Partial incubation during egg laying reduces eggshell microbial loads in a temperate‐breeding passerine

Abstract

Incubation prior to clutch completion may be adaptive if it maintains egg viability by inhibiting eggshell microbial growth, thus reducing the likelihood that the embryo becomes infected. To test this hypothesis, we examined the effect of partial incubation during egg laying on eggshell microbial loads in eastern bluebirds Sialia sialis breeding at a temperate‐zone site. We sampled eggshell microbes prior to and following four days of exposure to either partial incubation during the laying period or ambient environmental conditions without incubation (experimental eggs). Microbial colony counts declined significantly for eggs left in the nest during the laying period but did not vary significantly for eggs exposed to ambient conditions. Initial microbial loads were more similar to those previously reported from tropical than temperate environments, and microbes from potentially pathogenic groups were detected on 88% of first‐laid eggs on the day of laying. Egg viability was maintained when eggs were held indoors for four days without incubation but declined sharply thereafter. Our results suggest that partial incubation during egg laying may enhance egg viability in eastern bluebirds by reducing eggshell microbial loads; these effects appear stronger than those usually reported from the temperate zone.

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

“…These findings are in line with our previous study demonstrating no effect of partial incubation on the probability and intensity of microbial trans-shell infection in mallard (Anas platyrhynchos) eggs (Javurkova et al, 2014). It appears, therefore, that the protective role of incubation is inherent in the reduction of the eggshell microbial load (Cook et al, 2005a;D'Alba et al, 2010a;Ruiz-De-Castaneda et al, 2011Soler et al, 2015;Bollinger et al, 2018) and the enhancement of commensal/beneficial eggshell microbes (Shawkey et al, 2009;Grizard et al, 2014Grizard et al, , 2015 that are able to enter the egg interior. We Statistics for particular explanatory variables were found using a backward stepwise procedure, and correspond to the step when each term was removed from the model.…”

“…Among them, variation in the eggshell microstructure (D'Alba et al, 2014;Grellet-Tinner et al, 2017), eggshell pigmentation (Ishikawa et al, 2010), deposition of egg white antimicrobial proteins (AMPs) into the eggshell membranes and cuticle (Bain et al, 2013;Gautron et al, 2011;Wellman-Labadie et al, 2008a), and cuticle nanostructuring (D'Alba et al, 2016(D'Alba et al, , 2017 have been documented to significantly reduce the eggshell microbial load. Among behavioural mechanisms, partial and full incubation of a clutch have been shown to significantly reduce the abundance (Bollinger et al, 2018;Cook et al, 2005a;D'Alba et al, 2010a;Ruiz-De-Castaneda et al, 2011 but also the diversity and community structure of the eggshell microbiota (Grizard et al, 2014(Grizard et al, , 2015Lee et al, 2014). In contrast, defence mechanisms in species of the family Megapodiidae, which do not incubate their clutches, lie in the covering of the eggshells with an inorganic layer of nanometer-scale spheres of hydroxyapatite, making the eggshells super-hydrophobic and preventing attachment by bacteria (D'Alba et al, 2014).…”

Partial incubation-induced changes in concentrations of egg white antimicrobials do not influence trans-shell infection but affect hatchling phenotype

“…For example, changes of egg white lysozyme and ovotransferrin concentrations were found to enhance proliferation of beneficial probiotic microorganism in egg white 30 . Therefore, while incubation may significnatly shift eggshell microbiota 6,[45][46][47][48] , its selective antimicrobial effect inside the egg is most probably inherent in mediation of changes in chemical and proteomic profile of the egg white. Furthermore, as evidence exists for physiological role of lysozyme and avidin on developing embryo resulting in alterations of hatchlings phenotypic traits 49,50 , incubation-mediated changes in egg white AMPs profile might also significantly shape hatchlings´ phenotype.…”

“…Nevertheless, proximate role of clutch covering with feather nest lining on egg white AMPs concentration has not yet been evaluated to date. Partial incubation is behaviour preceding full incubation of complete clutch in many bird species 53 with documented function to keep eggs dry 54 , modulate eggshell microbiota 18,48 , or have antipredator role 55,56 . Yet, if partial incubation may affect or stabilize antimicrobial properties of egg content is unknown.…”

Ambient temperature and female body condition are related to night incubation behavior in wood ducksAix sponsa

“…For example, partial incubation may preserve the viability of unhatched eggs prior to clutch completion and full incubation begins (Arnold et al , Arnold ). Indeed, partial incubation may protect early laid eggs from extreme temperatures (Grant , Ward , MacDonald et al , Carroll et al ) or infection by pathogenic microflora (Cook et al , , b, Shawkey et al , D'Alba et al , Ruiz‐De‐Castañeda et al , Bollinger et al ; but see Walls et al , , Javŭrková et al ), which can be deleterious to egg viability. Additionally, partial incubation may reduce the length of the full incubation period by promoting embryonic development prior to the onset of full incubation (Nilsson and Svensson , Grenier and Beissinger , Hanssen et al , Hepp , DuRant et al ).…”