Food Requirement and Risk-Sensitive Foraging in Shortfall Minimizers

Risk-sensitive foraging documents the response of animals to variances in their food supply. This potentially powerful theory has only recently received attention by ecologists. Scenarios incorporating risk-sensitive foraging are presented in an effort to further stimulate ecologists to persue this subject. Animals facing time constraints due to predator avoidance or other conflicting demands during foraging are likely to exhibit risk-sensitive foraging. Risk-sensitive foraging in the population context is also discussed, and conditions are outlined under which risk-sensitive foraging should exist as a density-dependent strategy.

Risk—sensitive foraging decision (i.e., those based on both reward mean and variance) have often been observed in laboratory contexts, but there are few observations of risk—sensitive foraging in the wild. Indeed, wild foragers need not show risk sensitivity, since they can adopt alternative tactics for minimizing their probabilities of energy shortfall. I tested for risk—sensitive foraging in a natural context in coastal southwest British Columbia, Canada. Seablush (Plectritis congesta) and dwarf huckleberry (Vaccinium caespitosum) are co—occurring plants that offer foraging bumble bees equivalent expected rates of net energy intake, but that differ in variability. The equalization of mean profitabilities of floral rewards results from the actions of nectar—collecting foragers. Risk—sensitive diet choice can therefore be based solely on the variances of the foraging alternatives. I manipulated the energy requirements of bumble bee colonies (Bombus melanopygus, B. mixtus, B. sitkensis) by draining or enhancing their honey pots. I then censused foragers from these colonies on the two flower species. If bees were risk sensitive in their diet choice, they should have increased their relative use of the more variable flower type (dwarf huckleberry) when their colonies were nectar depleted compared to when their colonies were nectar enhanced. This was indeed the case. Wild—foraging bumble bees thus appear to be sensitive to both the mean and the variance of the energy rewards offered by alternative flower species, and this sensitivity is affected by colony energy requirements. These results suggest that wild foragers may change their risk sensitivity.

Risk-sensitivity: ambient temperature affects foraging choice

Importance of whole-plant biomass allocation and reproductive timing to habitat differentiation across the North American sunflowers.

This virtual (online) study tested the common but largely untested assumptions that food energy density, level of processing (NOVA categories), and carbohydrate-to-fat (CF) ratio are key determinants of food reward. Individual participants (224 women and men, mean age 35 y, 53% with healthy weight, 43% with overweight or obesity) were randomised to one of three, within-subjects, study arms: energy density (32 foods), or level of processing (24 foods), or CF ratio (24 foods). They rated the foods for taste pleasantness (liking), desire to eat (food reward), and sweetness, saltiness, and flavour intensity (for analysis averaged as taste intensity). Against our hypotheses, there was not a positive relationship between liking or food reward and either energy density or level of processing. As hypothesised, foods combining more equal energy amounts of carbohydrate and fat (combo foods), and foods tasting more intense, scored higher on both liking and food reward. Further results were that CF ratio, taste intensity, and food fibre content (negatively), independent of energy density, accounted for 56% and 43% of the variance in liking and food reward, respectively. We interpret the results for CF ratio and fibre in terms of food energy-to-satiety ratio (ESR), where ESR for combo foods is high, and ESR for high-fibre foods is low. We suggest that the metric of ESR should be considered when designing future studies of effects of food composition on food reward, preference, and intake.

Are pigs sensitive to variability in food rewards?

Foraging theory depicts dietary choice as a function of prey quality and absolute abundance. Ecological processes, however, can depend on the way foragers respond to the relative abundances of available prey types; several models for frequency-dependent foraging adequately describe these responses. Our laboratory experiments with white-throated sparrows investigated preferential choice of two food rewards as we manipulated both reward quality and relative abundance. In any single experiment the two rewards provided the same mean food quantity, but the variances differed. Average energy budgets predicted risk-aversion, so that foraging preference should decrease as reward variance increases. We presented each two-reward pairing at availability ratios of 1:2, 1:1, and 2:1 for three consecutive days. By the third day risk-aversion exceeded preference for reward variance significantly. When relative abundances of the low and high variance rewards were not equal, the birds tended to prefer the rare over the common reward. This response began before the birds had thoroughly sampled the reward distributions. Preference for rarity apparently constrained the birds' economic response to reward variance levels.

