Metabolic depression in animals: physiological perspectives and biochemical generalizations

Depression of metabolic rate has been recorded for virtually all major animal phyla in response to environmental stress. The extent of depression is usually measured as the ratio of the depressed metabolic rate to the normal resting metabolic rate. Metabolic rate is sometimes only depressed to approx. 80% of the resting value (i.e. a depression of approx. 20% of resting); it is more commonly 5-40 % of resting (i.e. a depression of approx. 60-95% of resting); extreme depression is to 1% or less of resting, or even to an unmeasurably low metabolic rate (i.e. a depression of approx. 99-100% of resting). We have examined the resting and depressed metabolic rate of animals as a function of their body mass, corrected to a common temperature. This allometric approach allows ready comparison of the absolute level of both resting and depressed metabolic rate for various animals, and suggests three general patterns of metabolic depression. Firstly, metabolic depression to approx. 0.05-0.4 of rest is a common and remarkably consistent pattern for various non-cryptobiotic animals (e.g. molluscs, earthworms, crustaceans, fishes, amphibians, reptiles). This extent of metabolic depression is typical for dormant animals with ‘intrinsic’ depression, i.e. reduction of metabolic rate in anticipation of adverse environmental conditions but without substantial changes to their ionic or osmotic status, or state of body water. Some of these types of animal are able to survive anoxia for limited periods, and their anaerobic metabolic depression is also to approx. 0.05-0.4 of resting. Metabolic depression to much less than 0.2 of resting is apparent for some ‘resting’, ‘over-wintering’ or diapaused eggs of these animals, but this can be due to early developmental arrest so that the egg has a low ‘metabolic mass’ of developed tissue (compared to the overall mass of the egg) with no metabolic depression, rather than having metabolic depression of the entire cell mass. A profound decrease in metabolic rate occurs in hibernating (or aestivating) mammals and birds during torpor, e.g. to less than 0.01 of pre-torpor metabolic rate, but there is often no intrinsic metabolic depression in addition to that reduction in metabolic rate due to readjustment of thermoregulatory control and a decrease in body temperature with a concommitant Q₁₀ effect. There may be a modest intrinsic metabolic depression for some species in shallow torpor (to approx. 0.86) and a more substantial metabolic depression for deep torpor (approx. 0.6), but any energy saving accruing from this intrinsic depression is small compared to the substantial savings accrued from the readjustment of thermoregulation and the Q₁₀ effect. Secondly, a more extreme pattern of metabolic depression (to < 0.05 of rest) is evident for cryptobiotic animals. For these animals there is a profound change in their internal environment-for anoxybiotic animals there is an absence of oxygen and for osmobiotic, anhydrobiotic or cryobiotic animals there is an alteration of the ionic/osmotic balance or state of body water. Some normally aerobic animals can tolerate anoxia for considerable periods, and their duration of tolerance is inversely related to their magnitude of metabolic depression; anaerobic metabolic rate can be less than 0.005 of resting. The metabolic rate of anhydrobiotic animals is often so low as to be unmeasurable, if not zero. Thus, anhydrobiosis is the ultimate strategy for eggs or other stages of the life cycle to survive extended periods of environmental stress. Thirdly, a pattern of absence of metabolism when normally hydrated (as opposed to anhydrobiotic or cryobiotic) is apparently unique to diapaused eggs of the brine-shrimp (Artemia spp., an anostracan crustacean) during anoxia. The apparent complete metabolic depression of anoxic yet hydrated cysts (and extreme metabolic depression of normoxic, hypoxic, or osmobiotic, yet hydrated cysts), is an obvious exception to the above patterns. In searching for biochemical mechanisms for metabolic depression, it is clear that there are five general characteristics at the molecular level of cells which have a depressed metabolism; a decrease in pH, the presence of latent mRNA, a change in protein phosphorylation state, the maintenance of one particular energy-utilizing process (ion pumping), and the down-regulation of another (protein synthesis). Oxygen sensing is now the focus of intense investigation and obviously plays an important role in many aspects of cell biology. Recent studies show that oxygen sensing is involved in metabolic depression and research is now being directed towards characterising the proteins and mechanisms that comprise this response. As more data accumulate, oxygen sensing as a mechanism will probably become the sixth general characteristic of depressed cells. The majority of studies on these general characteristics of metabolically depressed cells come from members of the most common group of animals that depress metabolism, those non-cryptobiotic animals that remain hydrated and depress to 0.05-0.4 of rest. These biochemical investigations are becoming more molecular and sophisticated, and directed towards defined processes, but as yet no complete mechanism has been delineated. The consistency of the molecular data within this group of animals suggests similar metabolic strategies and mechanisms associated with metabolic depression. The biochemical ‘adaptations’ of anhydrobiotic organisms would seem to be related more to surviving the dramatic reduction in cell water content and its physico-chemical state, than to molecular mechanisms for lowering metabolic rate. Metabolic depression would seem to be an almost inevitable consequence of their altered hydration state. The unique case of profound metabolic depression of hydrated Artemia spp. cysts under a variety of conditions could reflect unique mechanisms at the molecular level. However, the available data are not consistent with this possibility (with the exception of a uniquely large decrease in ATP concentration of depressed, hydrated Artemia spp. cysts) and the question remains: how do cells of anoxic and hydrated Artemia spp. differ from anoxic goldfish or turtle cells, enabling them so much more completely to depress their metabolism?     

