A review of cetacean lung morphology and mechanics

Cetaceans possess diverse adaptations in respiratory structure and mechanics that are highly specialized for an array of surfacing and diving behaviors. Some of these adaptations and air management strategies are still not completely understood despite over a century of study. We have compiled the historical and contemporary knowledge of cetacean lung anatomy and mechanics in regards to normal lung function during ventilation and air management while diving. New techniques are emerging utilizing pulmonary mechanics to measure lung function in live cetaceans. Given the diversity of respiratory adaptations in cetaceans, interpretations of these results should consider species‐specific anatomy, mechanics, and behavior. J. Morphol. 274:1425–1440, 2013. © 2013 Wiley Periodicals, Inc.     

Respiratory adaptations to running-water microhabitats in mayfly larvae Epeorus sylvicola and Ecdyonurus torrentis, Ephemeroptera

The mayfly larvae Epeorus sylvicola and Ecdyonurus torrentis inhabit either fast-flowing or, for the latter species, calm zones of running water. We studied (1) mechanisms and limitations of oxygen transport in single individuals (oxygen consumption rate, occurrence and rate of gill movements, and heartbeats) in running water of different oxygen concentrations and (2) capacities for anaerobiosis (L-lactate production). Our aim was to look for specific adaptations in the two species to slightly different microhabitats. Epeorus sylvicola, whose immovable gills are not able to generate ventilatory convection, proved to be an oxyconformer at both test temperatures (11 degrees and 15 degrees C). Ecdyonurus torrentis showed a progressively stronger oxyregulatory behavior at higher temperatures. In this species an onset of gill beating was found at moderate hypoxia (below 16 kPa). Ventilating individuals reached maximum rates (300 min-1) of 5-14 kPa. In the case of a further reduction of oxygen partial pressure, the ventilatory rate started to decrease. Ventilatory activity, however, was maintained down to very low oxygen concentrations. Neither in E. sylvicola nor in E. torrentis was experimental evidence found to confirm the hypothesis of a respiratory function of hindgut movements. During hypoxia, the heart rate was constant in both species (E. sylvicola: 80 min-1; E. torrentis: 60 min-1): bradycardia occurred either below 1.5 kPa or below 4 kPa. Anaerobiosis, that is, lactate production, was not detected in either species.     

Using Isolated Mitochondria from Minimal Quantities of Mouse Skeletal Muscle for High throughput Microplate Respiratory Measurements

Skeletal muscle mitochondria play a specific role in many disease pathologies. As such, the measurement of oxygen consumption as an indicator of mitochondrial function in this tissue has become more prevalent. Although many technologies and assays exist that measure mitochondrial respiratory pathways in a variety of cells, tissue and species, there is currently a void in the literature in regards to the compilation of these assays using isolated mitochondria from mouse skeletal muscle for use in microplate based technologies. Importantly, the use of microplate based respirometric assays is growing among mitochondrial biologists as it allows for high throughput measurements using minimal quantities of isolated mitochondria. Therefore, a collection of microplate based respirometric assays were developed that are able to assess mechanistic changes/adaptations in oxygen consumption in a commonly used animal model. The methods presented herein provide step-by-step instructions to perform these assays with an optimal amount of mitochondrial protein and reagents, and high precision as evidenced by the minimal variance across the dynamic range of each assay.     

‘Cool’ adaptations to cold environments: globins in Notothenioidei (Actynopterygii,Perciformes)

Notothenioidei, the taxonomic group of teleosts that dominates the Southern Ocean and dwell in the Ross Sea at large, provide an example of marine species that underwent unique adaptations to life at low temperatures and high oxygen concentrations, resulting in morphological, physiological, genomic, and biochemical peculiarities in comparison with warm-water fish. Global Warming raises concerns over the fate of these stenothermal fish, as their adaptation has been accompanied by irreversible genomic losses, which suggest a poor genetic potential to adapt to warmer climates. Specifically, this review focuses on adaptation of proteins belonging to the globin superfamily, which include the respiratory proteins hemoglobin and myoglobin and the non-respiratory proteins neuroglobin and cytoglobin. Here, we describe their molecular adaptations to cold temperatures in the framework of the physiology of oxygen transport and management of oxidative stress in fish species largely populating the Ross Sea.     

