Bert J. Tolkamp

Towards a functional explanation for the occurrence of anorexia during parasitic infections

The development and occurrence of anorexia, the voluntary reduction in food intake during parasitic infections in animals, is somewhat paradoxical and contrary to conventional wisdom and expectation. We take the view that its occurrence is an evolved, costly behavioural adaptation which serves a function. Five such functional and general hypotheses to account for it are developed: (1) anorexia is induced by the parasite for its own benefit; (2) food intake decreases to starve parasites; (3) the negative effect on the hosts energetic efficiency during parasitic diseases has a direct effect on food consumption; (4) food intake decreases for the purpose of promoting an effective immune response in the host; and (5) anorexia allows the host to become more selective in its diet, and thus select foods that either minimize the risk of infection or are high in antiparasitic compounds. Only hypotheses (4) and (5) survive the comparison for consistency with the physiological, metabolic and behavioural alterations that occur during the development of parasitic infections, and with the rule of generality (i.e. account for its occurrence in both protozoan and helminth infections). Both surviving hypotheses will need further experimental testing for their support or rejection, and such experiments are proposed. Also, the advantages and consequences of viewing anorexia during parasitic infections within a functional framework are discussed. These arise from the recognition that anorexia is a disease-coping strategy, part of the mechanism of recognition of parasite invasion by the immune system, which leads to a modification of the hosts feeding behaviour. Copyright 1998 The Association for the Study of Animal Behaviour

Changes in Feeding Behavior as Possible Indicators for the Automatic Monitoring of Health Disorders in Dairy Cows

Changes in short-term feeding behavior of dairy cows that occur with the onset of the health disorders ketosis, acute locomotory problems, and chronic lameness were investigated using data collected during previous experiments. The objective of the study was to describe and quantify those changes and to test their suitability as early indicators of disease. Feed intake, feeding time, and number of daily feeder visits were recorded with computerized feeders. Ketosis in 8 cows was characterized by rapid daily decreases in feed intake [-10.4 kg of fresh matter (FM)], feeding time (-45.5 min), and feeding rate (-25.3 g of FM/min) during an average of 3.6 d before diagnosis by farm staff. Acute locomotion disorders in 14 cows showed smaller daily decreases in feed intake (-1.57 kg of FM) and feeding time (-19.1 min), and a daily increase in feeding rate (+21.6 g of FM/min) during an average of 7.7 d from onset to diagnosis. The effects of chronic lameness on short-term feeding behavior were assessed by analyzing changes during the 30 d before and 30 d after all cows were checked for foot lesions and trimmed, and cows were classified as either lame (n = 81) or not lame (n = 62). During the 30 d before trimming, cows classified as lame showed significant changes in daily feeding time, number of daily visits, and feeding rate, but nonlame cows did not. In lame cows, the observed daily changes (slope) for the 30 d before and the 30 d after trimming were -0.75 and +0.32 min/d for daily feeding time, -0.35 and +0.31 for daily number of visits, and +0.77 and -0.35 g/min for feeding rate, respectively. These changes in feeding behavior were not different among cows consuming low or high forage rations. Daily feeding time was the feeding characteristic that changed most consistently in relation to the studied disorders. A simple algorithm was used to identify cows whose daily feeding time was lower than the previous 7-d rolling average minus 2.5 standard deviations. The algorithm resulted in detection of more than 80% of cows with acute disorders at least 1 d before diagnosis by farm staff. Short-term feeding behavior showed very characteristic changes with the onset of disorders, which suggests that a system that monitors short-term feeding behavior can assist in the early identification of sick cows.

To split behaviour into bouts, log-transform the intervals.