Periodic fluctuations or cycles in populations of small mammals have been widely studied, but much controversy still exists about their causes. Cycles of voles and lemmings are produced by the integrated effects of intrinsic and extrinsic factors, and the problem is to define accurately how these interact. Spacing behavior is a key component of population regulation in voles and lemmings, and this is illustrated most dramatically by the fence effect. We do not know which mechanisms produce changes in social behavior. Phenotypic changes produced by maternal effects or stress are now believed most likely, but there has been too little work done on genetic effects on spacing and we know almost nothing about kin-related social behavior in voles and lemmings. Both predation and food supply may be the extrinsic factors involved in cyclic population dynamics. Single-factor experiments suggest that food shortage by itself does not seem to be a necessary factor for cycles nor does predation, but the interaction between food and predation could be a key variable in understanding how extrinsic factors affect cycles of voles. Cycles of snowshoe hares are caused by an interaction between predation and food supplies, possibly integrated through risk-sensitive foraging. Spacing behavior is not a component of cycles of hares because snowshoe hares differ from voles and lemmings in having no known form of spacing behavior that can produce social mortality. The short-term cycle of voles and lemmings thus seems to have a different explanation from the long-term cycle of snowshoe hares. In some places, lemmings may be locked in a predator-pit at low density. Experimental exclusion of predators improved survival of adults in a population of collared lemmings, but was not sufficient to allow them to escape the predator-pit because of losses of juveniles. Whether cyclic populations of lemmings also fall into a predator-pit in the low phase remains to be determined. The low phase does not occur in every cycle and it is particularly difficult to explain. Progress in analyzing cyclic fluctuations has been made most rapidly when we define clear alternative hypotheses and carry out experimental manipulations on field populations. Much remains to be done on these small mammals.

Understanding the responses of foragers to patchy distributions of resources has formed a fundamental challenge in behavioral ecology. Two currencies have been used to assess the patch preferences of herbivores—intake rate maximization and risk sensitivity. We wished to understand if small mammalian foragers, collared lemmings (Dichrostonyx groenlandicus), choose patches to maximize food intake rate or to reduce risk of starvation in “variable” environments. Moreover, we examined the possibility that maximizing intake rate depends on the spatial scale of patchiness. We designed an experiment offering two alternative patches of food, varying the predictability of food rewards and the “potential intake rate” at different spatial scales. Collared lemmings did not consistently select patches that maximized their intake rate at either scale studied. Instead, they chose patches offering the least variation in food reward over the course of the experiment. Collared lemmings used prior knowledge gained from previous foraging bouts to assess food variability. We interpret these results as evidence for risk-averse foraging strategies, which are predicted for continuous foragers aiming to minimize risk of starvation.

Risk-sensitive foraging may occur whenever feeding success has non-linear effects on fitness. Models of sensitivity to variation in amount of food obtained have concentrated on foraging in order to survive even though feeding during growth, migration, or reproduction can have strong and non-linear effects on fitness. I illustrate how risk-sensitive foraging for reproduction could differ from risk-sensitive foraging for survival using two simple models. Each model assumes that organisms must accumulate some threshold amount of resources before they can reproduce. In the first model, additional resources above the threshold lead to increased reproductive success. Here variance in feeding success can be advantageous even when the mean gain would allow organisms to reproduce. In the second model, early breeding is superior to late breeding because recruitment rate declines over time. Here a symmetrical distribution in foraging rates results in a skewed distribution of breeding times. Despite this, variance in feeding success may be advantageous even when the seasonal decline in recruitment is linear. The advantage of risk is much larger if foragers can switch freely between feeding options. These two models are united by “the bankruptcy effect” because all failures to reproduce carry the same consequences. These simple models suggest that risk-prone foraging may be likely when factors other than survival are important for fitness. Finally, I advocate using a mix of modelling techniques, note the implicitly risk-sensitive nature of stochastic dynamic programming, and speculate on potential connections between risk-sensitive foraging and theories of life histories in variable environments. INTRODUCTION visit restaurants that provided twice

Locusts can learn associations between olfactory stimuli and food rewards, and use the acquired memories to choose between foods according to their nutrient requirements. They are a model system for both the study of olfactory coding and insect nutritional regulation. Previous studies have used operant paradigms for conditioning freely moving locusts, restricting the study of the neural mechanisms underlying the acquisition of olfactory memories, which requires restrained preparations for electrophysiological recordings. Here we present two complementary paradigms for the classical conditioning of olfactory memories in restrained desert locusts (Schistocerca gregaria). These paradigms allow precise experimental control over the parameters influencing learning. The first paradigm is based on classical (Pavlovian) appetitive conditioning. We show that opening of the maxillary palps can be used as a measure of memory acquisition. Maxillary palp opening in response to odour presentation is significantly higher in locusts trained with paired presentation of an odour and a food reward than in locusts trained either with unpaired presentation of food and odour or the odour alone. The memory formed by this conditioning paradigm lasts for at least 24 h. In the second paradigm, we show that classical conditioning of an odour memory in restrained locusts influences their decisions in a subsequent operant task. When locusts that have been trained to associate an odour with a food reward are placed in a Y-maze, they choose the arm containing that odour significantly more often than naïve locusts. A single conditioning trial is sufficient to induce a significant bias for that odour for up to 4 h. Multiple- and block-trial training induce a significant bias that lasts at least 24 h. Thus, locusts are capable of forming appetitive olfactory memories in classical conditioning paradigms and can use these memories to modify their decisions.

