Herbivore population regulation and resource heterogeneity in a stochastic environment.

Large-mammal herbivore populations are subject to the interaction of internal density-dependent processes and external environmental stochasticity. We disentangle these processes by linking consumer population dynamics, in a highly stochastic environment, to the availability of their key forage resource via effects on body condition and subsequent fecundity and mortality rates. Body condition and demographic rate data were obtained by monitoring 500 tagged female goats in the Richtersveld National Park, South Africa, over a three-year period. Identifying the key resource and pathway to density dependence for a population allows environmental stochasticity to be partitioned into that which has strong feedbacks to population stability, and that which does not. Our data reveal a density- dependent seasonal decline in goat body condition in response to concomitant density-dependent depletion of the dry-season forage resource. The loss in body condition reduced density-dependent pregnancy rates, litter sizes, and pre-weaning survival. Survival was lowest following the most severe dry season and for juveniles. Adult survival in the late-dry season depended on body condition in the mid-dry season. Population growth was determined by the length of the dry season and the population size in the previous year. The RNP goat population is thereby dynamically coupled primarily to its dry-season forage resource. Extreme environmental variability thus does not decouple consumer resource dynamics, in contrast to the views of nonequilibrium protagonists.

Having it all: historical energy intakes do not generate the anticipated trade-offs in fecundity.

An axiom of life-history theory, and fundamental to our understanding of ageing, is that animals must trade-off their allocation of resources since energy and nutrients are limited. Therefore, animals cannot "have it all"--combine high rates of fecundity with extended lifespans. The idea of life-history trade-offs was recently challenged by the discovery that ageing may be governed by a small subset of molecular processes independent of fitness. We tested the "trade-off" and "having it all" theories by examining the fecundities of C57BL/6J mice placed onto four different dietary treatments that generated caloric intakes from -21 to +8.6% of controls. We predicted body fat would be deposited in relation to caloric intake. Excessive body fat is known to cause co-morbidities that shorten lifespan, while caloric restriction enhances somatic protection and increases longevity. The trade-off model predicts that increased fat would be tolerated because reproductive gain offsets shortened longevity, while animals on a restricted intake would sacrifice reproduction for lifespan extension. The responses of body fat to treatments followed our expectations, however, there was a negative relationship between reproductive performance (fecundity, litter mass) and historical intake/body fat. Our dietary restricted animals had lower protein oxidative damage and appeared able to combine life-history traits in a manner contrary to traditional expectations by having increased fecundity with the potential to have extended lifespans.

The evolution of phylogenetic differences in the efficiency of digestion in ruminants.

This study investigates, for the first time (to our knowledge) for any animal group, the evolution of phylogenetic differences in fibre digestibility across a wide range of feeds that differ in potential fibre digestibility (fibre to lignin ratio) in ruminants. Data, collated from the literature, were analysed using a linear mixed model that allows for different sources of random variability, covariates and fixed effects, as well as controlling for phylogenetic relatedness. This approach overcomes the problem of defining boundaries to separate different ruminant feeding styles (browsers, mixed feeders and grazers) by using two covariates that describe the browser-grazer continuum (proportion of grass and proportion of browse in the natural diet of a species). The results indicate that closely related species are more likely to have similar values of fibre digestibility than species that are more distant in the phylogenetic tree. Body mass did not have any significant effect on fibre digestibility. Fibre digestibility is estimated to increase with the proportion of grass and to decrease with the proportion of browse in the natural diet that characterizes the species. We applied an evolutionary model to infer rates of evolution and ancestral states of fibre digestibility; the model indicates that the rate of evolution of fibre digestibility accelerated across time. We suggest that this could be caused by a combination of increasing competition among ruminant species and adaptation to diets rich in fibre, both related to climatically driven environmental changes in the past few million years.

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 organism's 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.

Theoretical developments in the study and prediction of food intake.

The purpose of the present paper is to review recent theoretical developments in food intake modelling applied to animal science and ecology. The models are divided into those that have been developed for intensive agricultural systems, and those which consider more extensive systems and natural systems. For the most part the present paper discusses models that predict the food intake of herbivores. The mechanisms of each model are discussed, along with a brief mention of the experimental support for the most popular models. We include a discussion of models that approach the study of food intake behaviour from an evolutionary perspective, and suggest that lifetime models are especially useful when food intake carries an intrinsic cost. These long timescale evolutionary models contrast with the more common food intake models, whose timescale is usually much shorter. We conclude that the 'eating to requirements' model highlights an important food intake mechanism that provides an accurate predictive tool for intensive agricultural systems. The mechanisms of food intake regulation in extensive systems are less certain, and closer links between the ideas of animal science and ecology will be helpful for improving our understanding of food intake regulation.

Metabolic constraints on voluntary intake in ruminants.

