Agustí Muñoz-Garcia

Tropical birds have a slow pace of life

Tropical birds are relatively long-lived and produce few offspring, which develop slowly and mature relatively late in life, the slow end of the life-history axis, whereas temperate birds lie at the opposite end of this continuum. We tested the hypothesis that tropical birds have evolved a reduced basal metabolic rate (BMR). We measured BMR of 69 species of tropical birds, the largest data set amassed on metabolic rates of tropical birds, and compared these measurements with 59 estimates of BMR for temperate birds. Our analyses included conventional least squares regression, regressions based on phylogenetic independent contrasts, and a comparison of BMR of 13 phylogenetically matched pairs, one species from the tropics and one from northerly temperate areas. Our triptych showed that tropical birds had a reduced BMR, compelling evidence for a connection between the life history of tropical birds and a slow pace of life. Further, tropical migrants breeding in temperate habitats had a lower BMR than did temperate residents, suggesting that these migrants have physiological traits consistent with a slow pace of life. In addition, we determined that tropical birds had a lower cold-induced peak metabolic rate and thermogenic metabolic scope than temperate species, a finding that is consistent with the hypothesis that their environment has not selected for high levels of thermogenesis, or alternatively, that a slow pace of life may be incompatible with high thermogenic capacity. We conclude that physiological function correlates with the suite of life-history traits.

Basal Metabolic Rate in Carnivores Is Associated with Diet after Controlling for Phylogeny

Studies of basal metabolic rate (BMR), the minimum metabolic rate of postabsorptive, inactive endotherms while in their rest phase and thermal neutral zone, have contributed significantly to our understanding of animal energetics. Besides body mass, the main determinant of BMR, researchers have invoked diet and phylogenetic history as important factors that influence BMR, although their relative importance has been controversial. For 58 species within the Carnivora, we tested the hypothesis that BMR is correlated with home range size, a proxy for level of activity, and diet, using conventional least squares regression (CLSR) and regression based on phylogenetic independent contrasts (PIC). Results showed that BMR of Carnivora was positively correlated with home range size after controlling for body mass, regardless of the statistical method employed. We also found that diet and mass‐adjusted home range size were correlated. When we simultaneously tested the effect of diet and mass‐adjusted home range on mass‐adjusted BMR, home range size was insignificant because of its colinearity with diet. Then we eliminated home range size from our model, and diet proved to be significant with both CLSR and PIC. We concluded that species that eat meat have larger home ranges and higher BMR than species that eat vegetable matter. To advance our understanding of the potential mechanisms that might explain our results, we propose the “muscle performance hypothesis,” which suggests that selection for different muscle fiber types can account for the differences in BMR observed between meat eaters and vegetarian species within the Carnivora.

Cutaneous water loss and lipids of the stratum corneum in house sparrows Passer domesticus from arid and mesic environments.

SUMMARY Birds that live in hot, dry environments must balance water intake with losses in order to maintain water homeostasis. The outer layer of the integument, called the stratum corneum (SC), consists of corneocytes embedded in a matrix of lipids. The SC serves as a barrier to water vapor diffusion through the skin. We measured cutaneous water loss (CWL) in two populations of house sparrow Passer domesticus L., one living in a desert environment in Saudi Arabia, and another living in a mesic environment in Ohio, USA. We found that CWL rates at 30°C were lower in desert individuals (11.9±2.2 mg H2O cm-2 day-1; N=11) than in mesic birds (16.0±2.6 mg H2O cm-2 day-1; N=14). We hypothesized that changes in the lipid composition of the SC could affect CWL. We analyzed four classes of lipids in the SC: ceramides, cerebrosides, cholesterol and free fatty acids, by thin layer chromatography. Compared to mesic sparrows, desert birds had a higher amount of ceramides (49.2±10.3 mg g-1 SC dry mass in Saudi Arabia; 38.2±18.0 mg g-1 SC dry mass in Ohio) and cerebrosides (101.2±48.9 mg g-1 SC dry mass in Saudi Arabia; 56.5±34.0 mg g-1 SC dry mass in Ohio), and a lower percentage of cholesterol (4.1±3.6% in Saudi Arabia; 5.4±2.5% in Ohio) in their SC. Although CWL was lower in sparrows from Arabia, and lipid composition of their SC differed, we could not detect differences between rates of water loss through non-living skin attached to glass vials (46.0±15.7 mg H2O cm-2 day-1 for sparrows in Saudi Arabia; 45.8±27.2 mg H2O cm-2 day-1 for sparrows in Ohio). These results suggest that biological control mechanisms interact with layers of lipids in the stratum corneum to adjust CWL to the environment.