Nonparallel transport and mechanisms of secretion.

After many years of controversy, it is now clear that at least some cells and tissues that secrete more than one product can vary the composition of the secreted mixture as the result of the differential transport of various substances out of the cells that secrete them. In this article we discuss this phenomenon, non-parallel transport or secretion, and how it has and continues to inform us about how cells release the products they manufacture. We focus on expression of the phenomenon in the secretion of digestive enzymes by the exocrine pancreas, where it has been studied most extensively.     

The combined role of the main olfactory and vomeronasal systems in social communication in mammals

The main olfactory and the vomeronasal systems are the two systems by which most vertebrates detect chemosensory cues that mediate social behavior. Much research has focused on how one system or the other is critical for particular behaviors. This has lead to a vision of two distinct and complexly autonomous olfactory systems. A closer look at research over the past 30 years reveals a different picture however. These two seemingly distinct systems are much more integrated than previously thought. One novel set of chemosensory cues in particular (MHC Class I peptide ligands) can show us how both systems are capable of detecting the same chemosensory cues, through different mechanisms yet provide the same general information (genetic individuality). Future research will need to now focus on how two seemingly distinct chemosensory systems together detect pheromones and mediate social behaviors. Do these systems work independently, synergistically or competitively in communicating between individuals of the same species?     

In vivo downregulation of protein synthesis in the snail Helix apersa during estivation

Protein synthesis is downregulated during metabolic depression in a number of systems where the metabolic depression is effected by obvious extrinsic cues. The metabolic depression of the estivating land snail Helix apersa occurs in the absence of any obvious physiological stress and has an intrinsic component independent of temperature, pH, O(2) status, or osmolality. We show that this metabolic depression is accompanied by a downregulation of protein synthesis in vivo. The rate of protein synthesis decreases in two major tissues during estivation: to 23% and 53% of the awake rate in hepatopancreas and foot muscle, respectively. We show from calculations of the theoretical contribution of protein synthesis to total O(2) consumption that the depression of protein synthesis must be a significant, obligate, in vivo component of metabolic depression in H. aspersa.     

Mechanisms of muscle dedifferentiation during regeneration

For many years people have known that amphibians have an amazing ability to regenerate lost body parts. In contrast humans have limited regeneration capacity and even simple wound healing results in scarring. Despite more than a century of scientific inquiry, this remarkable phenomenon remains poorly understood. Recent research has begun to provide insight into how this unique process that is now fully accepted to occur via the reversal of cell differentiation is executed at the molecular level. As more and more is known about regeneration and dedifferentiation we can begin to address the question: if given the right signals could mammals also regenerate body structures?     