Adaptations of fish species to oxygen depletion in a central Amazonian floodplain lake

Pronounced seasonal and daily oxygen concentration changes are characteristic for Amazonian floodplain lakes. Studies on the fish fauna of the Lago Camaleão, Solimões River, Amazonas, Brazil, showed several fish species which are able to survive prolonged periods of heavy hypoxia. Twenty species belonging to eight families were observed in the laboratory in order to determine their respiratory adaptations to hypoxic conditions and oxygen concentrations at which the fish present respiratory adaptations. Finally, the fish species were distributed throughout the habitats of Lake Camaleão according to their adaptation responses. Ten fish species used the surface water for aquatic surface respiration, four species used atmospheric oxygen for aerial respiration, four species used oxygen supplied by the exudation of the roots of floating macrophytes and two exhibited a high tolerance to hypoxic conditions, and well-developed physiological biochemical mechanisms. The fish fauna is well adapted to low oxygen concentrations. The large variety of morpho-anatomical adaptations associated with biochemical and physiological mechanisms to tolerate hypoxic and anoxic conditions enable the 20 fish species to exploit several habitats of Lago Camaleão, such as floating aquatic macrophyte meadows, open water and near the shoreline.     

Free radicals generated by contracting muscle: by-products of metabolism or key regulators of muscle function?

Skeletal muscle fibers generate reactive oxygen species (ROS) at a number of subcellular sites and this generation is increased by contractile activity. Early studies suggested that generation of superoxide as a by-product of mitochondrial oxygen consumption was the major source of muscle ROS generation and that the species produced were inevitably damaging to muscle, but recent data argue against both of these possibilities. Developments in analytical approaches have shown that specific ROS are generated in a controlled manner by skeletal muscle fibers in response to physiological stimuli and play important roles in the physiological adaptations of muscle to contractions. These include optimization of contractile performance and initiation of key adaptive changes in gene expression to the stresses of contractions. These positive benefits of the ROS that are induced by contractile activity contrast starkly with the increasing evidence that ROS-induced degenerative pathways are fundamental to aging processes in skeletal muscle. A fuller understanding of these contrasting roles is recognized to be important in the design of strategies to maintain and optimize skeletal muscle function during exercise and to help prevent the devastating effects of sarcopenia and other muscle-wasting conditions.     

Is Aquatic Life Correlated with an Increased Hematocrit in Snakes?

Background

Physiological adaptations that allow air-breathing vertebrates to remain underwater for long periods mainly involve modifications of the respiratory system, essentially through increased oxygen reserves. Physiological constraints on dive duration tend to be less critical for ectotherms than for endotherms because the former have lower mass-specific metabolic rates. Moreover, comparative studies between marine and terrestrial ectotherms have yet to show overall distinct physiological differences specifically associated with oxygen reserves.

Methodology/Principal Findings

We used phylogenetically informed statistical models to test if habitat affects hematocrit (an indicator of blood oxygen stores) in snakes, a lineage that varies widely in habitat use. Our results indicate that both phylogenetic position (clade) and especially habitat are significant predictors of hematocrit. Our analysis also confirms the peculiar respiratory physiology of the marine Acrochordus granulatus.

Conclusion/Significance

Contrary to previous findings, marine snakes have significantly–albeit slightly–elevated hematocrit, which should facilitate increased aerobic dive times. Longer dives could have consequences for foraging, mate searching, and predation risks. Alternatively, but not exclusively, increased Hct in marine species might also help to fuel other oxygen-demanding physiological adaptations, such as those involved in osmoregulation.     