Analysis of behaviour that is displayed in bouts depends crucially on quantitative estimates of bout criteria, that is, the lengths of the shortest intervals between bouts. Current methods estimate bout criteria by modelling the log-transformed (cumulative) frequency distributions of intervals between events. For analysis of feeding behaviour, these models will not result in biologically meaningful quantitative estimates (Tolkamp et al. 1998, Journal of Theoretical Biology194, 235-250). We proposed a method that models the frequency distribution of log-transformed interval lengths instead. Applying this method to a single data set showed that the log-transformed lengths of intervals between feeding events were distributed as two Gaussians. Here we test this model using a data set of 35 171 intervals between feeding that was obtained during an experiment with 38 cows in three dietary treatment groups. No meaningful bout criterion could be obtained for some individuals, which casts doubt on the general validity of the proposed model. Addition of a third log-normal improved the fit of the model and we hypothesized that this third population represents intervals including drinking. In a second experiment, we found the measurements to be consistent with this hypothesis. We obtained meaningful meal criteria for all individuals by fitting either a double, or a triple, log-normal model to the frequency distributions of the lengths of intervals between feeding. These log-normal models appear to be not only more biologically meaningful than log (cumulative) frequency models but also far more flexible. Copyright 1999 The Association for the Study of Animal Behaviour.

‘Freedom from hunger’ and preventing obesity: the animal welfare implications of reducing food quantity or quality

In animals, including humans, free access to high-quality (generally energy-dense) food can result in obesity, leading to physiological and health problems. Consequently, various captive animals, including laboratory and companion animals and certain farm animals, are often kept on a restricted diet. Quantitative restriction of food is associated with signs of hunger such as increases in feeding motivation, activity and redirected oral behaviours which may develop into stereotypies. An alternative approach to energy intake restriction is to provide more food, but of a reduced quality. Such alternative diets are usually high in fibre and have lower energy density. The benefits of these alternative diets for animals are controversial: some authors argue that they result in more normal feeding behaviour, promote satiety and so improve animal welfare; others argue that ‘metabolic hunger’ remains no matter how the restriction of energy intake and weight gain is achieved. We discuss the different arguments behind this controversy, focusing on two well-researched cases of food-restricted farmed livestock: pregnant sows and broiler breeders. Disagreement between experts results from differences in assumptions about what determines and controls feeding behaviour and food intake, from the methodology of assessing animal hunger and from the weighting placed on ‘naturalness’ of behaviour as a determinant of welfare. Problems with commonly used behavioural and physiological measures of hunger are discussed. Future research into animal feeding preferences, in particular the relative weight placed on food quantity and quality, would be valuable, alongside more fundamental research into the changes in feeding physiology associated with alternative diets.

The evolution of the control of food intake

The ultimate goal of an organism is to maximise its inclusive fitness, and an important sub-goal must be the optimisation of the lifetime pattern of food intake, in order to meet the nutrient demands of survival, growth and reproduction. The conventional assumption that fitness is maximised by maximising daily food intake, subject to physical and physiological constraints, has been challenged recently. Instead, it can be argued that fitness is maximised by balancing benefits and costs over the organisms lifetime. The fitness benefits of food intake are a function of its contribution to survival, growth (including necessary body reserves) and reproduction. Against these benefits must be set costs. These costs include not only extrinsic foraging costs and risks, such as those due to predation, but also intrinsic costs associated with food intake, such as obesity and oxidative metabolism that may reduce vitality and lifespan. We argue that the aggregate of benefits and costs form the fitness function of food intake and present examples of such an approach to predicting optimal food intake.

Associations between basal metabolic rate and reproductive performance in C57BL/6J mice

SUMMARY Basal metabolic rate (BMR) is highly variable, both between and within species. One hypothesis is that this variation may be linked to the capacity for sustained rate of energy expenditure, leading to associations between high BMR and performance during energy-demanding periods of life history, such as reproduction. However, despite the attractive nature of this hypothesis, previous studies have failed to show an association between BMR and fecundity. Our approach was to mate 304 C57BL/6J mice and allow them to wean pups before measuring BMR by indirect calorimetry. We did not find an association between BMR and litter mass, size or pup mass at birth or weaning that could not be accounted for by the body mass of the dam. There was also no relationship between BMR (or BMR corrected for body mass) and birth or weaning success, losses during weaning, or sex ratio. However, a significant relationship was found between BMR and gestational weight loss indicative of foetal resorption. This suggests that during pregnancy the available energy may be limited and partitioned away from the growing foetus and towards maintenance of the mother. In this context, a high BMR may actually be disadvantageous, conflicting with the idea that high BMR may bring reproductive benefits.