Does variation in glucocorticoid concentrations predict fitness? A phylogenetic meta-analysis

We compare the (relative) abundance of life phases [juveniles (JU), initial phase (IP) and terminal phase (TP) fish], social categories (territorial and group adults), and fish following alternative mating styles, in three local populations of the protogynous reef herbivore,Sparisoma viride, on the fringing reef of Bonaire (Netherlands Antilles). In order to determine the adaptive significance of variations in social organization, they are related to the density of conspecifics and other herbivores and to the availability of food, shelter and mating sites. The most striking difference is the high abundance of JU and group fish at one location (Playa Frans) and the total absence of group fish at another (Red Slave). These differences are coherent with a gradient in population density, total herbivore density, scarid grazing pressure, and reproductive output, all of which are highest at Playa Frans and lowest at Red Slave. Exposure to waves and currents shows an inverse trend. The differences in the relative abundance of territorial fish can be explained by the concept of economic defendability, which is reduced at higher population density. In a life history context, small TP group males represent ‘bachelors’ that sacrifice current reproduction for better future prospects. As predicted by life history theory, early sex change is promoted at sites where the future rewards are higher (higher spawning rates of large TP males) and where the costs incurred during the bachelor phase are reduced (more spawning opportunities for group TP males). At Red Slave an alternative male mating style (‘streaking’) appears to be promoted by the lack of a refuge for group TP males and by a dense gorgonian canopy, allowing IP males to reside inside territories. We conclude that most observed differences in population structure can be considered adaptive in an ecological and in a life history context. Population density is a major factor in both contexts. Analysis of the variability in adult density in relation to JU density and the availability of food and shelter indicates that theS. viride populations at Bonaire are not totally controlled by stochastic processes. Considering the small spatial scale and the high dispersal of the planktonic embryos and larvae, the observed variability in behavioural and life history traits ofS. viride points to a high degree of phenotypic plasticity.

Risk-sensitive foraging theory predicts that predators which face starvation if there is a temporary shortfall in their food supply should choose feeding sites on the basis of variation in as well as mean expected reward rate. For a given mean reward rate they should choose high variance feeding sites (be risk-prone) if they are running below energy requirement, but low variance sites (be risk-averse) if they are running above. Common shrews presented with a choice between constant and variable feeding stations were more likely to visit the variable station when they were running below energy requirement and more likely to visit the constant station when they were running above. However, the tendency towards risk-aversion above requirement was greater than that towards risk-proneness below. When all shrews were considered together, the probability of visiting the variable station correlated negatively and continuously with intake relative to requirement.

Wintering Black Ducks (Anas rubripes) concentrate in wetlands along the Atlantic coast where natural and anthropogenic disturbances have increased over the last 50 years, a period in which the population of Black Ducks has declined. We studied the sensitivity of Black Ducks to perturbations in food supply that often result from disturbances by storms, predators, and people. In the paper, we characterize the responses of captive Black Ducks to shifts in food quality and availability during winter and apply those measures to a comparison of wild birds. Captive ducks that were fed intermittently (3 consecutive days/week) compensated for fasted days to achieve similar body mass and body fat to control birds that were fed every day on both animal- and plant-based diets. However, birds that were fed intermittently expended 15% more energy each day than controls when both groups were fed (536 vs. 464kJ/kg0.75), which indicates that variable food supply increases the costs of maintenance and thus reduces the number of birds that can be supported on the same resource of food without interruptions to foraging. Egg production was not affected by diet quality provided in spring or by the frequency of feeding during the preceding winter months. Black Ducks lost body fat through winter in captivity and in the wild. Fat stores of birds in New Jersey were greater than those of birds in Maine (13.3 vs. 8.3% of body mass) in January, which reflected the high energy demands of cold temperatures in Maine. Values for ∂15N were greater in Maine than in New Jersey for both red blood cells and plasma, which indicated a consistent diet of marine invertebrates in Maine. Greater isotopic variation in red blood cells indicated that diets were more diverse in New Jersey than in Maine for both ∂15N (9.7 ± 1.1 vs. 11.2 ± 0.4‰) and for ∂13C (- 15.1 ± 2.2 vs. - 13.8 ± 1.4‰). Plasma ∂13C was enriched over red blood cells in wild birds especially those with low fat stores, which suggested birds with low energy stores were shifting diets. Black Ducks can compensate for disturbances in feeding by increasing intakes if they have access to high quality wetlands where they are able to find abundant food. High energy demands at cold temperatures may constrain fat stores and thus the tolerance of feeding disturbances especially at the northern limits of the winter range. We hypothesize that decreasing variation in diet may indicate an increase in vulnerability to disturbance in winter when body fat is low. Recent efforts to assess and improve habitat quality of Black Ducks could be enhanced by monitoring the body composition and diet of birds to assess their vulnerability to disturbances in food supply and energy demands.