Infrared thermal imaging associated with pain in laboratory animals

The science of animal welfare has evolved over the years, and recent scientific advances have enhanced our comprehension of the neurological, physiological, and ethological mechanisms of diverse animal species. Currently, the study of the affective states (emotions) of nonhuman animals is attracting great scientific interest focused primarily on negative experiences such as pain, fear, and suffering, which animals experience in different stages of their lives or during scientific research. Studies underway today seek to establish methods of evaluation that can accurately measure pain and then develop effective treatments for it, because the techniques available up to now are not sufficiently precise. One innovative technology that has recently been incorporated into veterinary medicine for the specific purpose of studying pain in animals is called infrared thermography (IRT), a technique that works by detecting and measuring levels of thermal radiation at different points on the body’s surface with high sensitivity. Changes in IRT images are associated mainly with blood perfusion, which is modulated by the mechanisms of vasodilatation and vasoconstriction. IRT is an efficient, noninvasive method for evaluating and controlling pain, two critical aspects of animal welfare in biomedical research. The aim of the present review is to compile and analyze studies of infrared thermographic changes associated with pain in laboratory research involving animals.     

Developmental control of imprinted expression by macro non-coding RNAs

Genomic imprinting is a developmentally regulated epigenetic phenomenon. The majority of imprinted genes only show parent-of-origin specific expression in a subset of tissues or at defined developmental stages. In some cases, imprinted expression is controlled by an imprinted macro non-coding RNA (ncRNA) whose expression pattern and repressive activity does not necessarily correlate with that of the genes whose imprinted expression it controls. This suggests that developmentally regulated factors other than the macro ncRNA are involved in establishing or maintaining imprinted expression. Here, we review how macro ncRNAs control imprinted expression during development and differentiation and consider how this impacts on target choice in epigenetic therapy.     

The combined role of the main olfactory and vomeronasal systems in social communication in mammals

The main olfactory and the vomeronasal systems are the two systems by which most vertebrates detect chemosensory cues that mediate social behavior. Much research has focused on how one system or the other is critical for particular behaviors. This has lead to a vision of two distinct and complexly autonomous olfactory systems. A closer look at research over the past 30 years reveals a different picture however. These two seemingly distinct systems are much more integrated than previously thought. One novel set of chemosensory cues in particular (MHC Class I peptide ligands) can show us how both systems are capable of detecting the same chemosensory cues, through different mechanisms yet provide the same general information (genetic individuality). Future research will need to now focus on how two seemingly distinct chemosensory systems together detect pheromones and mediate social behaviors. Do these systems work independently, synergistically or competitively in communicating between individuals of the same species?     

Aerobic capacity of frog skeletal muscle during hibernation

Frogs submerged at 3 degrees C in hypoxic water (Po2=60 mmHg) depress their metabolic rate to 25% of that seen in control animals with access to air. The hypometabolic state of the skeletal muscle in such cold-submerged frogs is thought to be the most important contributor to the overall metabolic depression. The aim of this study was to determine whether the aerobic capacity of frog skeletal muscle became altered during 1-4 mo of hibernation to match the reduction in adenosine triphosphate (ATP) demand. To this end, the activities of key mitochondrial enzymes were measured in the skeletal muscle and in isolated mitochondria of frogs at different stages during hibernation. We also measured the activity of lactate dehydrogenase (LDH) as an indicator of glycolytic capacity. The activities of cytochrome c oxidase, citrate synthase, and LDH were significantly lower in frog skeletal muscle after 4 mo of hibernation compared with control conditions. The reduction in skeletal muscle aerobic capacity is apparently due to changes in the intrinsic properties of the mitochondria. Overall, these results indicate an important reorganisation of ATP-producing pathways during long-term metabolic depression to match the lowered ATP demand.     

