Lipid composition of the stratum corneum and cutaneous water loss in birds along an aridity gradient

Abstract

SUMMARYIntercellular and covalently bound lipids within the stratum corneum (SC), the outermost layer of the epidermis, are the primary barrier to cutaneous water loss (CWL) in birds. We compared CWL and intercellular SC lipid composition in 20 species of birds from desert and mesic environments. Furthermore, we compared covalently bound lipids with CWL and intercellular lipids in the lark family (Alaudidae). We found that CWL increases in birds from more mesic environments, and this increase was related to changes in intercellular SC lipid composition. The most consistent pattern that emerged was a decrease in the relative amount of cerebrosides as CWL increased, a pattern that is counterintuitive based on studies of mammals with Gaucher disease. Although covalently bound lipids in larks did not correlate with CWL, we found that covalently bound cerebrosides correlated positively with intercellular cerebrosides and intercellular cholesterol ester, and intercellular cerebrosides correlated positively with covalently bound free fatty acids. Our results led us to propose a new model for the organization of lipids in the avian SC, in which the sugar moieties of cerebrosides lie outside of intercellular lipid layers, where they may interdigitate with adjacent intercellular cerebrosides or with covalently bound cerebrosides.

The Impact of Humidity on Evaporative Cooling in Small Desert Birds Exposed to High Air Temperatures

“…Rates of cutaneous water loss (CEWL) in birds are regulated in part by adrenergic control of venous blood flow to the skin in response to heat stress (Ophir et al 2002) and as such are not completely passive, but the metabolic costs of modulating CEWL seem to be negligible (Marder and Ben-Asher 1983;Marder and GavrieliLevin 1987). The permeability of the skin to water is directly related to the relative quantity and structure of the lipids in the stratum corneum, which varies with environmental aridity and among phylogenetic classes of birds (Haugen et al 2003;Ro and Williams 2010;Muñoz-Garcia and Williams 2011;Champagne et al 2012). The specific mechanisms that columbiforme birds use to greatly enhance cutaneous evaporation at high temperatures have not received as much attention Hoffman and Walsberg 1999;McKechnie and Wolf 2004).…”

Lipid composition and molecular interactions change with depth in the avian stratum corneum to regulate cutaneous water loss

“…Ceramide II, the more polar group of ceramides, and cerebrosides increased at a greater rate with depth in winter birds than in summer birds, indicating that these lipids play an instrumental role in reducing CWL, especially in the deeper levels of the SC. More polar lipids have been correlated with lower rates of CWL in birds (Haugen et al, 2003;Muñoz-Garcia et al, 2008a,b;Champagne et al, 2012).…”

“…The composition and attendant organization of these lipid classes affects the rate of CWL . Previous studies on birds have found that higher amounts of free fatty acids and triacylglycerols within the SC are associated with higher rates of CWL, whereas more polar ceramides and cerebrosides are associated with lower rates of CWL (Haugen et al, 2003;Muñoz-Garcia et al, 2008a,b;Champagne et al, 2012). Cerebrosides are thought to be especially important in regulating CWL, as they account for approximately one-third of all lipids in the SC in birds, and occur in greater amounts in the SC of birds acclimated to cold, dry conditions than in birds acclimated to warmer, more humid conditions (Muñoz-Garcia et al, 2008a).…”

“…Some lipids within the matrix of the SC are covalently bound to the corneocytes (Wertz and Downing, 1987;Gu et al, 2008), whereas others occupy the intercellular space in layers called lamellae (Wertz and Downing, 1982). These lamellar lipids are arranged in either bilayers (Wertz and Downing, 1982;Champagne et al, 2012) or trilayers (Bouwstra et al, 2000;Muñoz-Garcia et al, 2008a), and appear to serve as the primary barrier to CWL . Lamellar lipids in the avian SC consist primarily of cholesterol esters, fatty acid methyl esters, triacylglycerols, free fatty acids, cholesterol, ceramides and cerebrosides, the last of these being a ceramide with a glucose moiety attached to the headgroup (Menon et al, 1986;Haugen et al, 2003;Muñoz-Garcia et al, 2006;Ro and Williams, 2010).…”

“…Because of this orientation, the sugar moieties of cerebrosides may slow the rate of CWL by forming strong hydrogen bonds with adjacent water molecules to form a primary solvation shell (Bach et al, 1982). Although these strong hydrogen bonds weaken the hydrogen bonding of water molecules outside the solvation shell (Gallina et al, 2006), the strong hydrogen bonds formed within the solvation shell increase the overall viscosity of the water, which may slow the rate of permeation through the SC (Comesaña et al, 2003;Clement et al, 2012;Champagne et al, 2012). Current models remain speculative and do not address variation in molecular interactions in different layers of the SC, or how this variation affects the rate of CWL.…”