The importance of the lipoxygenase-hepoxilin pathway in the mammalian epidermal barrier

This review covers the background to discovery of the two key lipoxygenases (LOX) involved in epidermal barrier function, 12R-LOX and eLOX3, and our current views on their functioning. In the outer epidermis, their consecutive actions oxidize linoleic acid esterified in ω-hydroxy-ceramide to a hepoxilin-related derivative. The relevant background to hepoxilin and trioxilin biochemistry is briefly reviewed. We outline the evidence that linoleate in the ceramide is the natural substrate of the two LOX enzymes and our proposal for its importance in construction of the epidermal water barrier. Our hypothesis is that the oxidation promotes hydrolysis of the oxidized linoleate moiety from the ceramide. The resulting free ω-hydroxyl of the ω-hydroxyceramide is covalently bound to proteins on the surface of the corneocytes to form the corneocyte lipid envelope, a key barrier component. Understanding the role of the LOX enzymes and their hepoxilin products should provide rational approaches to ameliorative therapy for a number of the congenital ichthyoses involving compromised barrier function. This article is part of a Special Issue entitled The Important Role of Lipids in the Epidermis and their Role in the Formation and Maintenance of the Cutaneous Barrier. Guest Editors: Kenneth R. Feingold and Peter Elias.

Cutaneous water loss and sphingolipids in the stratum corneum of house sparrows, Passer domesticus L., from desert and mesic environments as determined by reversed phase high-performance liquid chromatography coupled with atmospheric pressure photospray ionization mass spectrometry.

SUMMARY Because cutaneous water loss (CWL) represents half of total water loss in birds, selection to reduce CWL may be strong in desert birds. We previously found that CWL of house sparrows from a desert population was about 25% lower than that of individuals from a mesic environment. The stratum corneum (SC), the outer layer of the epidermis, serves as the primary barrier to water vapor diffusion through the skin. The avian SC is formed by layers of corneocytes embedded in a lipid matrix consisting of cholesterol, free fatty acids and two classes of sphingolipids, ceramides and cerebrosides. The SC of birds also serves a thermoregulatory function; high rates of CWL keep body temperatures under lethal limits in episodes of heat stress. In this study, we used high-performance liquid chromatography coupled with atmospheric pressure photoionization-mass spectrometry (HPLC/APPI-MS) to identify and quantify over 200 sphingolipids in the SC of house sparrows from desert and mesic populations. Principal components analysis (PCA) led to the hypotheses that sphingolipids in the SC of desert sparrows have longer carbon chains in the fatty acid moiety and are more polar than those found in mesic sparrows. We also tested the association between principal components and CWL in both populations. Our study suggested that a reduction in CWL found in desert sparrows was, in part, the result of modifications in chain length and polarity of the sphingolipids, changes that apparently determine the interactions of the lipid molecules within the SC.

Phenotypic Flexibility in Cutaneous Water Loss and Lipids of the Stratum Corneum in House Sparrows (Passer domesticus) following Acclimation to High and Low Humidity

Resistance to water‐vapor diffusion through the skin is thought to be conferred by lipids in the stratum corneum (SC), the outer layer of the epidermis. We tested the effect of ambient humidity on cutaneous water loss (CWL) and lipid composition of the SC by acclimating house sparrows (Passer domesticus) to either a dry (6.5 g/m3 absolute humidity) or a humid (31 g/m3) environment for 3 wk at a thermoneutral temperature (30°C). Sparrows in the dry‐acclimated group reduced CWL by 36% compared with those in the humid environment. Relative to initial values, both groups of sparrows decreased CWL, 45% in the dry‐acclimated group and 23% in the humid group, suggesting that temperature is also an important stimulus for CWL apart from humidity. Both groups of acclimated sparrows decreased quantities of cholesterol, free fatty acids, and cerebrosides and increased the proportion of ceramides in their SC. Lipid amounts or proportions in the SC did not differ between dry‐ and humid‐acclimated sparrows, but the free fatty acid:ceramide ratio was significantly lower in dry‐acclimated birds. Also, lipid composition was only correlated with CWL in dry‐acclimated sparrows, suggesting that structural changes to SC lipids are more tightly linked to CWL regulation in response to low humidity. Our results demonstrate phenotypic flexibility in CWL and lipid composition of the SC and provide support for a functional relationship between these traits.