Observations on the mass migration of Bridled Terns Sterna anaethetus off the coast of Colombo

A mass mieration of Bridled Terns Sterna anaethetus has been observed periodically off the south western coast of Sri Lanka during the past several years (Hoffmann 1975, Phillips 1978) and it is now evident that the phenomenon is an annual occurrence A preliminary study was initiated in 1981 (De silva 1982) and the results encouraged the continuation of observations until late October 1984 Only those aspects of migration which were visible from land are dealt with here     

Effect of tick control on liveweight gain of cattle in central Zambia

Field trials were carried out during 1982-86 in two different ecotypes in central Zambia to determine the impact of tick control on the liveweight gain (LWG) of cattle. During the first 2 years of the trial a diamidide acaricide (Amitraz) sprayed at weekly intervals caused periodic depression in LWG in young animals. Thereafter a pyrethroid acaricide (cypermethrin) was used. During the 1984-85 tick season infestations of 50-120 adult Amblyomma variegatum Fabricius in untreated animals caused significant reductions in LWG. From the differences in LWG between treated and untreated cattle, the induced loss in LWG was estimated at 46-61 g per engorged female A.variegatum.     

The application of transgenic techniques for the improvement of domestic animal productivity

The application of transgenesis techniques to domestic animals has now been achieved in all the major species of domestic animals. In this review, the progress towards genuine practical applications of the technique is examined. Areas which appear to have made progress during the past several years include the evaluation of animals with elevated growth hormone levels, the introduction of novel metabolic pathways, the expression of transgenes in the mammary glands of pigs and sheep, and the real possibility that functional immunoglobulin genes might be used to confer genetically-inherited disease resistance to commercially-valuable animal breeds.     

Risk Sensitivity in Behavior: Where Are We Now? Introduction to the Symposium

Risk-sensitive behavior is the phenomenon of animals exhibitingpreferences when offered choices whose outcomes differ in theirdegree of variance. It is now well demonstrated that many animalsare sensitive to differences in the magnitude of variance inrewards. A considerable body of literature on risk sensitivityhas been generated in recent years, encompassing theoreticaland empirical work, from both functional and mechanistic approaches.Nevertheless, it is less than clear how animal preferences forvariability are determined. It is therefore timely to look broadlyat what has been accomplished, and to identify the most promisingsynthetic approaches for future work.     

Thyroid hormone and growth: relationships with growth hormone effects and regulation

For some years, research in the field of growth endocrinology has been mainly focused on growth hormone (GH). However, it appears that GH does not always control growth rate. For instance, it does not clearly influence intra-uterine growth: moreover, although the results of GRF or GH administration appear convincing in rats, pigs or heifers, this is not the case in chickens and lambs. In addition, GH does not always clearly stimulate somatomedin production, particularly diring food restriction and fetal life, and in hypothyroid animals or sex-linked dwarf chickens. In such situations, this phenomenon is associated with a reduced T3 production, suggesting a significant influence of thyroid function on GH action, and more generally, on body growth. In fact, numerous data demonstrate that thyroid hormone is strongly involved in the regulation of body growth. In species with low maturity at birth, such as the rat. T4 and T3 affect postnatal growth eleven days earlier than the appearance of GH influence. In contrast to GH, thyroid hormone significantly influences fetal growth in sheep. Moreover, the body growth rate is clearly stimulated by T3 in dwarf animals. In addition to its complex metabolic effects involved in the general mechanisms of body growth, thyroid hormone stimulates the production of growth factors, particularly EGF and NGF. Moreover, it affects GH and somatomedin production and also their tissue activity. All these results strongly suggest that it would be difficult to study GH regulation and physiological effects without taking thyroid function into account.     

