Seasonal patterns in immune indices reflect microbial loads on birds but not microbes in the wider environment

Abstract

Abstract. Documenting patterns in immune function is a first step to understanding immune variation, but to comprehend causes and consequences, antigen and parasite exposure that may drive such variation must be determined. We measured host-independent microbial exposure in five species of larks (Alaudidae) in the Arabian Desert by sampling ambient air for culturable microbes during late spring and winter, two periods with contrasting environmental conditions. We developed a novel technique to assay densities of microbes shed from birds, and we quantified four indices of constitutive innate immunity. Birds shed significantly more microbes during spring than winter, and all immune indices except one were also significantly higher during spring. In contrast, concentrations of airborne environmental microbes were higher in winter. Among all birds in both seasons, lysis titers were positively correlated with total densities of microbes shed from birds, suggesting that immune defenses are directed towards the microbes that birds carry, rather than microbes in the wider environment. Our findings highlight the relevance of quantifying non-specific immune challenges in ecological immunology studies, and reinforce the importance of both host-dependent and host-independent measures of antigenic pressure for understanding immune variation.

Seasonal Patterns and Relationships among Coccidian Infestations, Measures of Oxidative Physiology, and Immune Function in Free-Living House Sparrows over an Annual Cycle

“…These results contrast with other studies on wild species, which showed significant sex-dependent change in immunological and oxidative state over the year (Pap et al 2010c;van de Crommenacker et al 2011;Hegemann et al 2012bHegemann et al , 2013Horrocks et al 2012;Rubolini et al 2012). However, most of these studies did not measure change in parasite pressure over the year (but see Horrocks et al 2012), making it difficult to pinpoint a direct association between variation in physiological state and parasite infection. In our study on captive house sparrows, we showed that the number of coccidians varied little over the year, which was somewhat expected because of the limited change in transmission conditions of the infective oocysts in an environment of captivity (Pap et al 2014).…”

“…Several studies have shown that components of the immune system may vary over the year; however, divergent changes were found between species, populations, and physiological traits, with no clear pattern of high and low responses in particular seasons (Møller et al 2003;Buehler et al 2008aBuehler et al , 2012Martin et al 2008;Pap et al 2010bPap et al , 2014Hegemann et al 2012aHegemann et al , 2012bHegemann et al , 2013Horrocks et al 2012). Sex differences in reproductive physiology or parental investment may also affect immune function, the defense capacity of the antioxidant system, and/or the oxidative damage (Alonso-Alvarez et al 2007; Metcalfe and Alonso-Alvarez 2013;Rubolini et al 2012).…”

Bacteria and the evolution of honest signals. The case of ornamental throat feathers in spotless starlings

“…By evaluating traits that reliably signal immune capacity, receivers are able to choose less infected mates with genes conferring pathogen resistance that would be inherited by their offspring (Hamilton & Zuk 1982;Folstad & Karter 1992). Behavioural defences or non-specific innate immune responses, which represent the most important antibacterial barriers (Playfair & Bancroft 2004), are active against a wide range of micro-organisms, likely including those able to degrade signalling traits (Horrocks et al 2012). Thus, the ability of animals to preserve signals against degrading micro-organisms may reflect their defence competence, not only because of the relationship between the exaggeration of signals and associated increase in immune-suppressive hormones in blood (Folstad & Karter 1992), but also because well-maintained, non-degraded structures will inform about the ability to fight degrading microbes (Shawkey, Pillai & Hill 2009;Ruiz de Castañeda et al 2012).…”

Island Life Shapes the Physiology and Life History of Eastern Bluebirds (Sialia sialis)

“…Compared to agglutination titers, haptoglobin concentrations are considerably more labile over short timescales (van de Crommenacker et al 2010;Matson et al 2012aMatson et al , 2012b. A growing body of research explores both indexes in the contexts of avian ecology (Hegemann et al 2012;Horrocks et al 2012b), life history (Palacios et al 2007;Versteegh et al 2012), and geography (Matson 2006;Horrocks et al 2012a). …”