Ectoparasite Activity During Incubation Increases Microbial Growth on Avian Eggs

Abstract

While direct detrimental effects of parasites on hosts are relatively well documented, other more subtle but potentially important effects of parasitism are yet unexplored. Biological activity of ectoparasites, apart from skin injuries and blood-feeding, often results in blood remains, or parasite faeces that accumulate and modify the host environment. In this way, ectoparasite activities and remains may increase nutrient availability that may favour colonization and growth of microorganisms including potential pathogens. Here, by the experimental addition of hematophagous flies (Carnus hemapterus, a common ectoparasite of birds) to nests of spotless starlings Sturnus unicolor during incubation, we explore this possible side effect of parasitism which has rarely, if ever, been investigated. Results show that faeces and blood remains from parasitic flies on spotless starling eggshells at the end of incubation were more abundant in experimental than in control nests. Moreover, eggshell bacterial loads of different groups of cultivable bacteria including potential pathogens, as well as species richness of bacteria in terms of Operational Taxonomic Units (OTUs), were also higher in experimental nests. Finally, we also found evidence of a link between eggshell bacterial loads and increased embryo mortality, which provides indirect support for a bacterial-mediated negative effect of ectoparasitism on host offspring. Trans-shell bacterial infection might be one of the main causes of embryo death and, consequently, this hitherto unnoticed indirect effect of ectoparasitism might be widespread in nature and could affect our understanding of ecology and evolution of host-parasite interactions.

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

“…Avian reproductive strategies and overall reproductive success are probably under the strong selective pressure of environmental microorganisms. Recent studies have found bacterial density on the eggshell to be the main precursor of hatching failure across avian species (Lee et al, 2017;Peralta-Sanchez et al, 2018;Tomas et al, 2018). These findings are not surprising given that previous studies documented that microbes are able to pass through the eggshell into the egg interior and negatively affect embryo viability (Bruce and Drysdale, 1994;Pinowski et al, 1994;Cook et al, 2003;Fonseca et al, 2011;Hansen et al, 2015) or hatchling phenotype (Javurkova et al, 2014).…”

The Effects of Landscape Urbanization on the Gut Microbiome: An Exploration Into the Gut of Urban and Rural White-Crowned Sparrows

“…Egg-laying animals can initially inoculate eggs in ovo, as seen in five bird species and one lizard species (Ruiz-Rodríguez et al, 2018;Trevelline et al, 2018). For birds, the egg environment in the nest is relatively sterile and inoculation at this stage depends on temperature, humidity, nest hygiene (reviewed in D'Alba and Shawkey, 2015), and ectoparasites (Tomás et al, 2018). Once chicks are hatched, the food fed by parents is likely to further inoculate the gut microbiome (Ruiz-Rodríguez et al, 2018); therefore horizontal transmission of microbes is likely to have a strong effect on gut microbiome diversity.…”

Experimental old nest material predicts hoopoe Upupa epops eggshell and uropygial gland microbiota

“…Parental and breeding activity, as well as nest material and ectoparasites, determine bacterial environment of nesting cavities and of eggshells (González-Braojos et al 2012, Peralta-Sánchez et al 2012, Grizard et al 2015, Tomás et al 2018. These bacteria can have positive, negative or no effects on the offspring (Singleton and Harper 1996, Moreno et al 2003, González-Braojos et al 2012, Soler et al 2017, Devaynes et al 2018.…”