A History of Animal Welfare Science

Human attitudes to animals have changed as non-humans have become more widely incorporated in the category of moral agents who deserve some respect. Parallels between the functioning of humans and non-humans have been made for thousands of years but the idea that the animals that we keep can suffer has spread recently. An improved understanding of motivation, cognition and the complexity of social behaviour in animals has led in the last 30 years to the rapid development of animal welfare science. Early attempts to define welfare referred to individuals being in harmony with nature but the first usable definition incorporated feelings and health as part of attempts to cope with the environment. Others considered that welfare is only about feelings but it is argued that as feelings are mechanisms that have evolved they are a part of welfare rather than all of it. Most reviews of welfare now start with listing the needs of the animal, including needs to show certain behaviours. This approach has used sophisticated studies of what is important to animals and has replaced the earlier general guidelines described as freedoms. Many measures of welfare are now used and indicate how good or how poor the welfare is. Naturalness is not a part of the definition of welfare but explains why some needs exist. In recent years, welfare has become established as one of various criteria used to decide on whether a system is sustainable because members of the public will not accept systems that cause poor welfare. The study of welfare has become part of the scientific basis upon which important political decisions are made.     

Feedback loops between 3D vegetation structure and ecological functions of animals

Ecosystems function in a series of feedback loops that can change or maintain vegetation structure. Vegetation structure influences the ecological niche space available to animals, shaping many aspects of behaviour and reproduction. In turn, animals perform ecological functions that shape vegetation structure. However, most studies concerning three-dimensional vegetation structure and animal ecology consider only a single direction of this relationship. Here, we review these separate lines of research and integrate them into a unified concept that describes a feedback mechanism. We also show how remote sensing and animal tracking technologies are now available at the global scale to describe feedback loops and their consequences for ecosystem functioning. An improved understanding of how animals interact with vegetation structure in feedback loops is needed to conserve ecosystems that face major disruptions in response to climate and land-use change.     

The perception of students on the use of animals in higher education at the Federal University of Paraná, Southern Brazil

The use of animals in education and research is a controversial issue that involves ethical considerations. In Brazil, Act 11,794, which was approved in 2008, established the National Council on the Control of Animal Experimentation (CONCEA) and a database of institutions that use animals for research and education (CIUCA). This legislation also set out the regulations for the use of animals. In this study, we have evaluated the ethical issues involved in the use of animals for educational purposes at the Federal University of Paraná, through a qualitative-quantitative analysis that relied on written questionnaires. Our objective was to find out the opinions of students and staff from different academic fields, and at different stages in their professional development, on the use of animals for educational purposes. The study involved 101 students and 20 lecturers (i.e. tenure-track professors and all those who teach the students) in Biology, Pharmacology, Medicine and Veterinary Medicine. Approximately half of the students (45.5%) did not know the legislation that regulates the use of animals in education, and most of the lecturers believed that learning goals could not be achieved with alternative methods. Only 38.9% of the lecturers and 31.9% of the students trusted the usefulness of alternative methods. Furthermore, recent graduates were as unaware of the legislation, as were students in the first two years of their university courses. These results suggest that it is necessary to considerably expand the discussion on alternatives to animal use in the academic environment.     

Plant evolution and development in a post-genomic context

Large-scale gene-sequencing projects that have been undertaken in animals have involved organisms from contrasting taxonomic groups, such as worm, fly and mammal. By contrast, similar botanical projects have focused exclusively on flowering plants. This has made it difficult to carry out fundamental research on how plants have evolved from simple to complex forms - a task that has been very successful in animals. However, in the flowering plants, the many completely or partially sequenced genomes now becoming available will provide a powerful tool to investigate the details of evolution in one group of related organisms.     

The international movement of livestock

The purpose of this paper is to provide an overview of the international movement of livestock. The reasons for international movements of livestock are discussed. The factors involved in the international transfer of livestock and genetic material are presented. Statistics of animals, semen, and embryos exported from the United States for fiscal years 1981 and 1982 are presented. The principal countries involved in importing U.S. livestock are listed.     

Inbreeding avoidance in animals

The phenomenon of inbreeding depression is well documented and behavioral adaptations for inbreeding avoidance have been described. However, there is debate over whether inbreeding depression is always an important selective force on behavior. Here, we summarize recent evidence for inbreeding depression under natural conditions, review inbreeding avoidance mechanisms, and discuss how these are influenced by social structure. We also examine the idea that animals have evolved mechanisms to avoid outbreeding.