A Theory of Associating Food Types with Their Postingestive Consequences

Animals often face complex and changing food environments. While such environments are challenging, an animal should make an association between a food type and its properties (such as the presence of a nutrient or toxin). We use information theory concepts, such as mutual information, to establish a theory for the development of these associations. In this theory, associations are assumed to maximize the mutual information between foods and their consequences. We show that associations are invariably imperfect. An association’s accuracy increases with the length of a feeding session and the relative frequency of a food type but decreases as time delay between consumption and postingestive consequence increases. Surprisingly, the accuracy of an association is independent of the number of additional food types in the environment. The rate of information transfer between novel foods and a forager depends on the forager’s diet. In light of this theory, an animal’s diet may have two competing goals: first, the provision of an appropriate balance of nutrients, and second, the ability to quickly and accurately learn the properties of novel foods. We discuss the ecological and behavioral implications of making associational errors and contrast the timescale and mechanisms of our theory with those of existing theory.

Analysis of the feeding behavior of pigs using different models

Short-term feeding behavior is conventionally analysed using random process models. The assumption underlying these models have recently been questioned and this article describes the application of both random, and more biologically based, models to the feeding behavior of pigs. Feeder visits of 16 growing pigs, housed individually from 17 to 52 kg live weight, were recorded electronically over a continuous period of 35 days. Daily food intake increased linearly with time, but there was considerable individuality in the degree of order. Pigs made between 18.8 and 80.3 (mean 47.9) daily visits to the feeder. Intervals between visits could be described by two log-normal distributions. Two Gaussian density functions were fitted to the distribution of the log-transformed intervals. For the combined data from all animals the within- and between-meal intervals were 11.2 s and 100.1 min, respectively. A model with three Gaussian functions gave an improved fit to the interval distribution. The within and between meal intervals were then estimated to be 4.2 s and 93.9 min, respectively. The middle distribution of intervals ranged from 0.5 to 38.1 min. The intervals were also described by random process models; again, a three-process model gave an improved fit compared to a two-process model. The mean estimated number of meals per day from the three Gaussian model was 14.3, and from the three process random model, 16.3. A biological interpretation of the three types of interval suggests that: (1) pigs eat in meals separated by long intervals; (2) meals consist of clusters of eating bouts separated by shorter intervals, sometimes associated with drinking; (3) within each eating bout short intervals occur as pigs constantly move in and out of the feeder. It remains unclear what underlies the observed patterns of eating.

Intake Compensates for Resting Metabolic Rate Variation in Female C57BL/6J Mice Fed High-fat Diets

Objective: The literature is divided over whether variation in resting metabolic rate (RMR) is related to subsequent obesity. We set out to see whether the effect of RMR on weight gain in mice could be revealed with high‐fat feeding.

Control of energy balance in relation to energy intake and energy expenditure in animals and man: an ecological perspective

In this paper, we consider the control of energy balance in animals and man. We argue that patterns of mammalian feeding have evolved to control energy balance in uncertain environments. It is, therefore, expected that, under sedentary conditions in which the diet is rich in nutrients and abundantly available, animals and man will overeat. This suggests that no physiological defects are needed to induce overweight and ultimately obesity in man. Several considerations arise from these observations. The time period over which energy balance is controlled is far longer than allowed by most experiments. Physiological models of energy balance control often treat excess energy intake as a defect of regulation; ecological models view the same behaviour as part of normal energy balance control in environments where resources are uncertain. We apply these considerations to common patterns of human and animal feeding. We believe that the ecological perspective gives a more accurate explanation for the functionality of excess fat and the need to defend nutrient balance and avoid gross imbalances, as well as explaining hyperphagia in the face of plenty. By emphasising the common features of energy balance control in different mammalian species, the importance of changes in behaviour to accommodate changes in the environment becomes apparent. This also opens up possibilities for the control of body weight and the treatment of obesity in man.