The weak point in all current methods or models of diet formulation is the prediction of intake. The major uncertainty is not in the cases in which physical constraints apply, but in those in which voluntary intake is limited by feedback from metabolic factors. Voluntary intake is, ultimately, a psychological phenomenon, involving the integration of many signals, and reflects the flexibility of biological systems evolved to cope with variability in food supply, composition and animal state. Conditions giving rise to regulatory signals may provide a framework for modeling metabolic constraints on intake. The empirical evidence for metabolic feedback shows that the animal's productive potential, which affects its ability to utilize nutrients, interacts with the balance of absorbed nutrients to regulate intake. The relative importance of the sites where nutrient imbalance occurs (microbial or host animal metabolism) is unclear, as is the relevant time scale (minutes or days) of response. A model of the effects of asynchrony of nutrient supply to ruminal microbes suggests that ammonia and microbial recycling and the contribution of hind-gut fermentation reduce the asynchrony in the balance of nutrients absorbed into the bloodstream. Hitherto, rather little progress has been made in mathematical modeling of the metabolic processes controlling intake. Models that describe the phenomenon in terms of global variables, such as total energy intake, protein supply, and protein synthetic capacity, can simulate the way constraints may operate without requiring or providing a deeper understanding of the metabolic processes involved. Models describing the flux of energy and materials down established metabolic pathways have the potential to explore constraints on intake, but until the problem of parameterizing such models can be overcome, that potential will remain untapped.

Modeling metabolic costs of allelochemical ingestion by foraging herbivores.

A mathematical model of intermediary metabolism of allelochemicals by vertebrate herbivores is presented and used to quantify the metabolic costs of detoxification. Conjugation with glucuronic acid and maintenance of acid-base status causes catabolism of amino acid and is shown to result in loss of body protein and depletion of glucose. An interaction between allelochemical dose and nutrient status is found, and the ratio of allelochemical to nutrient absorption rate defines the tolerance of the animal to absorbable allelochemical concentration in foods. The interaction is nonlinear and the ecological implications of this for foraging behavior and diet choice are discussed.

Behavioural responses to amphetamine and apomorphine in pigs.

The effects of different doses of amphetamine (0-1.5 mg/kg) and apomorphine (0-1.0 mg/kg) on behaviour of pigs were compared. Amphetamine induced an increase in levels of nosing and rooting and of locomotion. These increases were, however, related to increased levels of standing. At higher doses (1.0-1.5 mg/kg), amphetamine specifically induced a rigid standing posture with jerking head and limb movements. Apomorphine at 0.1-1.0 mg/kg increased locomotion. In contrast to amphetamine, this effect was specific as it was not explained by increased levels of standing. At 1.0 mg/kg, apomorphine specifically induced "locomotion while the pigs maintained snout contact with the floor or trough." In addition, at this dose it induced drinking in one test, while licking in another. These differences may in part be due to differences in the test environment. Apomorphine exerted a strong conditioning effect, as indicated by the lack of behavioural variability in the postinjection period. This effect may explain the large interindividual variation in apomorphine response. Amphetamine and apomorphine elicit different behavioural syndromes in pigs, suggesting that they act on different neural systems. In addition, neither amphetamine nor apomorphine elicited behaviour that closely resembles environmentally induced stereotypies.

Relationship between amphetamine and environmentally induced stereotypies in pigs.

The study investigated the relationship between the behavioural response to a standard dose of amphetamine and environmentally induced stereotypies in pigs. There were large individual differences in the frequency of amphetamine-induced stereotypies and time spent in locomotion. In addition, these two measures tended to be negatively correlated to each other, indicating that they were competitive. Levels of amphetamine stereotypies were negatively correlated with those of chain manipulation and drinking after a period of 50 and 100 days of physical restraint and food restriction; levels of locomotion were positively correlated with levels of chain manipulation after 100 days of restraint and restrictive feeding. These results suggest that pigs differ in their predisposition to develop environmentally induced stereotypies, and that this is related to catecholaminergic systems in the brain. In an amphetamine test performed after the period of restraint and restrictive feeding, amphetamine stereotypies were generally higher than in the first test but behaviour was no longer correlated to previous levels of environmentally induced stereotypies. The qualitative differences between the two forms of stereotypy, their negative rather than positive correlation, and the lack of correlation between environment-dependent stereotypies and stereotypies in the second amphetamine test suggests a complex relationship between these two forms of stereotypies. The increased amphetamine sensitivity in the second amphetamine test may reflect the effect of stress on central catecholaminergic systems.

Modelling the nutritional ecology of ungulate herbivores: evolution of body size and competitive interactions.

A simulation model is used to quantify relationships between diet quality, digestive processes and body weight in ungulate herbivores. Retention time of food in the digestive tract is shown by regression to scale with W0.27, and to be longer in ruminants than in hindgut fermenters. Allometric relationships between whole gut mean retention time (MRT, h) and weight (W) were: MRT=9.4 W0.255 (r 2=0.80) for hindgut fermenters and MRT=15.3 W0.251 (r 2=0.76) in ruminants. Longer retention of ingesta by large-bodied ruminants and hindgut fermenters increases digestive efficiency relative to small animals and permits them to survive on lower-quality foods. Compared with ruminants, hindgut fermenters' faster throughput is an advantage which outweighs their lower digestive efficiency, particularly on poor quality foods, provided that food resources are not limiting. This suggests that the predominance of ruminants in the middle range of body weights results from their more efficient use of scarce resources under conditions of resource depletion. Considering only physical limitations on intake, the model shows that the allometric coefficient which scales energy intake to body mass is 0.88 in ruminants and 0.82 in hindgut fermenters. The advantages of large body size are countered by disadvantages where food quantity is limited, and we suggest that the upper limit to ungulate body size is determined by the ability to extract nutrients from feeding niches during the nadir of the seasonal cycle of resource quality and abundance.