Biochemical and physiological adaptations in the estuarine crab Neohelice granulata during salinity acclimation

Neohelice granulata (Chasmagnathus granulatus) is an intertidal crab species living in salt marshes from estuaries and lagoons along the Atlantic coast of South America. It is a key species in these environments because it is responsible for energy transfer from producers to consumers. In order to deal with the extremely marked environmental salinity changes occurring in salt marshes, N. granulata shows important and interesting structural, biochemical, and physiological adaptations at the gills level. These adaptations characterize this crab as a euryhaline species, tolerating environmental salinities ranging from very diluted media to concentrated seawater. These characteristics had led to its use as an animal model to study estuarine adaptations in crustaceans. Therefore, the present review focuses on the influence of environmental salinity on N. granulata responses at the ecological, organismic and molecular levels. Aspects covered include salinity tolerance, osmo- and ionoregulatory patterns, morphological and structural adaptations at the gills, and mechanisms of ion transport and their regulation at the gills level during environmental salinity acclimation. Finally, this review compiles information on the effects of some environmental pollutants on iono- and osmoregulatory adaptations showed by N. granulata.     

The respiratory complementarity of spider book lung and tracheal systems

Like most spiders, members of the orb-weaving family Uloboridae have a dual respiratory system. Book lungs oxygenate the hemolymph and tracheae carry oxygen directly to tissues. Most members of the family are characterized by an extensive tracheal system that extends into the prosoma, where branches enter the legs. A comparison of both absolute and size-specific indices of these two respiratory components in six uloborid species using the independent contrast method shows that their development is inversely related and indicates that these two systems are complementary. Species that more actively monitor reduced webs have tracheae with greater cross sectional areas and book lungs with smaller areas than do orb-weaving species that less aggressively manipulate their webs. Thus, the acuteness of a spider's oxygen demands appears to influence the development of its respiratory components. As the tracheae assume more responsibility for providing oxygen the book lungs become less well developed and vice versa. J. Morphol. 236:57–64, 1998. © 1998 Wiley-Liss, Inc.     

Composition en acides aminés des hémocyanines et adaptation respiratoire chez les écrevisses

Analysis of the amino acid composition of the hemocyanins from six species of the Astacidae, belonging to the Astacinae and the Cambarinae, shows that these respiratory pigments present a great deal of homology. This slight differentiation does not allow us to reconstruct the scheme of classification of the Astacidae into two sub-families. Comparison with the hemocyanins of two terrestrial Isopods and two marine Decapods leads to a dendrogram in which two groups of species are distinguished. The former comprises the freshwater crayfishes and the Isopods, the latter includes the marine Decapods. Such a separation can be explained by the importance of the mode of life and the development of respiratory adaptations for air-breathing, independently of the taxonomic position of the studied species.     

Environmental influences on the development of the cardiac system in fish and amphibians

In poikilothermic animals body temperature varies with environmental temperature, and this results in a change in metabolic activity (Q10 of enzymatic reactions typically is around 2-3). Temperature changes also modify gas transport in body fluids. While the diffusion coefficient increases with increasing temperatures, physical solubility and also hemoglobin oxygen affinity decrease. Therefore, an increase in temperature typically requires adjustments in cardiac activity because ventilatory and convectional transport of respiratory gases usually are tightly coupled in adults in order to meet the oxygen demand of body tissues. Hypoxic conditions also provoke adaptations in the central circulatory system, like the hypoxic bradycardia, which has been described for many adult lower vertebrates, combined with an increase in stroke volume and peripheral resistance. In embryos and larvae the situation is much more complicated, because nervous control of the heart is established only late during development, and because the site of gas exchange changes from mainly cutaneous gas exchange during early development to mainly pulmonary or branchial gas exchange in late stages. In addition, recent studies in amphibian and fish embryos and larvae reveal, that at least in very early stages convectional gas transport of the hemoglobin is not essential, which means that in these early stages ventilatory and convectional gas transport are not yet coupled. Accordingly, in early stages of fish and amphibians the central cardiac system often does not respond to hypoxia, although in some species behavioral adaptations indicate that oxygen sensors are functional. If a depression of cardiac activity is observed, it most likely is a direct effect of oxygen deficiency on the cardiac myocytes. Regulated cardiovascular responses to hypoxia appear only in late stages and are similar to those found in adult species.     