Climate change and cutaneous water loss of birds

Summary There is a crucial need to understand how physiological systems of animals will respond to increases in global air temperature. Water conservation may become more important for some species of birds, especially those living in deserts. Lipids of the stratum corneum (SC), the outer layer of the epidermis, create the barrier to water vapor diffusion, and thus control cutaneous water loss (CWL). An appreciation of the ability of birds to change CWL by altering lipids of the skin will be important to predict responses of birds to global warming. The interactions of these lipids are fundamental to the modulation of water loss through skin. Cerebrosides, with their hexose sugar moiety, are a key component of the SC in birds, but how these lipids interact with other lipids of the SC, or how they form hydrogen bonds with water molecules, to form a barrier to water vapor diffusion remains unknown. An understanding of how cerebrosides interact with other lipids of the SC, and of how the hydroxyl groups of cerebrosides interact with water molecules, may be a key to elucidating the control of CWL by the SC.

PNPLA1 has a crucial role in skin barrier function by directing acylceramide biosynthesis

Mutations in patatin-like phospholipase domain-containing 1 (PNPLA1) cause autosomal recessive congenital ichthyosis, but the mechanism involved remains unclear. Here we show that PNPLA1, an enzyme expressed in differentiated keratinocytes, plays a crucial role in the biosynthesis of ω-O-acylceramide, a lipid component essential for skin barrier. Global or keratinocyte-specific Pnpla1-deficient neonates die due to epidermal permeability barrier defects with severe transepidermal water loss, decreased intercellular lipid lamellae in the stratum corneum, and aberrant keratinocyte differentiation. In Pnpla1−/− epidermis, unique linoleate-containing lipids including acylceramides, acylglucosylceramides and (O-acyl)-ω-hydroxy fatty acids are almost absent with reciprocal increases in their putative precursors, indicating that PNPLA1 catalyses the ω-O-esterification with linoleic acid to form acylceramides. Moreover, acylceramide supplementation partially rescues the altered differentiation of Pnpla1−/− keratinocytes. Our findings provide valuable insight into the skin barrier formation and ichthyosis development, and may contribute to novel therapeutic strategies for treatment of epidermal barrier defects.

The Relationship between Cutaneous Water Loss and Thermoregulatory State in Kuhl’s Pipistrelle Pipistrellus kuhlii, a Vespertillionid Bat

Total evaporative water loss is the sum of respiratory water loss (RWL) and cutaneous water loss (CWL) and constitutes the main avenue of water loss in bats. Because bats fly and have large surface-to-volume ratios, they potentially have high rates of RWL and CWL. Most species of small insectivorous bats have the ability to reduce their body temperature (Tb) at rest, which substantially reduces energy expenditure and water loss. We hypothesized that bats reduce evaporative water loss during bouts of deep hypothermia (torpor) by decreasing RWL and CWL. We measured Tb, RWL, CWL, and resting metabolic rate (RMR) in Kuhl’s pipistrelle Pipistrellus kuhlii, a small insectivorous bat. In support of our hypothesis, we found that RWL decreased with decreasing RMR. We found that CWL was lower in torpid individuals than in normothermic bats; however, bats in deep torpor had similar or higher CWL than bats in shallow torpor, suggesting that they exert a less effective physiological control over CWL when in deep torpor. Because insectivorous bats spend most of their lives in torpor or hibernation, the regulation of CWL in different heterothermic states has relevant ecological and evolutionary consequences.

A Phylogenetic Approach to Total Evaporative Water Loss in Mammals

Maintaining appropriate water balance is a constant challenge for terrestrial mammals, and this problem can be exacerbated in desiccating environments. It has been proposed that natural selection has provided desert-dwelling mammals physiological mechanisms to reduce rates of total evaporative water loss. In this study, we evaluated the relationship between total evaporative water loss and body mass in mammals by using a recent phylogenetic hypothesis. We compared total evaporative water loss in 80 species of arid-zone mammals to that in 56 species that inhabit mesic regions, ranging in size from 4 g to 3,500 kg, to test the hypothesis that mammals from arid environments have lower rates of total evaporative water loss than mammals from mesic environments once phylogeny is taken into account. We found that arid species had lower rates of total evaporative water loss than mesic species when using a dichotomous variable to describe habitat (arid or mesic). We also found that total evaporative water loss was negatively correlated with the average maximum and minimum environmental temperature as well as the maximum vapor pressure deficit of the environment. Annual precipitation and the variable Q (a measure of habitat aridity) were positively correlated with total evaporative water loss. These results support the hypothesis that desert-dwelling mammals have lower rates of total evaporative water loss than mesic species after controlling for body mass and evolutionary relatedness regardless of whether categorical or continuous variables are used to describe habitat.