Are antimicrobial defences in bird eggs related to climatic conditions associated with risk of trans-shell microbial infection?

Abstract

IntroductionAll bird eggs are exposed to microbes in the environment, which if transmitted to the developing embryo, could cause hatching failure. However, the risk of trans-shell infection varies with environmental conditions and is higher for eggs laid in wetter environments. This might relate to generally higher microbial abundances and diversity in more humid environments, including on the surface of eggshells, as well as the need for moisture to facilitate microbial penetration of the eggshell. To protect against microbial infection, the albumen of avian eggs contains antimicrobial proteins, including lysozyme and ovotransferrin. We tested whether lysozyme and ovotransferrin activities varied in eggs of larks (Alaudidae) living along an arid-mesic gradient of environmental aridity, which we used as a proxy for risk of trans-shell infection.ResultsContrary to expectations, lysozyme activity was highest in eggs from hotter, more arid locations, where we predicted the risk of trans-shell infection would be lower. Ovotransferrin concentrations did not vary with climatic factors. Temperature was a much better predictor of antimicrobial protein activity than precipitation, a result inconsistent with studies stressing the importance of moisture for trans-shell infection.ConclusionsOur study raises interesting questions about the links between temperature and lysozyme activity in eggs, but we find no support for the hypothesis that antimicrobial protein deposition is higher in eggs laid in wetter environments.

Different incubation patterns affect selective antimicrobial properties of the egg interior: experimental evidence from eggs of precocial and altricial birds

“…However, we did not observe changes in egg white pH in altricial eggs resulting from different incubation patterns. As a similar trend with a rather slight decrease of egg white pH along with incubation cycle has been documented in studies on altricial eggs of the family Alaudidae (Horrocks et al, 2014;Grizard et al, 2015), this suggests that the effect of incubation pattern on egg white pH is likely to be species specific across the avian precocial-altricial spectrum.…”

“…It is therefore obvious that many other factors such as ambient temperature (Saino et al, 2004;Horrocks et al, 2014), nest humidity (Wellman-Labadie et al, 2008c), laying sequence and stage of breeding season (Saino et al, 2002;Bonisoli-Alquati et al, 2010) or individual intrinsic factors (D'Alba et al, 2010b) affect the deposition and/or activity of egg white AMPs. As we used two representative altricial and precocial model species bred under relatively controlled conditions, we can exclude these potentially confounding factors in our study.…”

Dehydration during egg production alters egg composition and yolk immune function

“…Microbial infection of eggs can drastically reduce clutch viability and, once pathogens pass through the membrane and infect the developing embryo, there is typically a low chance of survival (Kiesecker and Blaustein, 1997, Adamo, 1999, Cook et al, 2003, Brandl et al, 2014. A robust antimicrobial defense is therefore fundamental to the health of developing embryos (Shawkey et al, 2008, Horrocks et al, 2014. Python embryos at oviposition are approximately one-third through development (Lourdais et al, 2008) and have fully functional livers, which is primary source of synthesis for antimicrobial peptides (van Hoek, 2014).…”

Geographic variation in baseline innate immune function does not follow variation in aridity along a tropical environmental gradient

“…Results from studies that used similar immune indices to the ones used in this study are equivocal: a study 30 on different species of adult larks (Alaudidae) along an aridity gradient spanning desert, temperate and tropics showed negative correlations between aridity and haemagglutination and haemolysis titres, and haptoglobin concentration, but no correlations between aridity and ovotransferrin concentration. However, another study 83 on antimicrobial proteins in eggs from larks in different environments showed contrasting patterns between ovotransferrin and lysozyme concentration in egg albumen. Elsewhere in the tropics, a study 21 on chicks of Red-capped Larks Calandrella cinerea from three climatically distinct locations in Kenya recorded no differences between immune indices, even though these chicks showed significant differences in growth patterns.…”

“…S1-5). Studies involving larger latitudinal gradients show that mean annual temperature seems to explain variation in parasite load and immune indices better than precipitation 19,83 . Results from studies that used similar immune indices to the ones used in this study are equivocal: a study 30 on different species of adult larks (Alaudidae) along an aridity gradient spanning desert, temperate and tropics showed negative correlations between aridity and haemagglutination and haemolysis titres, and haptoglobin concentration, but no correlations between aridity and ovotransferrin concentration.…”