Ceruloplasmin decreases respiratory burst reaction during pregnancy

Testing of pregnant women reveals weakening of neutrophil-mediated effector functions, such as reactive oxygen species generation. This study provides data confirming the phenomenon, gained through application of the flow cytometry technique. Key factors influencing neutrophil functional activity in blood plasma of pregnant women have not been detected so far. At the same time, concentration of ceruloplasmin – a copper-containing glycoprotein – is known to increase in blood significantly during pregnancy. We observed the negative correlation between ceruloplasmin concentration in blood plasma of pregnant women and the intensity of respiratory burst of neutrophils. Fractionation of plasma using gel-filtration revealed that ceruloplasmin-containing fraction demonstrated suppression of the respiratory burst reaction. Partial elimination of ceruloplasmin from the blood of pregnant women, performed with the help of specific antibodies and followed by immunoprecipitation, leads to an increased respiratory burst reaction. On the contrary, addition of ceruloplasmin to blood samples of healthy donors noticeably decreases the respiratory burst reaction. The results presented prove that change in ceruloplasmin level in plasma is necessary and sufficient for modulating the ability of neutrophils to produce reactive oxygen species during pregnancy.     

Does size matter for hypoxia tolerance in fish?

Fish cover a large size range, from milligrams to tonnes, and many of them are regularly exposed to large variations in ambient oxygen levels. For more than half a century, there have been various, often divergent, claims regarding the effect of body size on hypoxia tolerance in fish. Here, we attempt to link old and new empirical data with the current understanding of the physiological mechanisms behind hypoxia tolerance. Three main conclusions are drawn: (1) body size per se has little or no impact on the ability to take up oxygen during hypoxic conditions, primarily because the respiratory surface area matches metabolic rate over a wide size range. If size-related differences are seen in the ability for oxygen uptake in a species, these are likely to reflect adaptation to different life-styles or habitat choice. (2) During severe hypoxia and anoxia, where fish have to rely on anaerobic ATP production (glycolysis) for survival, large individuals have a clear advantage over smaller ones, because small fish will run out of glycogen or reach lethal levels of anaerobic end-products (lactate and H(+)) much faster due to their higher mass-specific metabolic rate. (3) Those fish species that have evolved extreme adaptations to hypoxia, including haemoglobins with exceptionally high oxygen affinities and an alternative anaerobic end-product (ethanol), reveal that natural selection can be a much more powerful determinant of hypoxia tolerance than scaling of physiological functions.     

Reproductive strategies and energetic adaptations of polar zooplankton

Summary

Key factors governing polar ocean ecosystems are low temperatures and a pronounced seasonal variability of ice cover, light regime and primary production. Depending on their ecological niche and trophic position, zooplankton species at high latitudes have developed a variety of reproductive strategies and energetic adaptations to cope with these extreme environmental conditions. Life-cycle strategies of the herbivorous copepods and euphausiids, which make up the major portion of polar zooplankton biomass, include seasonal vertical migration, dormancy (diapause, quiescence) and the accumulation of energy reserves. These lipid stores help to buffer the pulsed seasonal food supply, and they play an important role in fueling reproduction independent of phytoplankton. Only a smaller fraction of the lipid reserves accumulated during spring and summer are usually catabolized for metabolic maintenance during the food-limited dark season. These deposits are retained until the end of winter and allow early egg production and spawning prior to—or coinciding with—the onset of vernal primary production. It enables the new generation to make full use of the short productive season for growth and development to reach viable overwintering stages. The Antarctic krill Euphausia superba is an exception since it uses its depot lipids for metabolic maintenance during the dark season. It therefore relies on external resources (Primary production) for reproductive processes, resulting in a later spawning period as compared to the other euphausiids. Another important component of the herbivorous Antarctic zooplankton, the salps, have developed a very different reproductive strategy. They are able to switch from sexual reproduction to asexual budding (metagenesis), which allows extreme multiplication rates under favourable feeding conditions. Due to these successful adaptations, herbivores are able to build up huge stocks, in spite of the short productive period. Omnivorous and carnivorous zooplankton species, e.g., amphipods or chaetognaths, are not much constrained by the seasonality problem, but experience a more constant food supply. They show a tendency towards K strategies with a prolonged reproductive period, reduced egg numbers and increasing parental care. However, they do not exhibit such typical “polar adaptations” as developed by the herbivorous species.     

