned fungal adaptation: an extended phenotype. Dead ants were found under leaves, attached by their mandibles, on the northern side of saplings ∼25 cm above the soil, where temperature and humidity conditions were optimal for fungal growth. Experimental relocation confirmed that parasite fitness was lower outside this manipulative zone. Host resources were rapidly colonized and further secured by extensive internal structuring. Nutritional composition analysis indicated that such structuring allows the parasite to produce a large fruiting body for spore production. Our findings suggest that the osmotrophic lifestyle of fungi may have facilitated novel exploitation strategies.

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.

NUTRIENT‐SPECIFIC COMPENSATION FOLLOWING DIAPAUSE IN A PREDATOR: IMPLICATIONS FOR INTRAGUILD PREDATION

In recent years it has become clear that intraguild predation (where predators feed on other predators) has important consequences for food webs, and yet very little is known about its nutritional or functional bases. In the most detailed study of the nutritional basis of foraging by a predator to date, we used geometrical analysis to test the ability of the generalist invertebrate predatory beetle, Agonum dorsale (Carabidae), to forage selectively for lipid and protein over a 10-day period following emergence from winter diapause, and we measured associated changes in body lipid and nitrogen content. Over the first 48 hours, beetles that were offered two nutritionally imbalanced but complementary foods self-selected a diet high in lipids, and thereafter the proportion of protein in the selected diet increased. Beetles confined to a single food with excess lipid (higher lipid:protein ratio than the self-selected diet) regulated intake to meet lipid requirements, while suffering a shortfall of protein. Those given diets with a lower lipid:protein ratio than the self-selected diet showed a progressive tendency across the 10-day experiment to over-ingest protein, thereby reducing the lipid deficit in their diet. Body composition changed markedly during the experiment, with the lipid content of the self-selecting insects increasing over the first 48 hours from 14% to 46% by dry mass, and thereafter remaining stable. We discuss some implications of our results for the understanding of intraguild predation.

Balancing of protein and lipid intake by a mammalian carnivore, the mink, Mustela vison.

Many herbivores and omnivores can balance their intake of macronutrients when faced with nutritionally variable environments. Carnivores, however, are widely believed to optimize their rates of prey capture and energy intake rather than balancing nutrients. We tested nutrient balancing in captive mink and found a pronounced ability to balance and regulate intake of protein and lipid. When faced with one of several different pairings of complementary foods varying in protein to lipid composition, mink apportioned intake between the two foods to defend a near constant ratio and amount (intake target) of the two macronutrients. When given only one food of fixed nutrient composition, mink balanced macronutrient intake relative to the intake target, without showing the excessive energy intake on diets with a low percentage of protein and energy deficit on diets with a high percentage of protein previously reported for herbivores and omnivores, including humans. This demonstration of nutrient balancing in a carnivorous mammal indicates that the capacity for nutrient balancing is a more general phenomenon across trophic levels than was hitherto believed to be the case.

Protein and carbohydrate composition of larval food affects tolerance to thermal stress and desiccation in adult Drosophila melanogaster

Larval nutrition may affect a range of different life history traits as well as responses to environmental stress in adult insects. Here we test whether raising larvae of fruit flies, Drosophila melanogaster, on two different nutritional regimes affects resistance to cold, heat and desiccation as well as egg production and egg-to-adult viability. We raised larvae on a carbohydrate-enriched and a protein-enriched growth medium. We found that flies developed on the high protein medium had increased heat and desiccation tolerance compared to flies developed on the carbohydrate-enriched medium. In contrast, flies developed on the carbohydrate-enriched growth medium recovered faster from chill coma stress compared to flies developed on a protein-enriched medium. We also found gender differences in stress tolerance, with female flies being more tolerant to chill coma, heat knockdown and desiccation stress compared to males. Egg production was highest in females that had developed on the protein-enriched medium. However, there was a sex-specific effect of nutrition on egg-to-adult viability, with higher viability for males developing on the sucrose-enriched medium, while female survival was highest when developing on the protein-enriched medium. Our study indicates that larval nutrition has a strong impact on the ability to cope with stress, and that the optimal nutrient composition varies with the type of stress.

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°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°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°C). Body temperature preference thus yielded maximal growth rates at the expense of efficient nutrient utilization.

Metabolic consequences of feeding and fasting on nutritionally different diets in the wolf spider Pardosa prativaga.

We investigated whether spiders fed lipid-rich rather than protein-rich prey elevate metabolism to avoid carrying excessive lipid deposits, or whether they store ingested lipids as a buffer against possible future starvation. We fed wolf spiders (Pardosa prativaga) prey of different lipid:protein compositions and measured the metabolic rate of spiders using closed respirometry during feeding and fasting. After a 16-day feeding period, spider lipid:protein composition was significantly affected by the lipid:protein composition of their prey. Feeding caused a large and fast increase in metabolism. The cost of feeding and digestion was estimated to average 21% of the ingested energy irrespective of diet. We found no difference in basal metabolic rate between dietary treatments. During starvation V ₀₂ and V(CO)₂decreased gradually, and the larger lipid stores in spiders fed lipid-rich prey appeared to extend survival of these spiders under starvation compared to spiders fed protein-rich prey. The results show that these spiders do not adjust metabolism in order to maintain a constant body composition when prey nutrient composition varies. Instead, lipids are stored efficiently and help to prepare the spiders for the long periods of food deprivation that may occur as a consequence of their opportunistic feeding strategy.

Nutrient balance affects foraging behaviour of a trap-building predator

Predator foraging may be affected by previous prey capture, but it is unknown how nutrient balance affects foraging behaviour. Here, we use a trap-building predator to test whether nutrients from previous prey captures affect foraging behaviour. We fed orb-weaving spiders (Zygiella x-notata) prey flies of different nutrient composition and in different amounts during their first instar and measured the subsequent frequency of web building and aspects of web architecture. We found that both the likelihood of web building and the number of radii in the web were affected by prey nutrient composition while prey availability affected capture area and mesh height. Our results show that both the balance of nutrients in captured prey and the previous capture rate may affect future foraging behaviour of predators.

Specialist ant-eating spiders selectively feed on different body parts to balance nutrient intake

Specialized predators must obtain all required nutrients from a single prey species. In some species nutrient balance may be possible by selecting various body parts. We tested how different ant body parts affect the fitness of a specialized ant predator and whether the predator possesses adaptations in its feeding behaviour that allow nutrient balancing while feeding on only a single prey species. We used a formicine-specialist spider, Zodarion rubidum, reared on three diet types: an entire ant, two ant gasters and two ant foreparts (heads, thoraces and legs) of Lasius ants. Spiders grew faster, survived longer and developed earlier on the diet consisting of two ant foreparts. Spiders fed on the two ant gasters had the slowest growth, highest mortality and slowest development while spiders fed entire ants showed intermediate performance. In preference experiments, we studied the spiders’ consumption of three Formicinae ant species that differ markedly in size. With small Lasius ants, spiders equally exploited the gaster and the foreparts, but with larger Formica and Camponotus ants, spiders fed significantly more on the foreparts than on the gaster. Spiders almost always fed on the gaster, suggesting that it might include beneficial nutrients. Nutritional analysis of the ant bodies of the three species revealed that there were more lipids in the gaster, while the foreparts contained more proteins. Our results suggest that ant-eating spiders might balance their nutritional needs by selectively consuming various body parts of their exclusive prey.