Relationship between agonistic behaviour and propensity to develop excessive drinking and chain manipulation in pigs.

Consistent individual differences in animals' responses to different stressful situations may indicate the involvement of a single behavioural and neurological mechanism across these situations. Two replicate groups of sixteen food restricted pigs were subjected to a group feeding competition test where group members were required to compete over a food source. All agonistic interactions were scored and ranked dominance scores were calculated. The pigs were subsequently put into two different forms of restrictive housing (restraint or loose), with half of the pigs food restricted. No housing effects were found. Only food restricted pigs developed excessive drinking and chain manipulation, but large individual differences existed. Pigs ranked high in dominance score were found to significantly increase their drinking levels over the experimental period of three months, having significantly higher drinking levels than low ranking pigs in the second and third month. No significant relationship was found between ranked dominance score and levels of chain manipulation. The present results suggest that in pigs differences in the propensity to develop forms of excessive drinking under restrictive housing and feeding conditions are related to agonistic tendencies in a group feeding competition test. These data also suggest that excessive drinking and chain manipulation are at least in part based on different behavioural and presumably neural mechanisms.

Resource partitioning by ungulates on the Isle of Rhum.

This paper describes the seasonal changes in vegetation community use by red deer, cattle, goats and ponies on the Isle of Rhum, Scotland. During the winter, when food resources were of low abundance and digestibility, the ungulates showed extensive resource partitioning. During the summer, when resource availability and digestibility was high, the grazing species, red deer, cattle and ponies congregated on the vegetation communities which contained high biomasses of a high quality resource, mesotrophic graminoids and forbs. Goats, with a digestive system adapted to dealing with browse, foraged primarily on the communities dominated by dwarf shrubs. The patterns of resource use in this group of ungulates are discussed in relation to competition; species had relatively exclusive esource use during periods of low food availability during tye winter and had a high degree of resource use overlap when food was abundant during the summer. This suggests that there was little competition for food during the summer and that exploitative competition for the high quality foods led to resource partitioning during the winter. Senarios are described which predict the pattern of resource use between two species (one competitively superior to the other on the preferred resource) utilizing mutually or exclusively preferred resources. A model developed by Illius and Gordon (1987), based on the allometry of metabolic requirements and bite size, is used to provide a mechanistic explanation for the observation that the red deer were able to exploit the high quality plant communities during the winter, whereas the cattle moved off to feed on poorer quality communities at this time.

Evaluation of LH-RH stimulation of testosterone as an index of reproductive status in rams and its application in wild antelope.

In rams a positive correlation (P less than 0.001) existed between average testosterone levels from 30-min blood sampling for 18 h and average testosterone levels of samples taken 0, 1 and 2 h after injection of LH-RH administered 90 min after anaesthesia. Attempts were therefore made to assess testosterone status by LH-RH challenge and limited blood sampling in animals immobilized in their natural habitat. In impala (Aepyceros melampus) territorial males had higher plasma testosterone values than did bachelors after LH-RH challenge (8.1 compared with 2.6 ng/ml, P less than 0.05). In blesbok (Damaliscus dorcas), the relationship was less clear, but testicular volume was correlated with plasma testosterone concentration and with testicular responsiveness measured by testosterone produced per unit of LH (P less than 0.001 and P less than 0.05, respectively). The LH-RH challenge technique therefore has value as a measure of testicular function and permits study of ungulates in their natural environment.

Plasma concentrations of testosterone in the developing ram in different social environments.

Plasma testosterone profiles were determined by taking frequent blood samples at intervals from birth to 21 months of age from rams reared in isolation, in an all-male group and in a mixed-sex group. The testosterone pattern was not modified by these different social environments. The ability of the ram to copulate when first exposed to an oestrous ewe, apparently a maturational process, was also independent of social rearing. At birth plasma testosterone levels were detectable but low, they were higher at 10 and 16 weeks of age and showed a marked rise by 26 weeks, coincident with the time of puberty. Depressive effects of season on testosterone profiles occurred during the 2nd year of life but not the 1st year.

Effects of ewe proximity on peripheral plasma testosterone levels and behaviour in the ram.

Groups of yearling and immature rams were kept for 6 months during the breeding season either adjacent to or apart from ovariectomized ewes in which oestrus was induced by hormone therapy. The older rams kept near ewes were found to have larger testes, higher plasma testosterone levels and greater sexual and aggressive activity, although the immature animals showed no response. Plasma testosterone concentration was also found to increase after copulation in some animals.