Aerobic metabolism in the genus Lactobacillus: impact on stress response and potential applications in the food industry

This review outlines the recent advances in the knowledge on aerobic and respiratory growth of lactic acid bacteria, focusing on the features of respiration‐competent lactobacilli. The species of the genus Lactobacillus have been traditionally classified as oxygen‐tolerant anaerobes, but it has been demonstrated that several strains are able to use oxygen as a substrate in reactions mediated by flavin oxidases and, in some cases, to synthesize a minimal respiratory chain. The occurrence of genes related to aerobic and respiratory metabolism and to oxidative stress response apparently correlates with the taxonomic position of lactobacilli. Members of the ecologically versatile Lactobacillus casei, L. plantarum and L. sakei groups are apparently best equipped to deal with aerobic/respiratory growth. The shift from anaerobic growth to aerobic (oxygen) and/or respiratory promoting (oxygen, exogenous haem and menaquinone) conditions offers physiological advantages and affects the pattern of metabolite production in several species. Even if this does not result in dramatic increases in biomass production and growth rate, cells grown in these conditions have improved tolerance to heat and oxidative stresses. An overview of benefits and of the potential applications of Lactobacillus cultures grown under aerobic or respiratory conditions is also discussed.     

Comparison of oxygen consumption in drosophilid flies from different climates

Oxygen consumption at rest was studied in drosophilid species from cool‐temperate, warm‐temperate and subtropical regions to assess whether adaptations to different climates are associated with changes in metabolic rates. In experiments at 23°C using 8‐day‐old males of 28 species, body mass was revealed to be a significant predictor of oxygen consumption. No significant relation was detected between mass‐adjusted oxygen consumption and latitudinal distribution or thermal tolerance by either conventional regression analysis or a phylogenetically based method. The effect of temperature on oxygen consumption was studied with experiments at 15, 18, 23 and 28°C using 8‐ and 24‐day‐old males of four species of each of the montium species subgroup and the subgenus Drosophila. In these experiments, it was confirmed that temperature was a significant predictor of mass‐adjusted oxygen consumption. In both lineages, mass‐adjusted oxygen consumption was not higher in cool‐temperate species than in subtropical species. Thus, adaptations to colder climates are not associated with elevation of metabolic rates in these drosophilid species. The results of the present study also indicate that oxygen consumption is not related to the capacity to walk quickly.     

A computational model of cardiomyocyte metabolism predicts unique reperfusion protocols capable of reducing cell damage during ischemia/reperfusion

If a coronary blood vessel is occluded and the neighboring cardiomyocytes deprived of oxygen, subsequent reperfusion of the ischemic tissue can lead to oxidative damage due to excessive generation of reactive oxygen species. Cardiomyocytes and their mitochondria are the main energy producers and consumers of the heart, and their metabolic changes during ischemia seem to be a key driver of reperfusion injury. Here, we hypothesized that tracking changes in cardiomyocyte metabolism, such as oxygen and ATP concentrations, would help in identifying points of metabolic failure during ischemia and reperfusion. To track some of these changes continuously from the onset of ischemia through reperfusion, we developed a system of differential equations representing the chemical reactions involved in the production and consumption of 67 molecular species. This model was validated and used to identify conditions present during periods of critical transition in ischemia and reperfusion that could lead to oxidative damage. These simulations identified a range of oxygen concentrations that lead to reverse mitochondrial electron transport at complex I of the respiratory chain and a spike in mitochondrial membrane potential, which are key suspects in the generation of reactive oxygen species at the onset of reperfusion. Our model predicts that a short initial reperfusion treatment with reduced oxygen content (5% of physiological levels) could reduce the cellular damage from both of these mechanisms. This model should serve as an open-source platform to test ideas for treatment of the ischemia reperfusion process by following the temporal evolution of molecular concentrations in the cardiomyocyte.     

The oxygen sensing signal cascade under the influence of reactive oxygen species

Structural and functional integrity of organ function profoundly depends on a regular oxygen and glucose supply. Any disturbance of this supply becomes life threatening and may result in severe loss of organ function. Particular reductions in oxygen availability (hypoxia) caused by respiratory or blood circulation irregularities cannot be tolerated for longer periods due to an insufficient energy supply by anaerobic glycolysis. Complex cellular oxygen sensing systems have evolved to tightly regulate oxygen homeostasis. In response to variations in oxygen partial pressure (PO2), these systems induce adaptive and protective mechanisms to avoid or at least minimize tissue damage. These various responses might be based on a range of oxygen sensing signal cascades including an isoform of the neutrophil NADPH oxidase, different electron carrier units of the mitochondrial chain such as a specialized mitochondrial, low PO2 affinity cytochrome c oxidase (aa3) and a subfamily of 2-oxoglutarate dependent dioxygenases termed HIF (hypoxia inducible factor) prolyl-hydroxylase and HIF asparaginyl hydroxylase called factor-inhibiting HIF (FIH-1). Thus, specific oxygen sensing cascades involving reactive oxygen species as second messengers may by means of their different oxygen sensitivities, cell-specific and subcellular localization help to tailor various adaptive responses according to differences in tissue oxygen availability.     

Thermodynamics constrains the evolution of insect population growth rates: "warmer is better"

Diverse biochemical and physiological adaptations enable different species of ectotherms to survive and reproduce in very different temperature regimes, but whether these adaptations fully compensate for the thermodynamically depressing effects of low temperature on rates of biological processes is debated. If such adaptations are fully compensatory, then temperature-dependent processes (e.g., digestion rate, population growth rate) of cold-adapted species will match those of warm-adapted species when each is measured at its own optimal temperature. Here we show that cold-adapted insect species have much lower maximum rates of population growth than do warm-adapted species, even when we control for phylogenetic relatedness. This pattern also holds when we use a structural-equation model to analyze alternative hypotheses that might otherwise explain this correlation. Thus, although physiological adaptations enable some insects to survive and reproduce at low temperatures, these adaptations do not overcome the "tyranny" of thermodynamics, at least for rates of population increase. Indeed, the sensitivity of population growth rates of insects to temperature is even greater than predicted by a recent thermodynamic model. Our findings suggest that adaptation to temperature inevitably alters the population dynamics of insects. This result has broad evolutionary and ecological consequences.     

Preface: New challenges in anostracan research,a tribute to Graziella Mura

Although conjugating algae are considered to have a cosmopolitan freshwater distribution, numerous ecological and taxonomic investigations revealed that many desmid taxa (at the level of genus, species and variety) are capable of occupying specific geographic zones, characterized by particular climatic attributes. Earlier studies have dealt with influences of temperature and irradiation (photosynthetically active radiation and ultraviolet radiation) on the physiology and ultrastructure of desmids. Yet, recent investigations demonstrated a clear relationship between these climatic factors and the distributional potential of conjugating algae, taking into account their photosynthetic, physiological and ultrastructural adaptations which had been revealed during and after certain temperature and irradiation treatments. Despite the fact that desmids can be considered as high-light-adapted algae, various species- and strain-specific characteristics and adaptations appeared in accordance with the light intensities predominating at their source localities, as estimated by their photosynthetic performance (obtained from PAM fluorometry and oxygen evolution measurements), pigment composition and morpho-anatomical characteristics. Interestingly, the high-light adaptation of photosynthesis as well as the relatively high growth temperature optima for majority of the desmid species investigated may provide some support for Coesel’s hypothesis on the origin of desmids in the tropical zone.