Immune response to an endotoxin challenge involves multiple immune parameters and is consistent among the annual-cycle stages of a free-living temperate zone bird

Abstract

SUMMARYTrade-offs between immune function and other physiological and behavioural processes are central in ecoimmunology, but one important problem is how to distinguish a reallocation of resources away from the immune system from a reallocation or redistribution within the immune system. While variation in baseline values of individual immune parameters is well established, studies in wild animals on multiple parameters during an immune response are lacking. It also remains to be tested whether and how immune responses correlate with baseline values that vary, for example, over the course of an annual cycle. We studied immunological responses to an endotoxin challenge in skylarks (Alauda arvensis), a partial migrant bird breeding in temperate zones. We compared birds injected with the endotoxin LPS with un-injected controls, characterizing immunological responses with leukocyte profiles, titres of lytic enzymes and natural antibodies, and concentrations of haptoglobin and heat shock proteins. We did this in five annual-cycle stages to test whether the response varied throughout the year. The endotoxin challenge affected six of 10 measured parameters. Lysis titres and proportions of heterophils increased; haptoglobin concentrations and proportions of lymphocytes, basophils and eosinophils decreased. The variable effects on different immune components demonstrate the complexity of an immune response. We found no evidence that the response differed between annual-cycle stages. The response was independent of baseline measures taken directly upon capture in the field, indicating that birds were facing no immunological ceiling when mounting an immune response. Values of five parameters collected under field conditions were significantly related to values taken under standardized laboratory conditions. We conclude that multiple parts of the immune system are modulated during an immunological response and that responses are not re-organized throughout the annual cycle.Key words: inflammation, ecological immunology, acute phase response, lipopolysaccharide, LPS, annual cycle, birds. Received 20 November 2012; Accepted 8 March 2013The Journal of Experimental Biology 216, 2573Biology 216, -2580Biology 216, © 2013 Nelson, 2004;Hasselquist, 2007;Martin et al., 2008). Immunological mechanisms aimed at avoiding autoimmunity (Råberg et al., 1998) and preventing oxidative stress (Sorci and Faivre, 2009) might further influence this process. Several studies on non-induced (baseline) immune function indeed show that different indices express different seasonal patterns among and within annual-cycle stages (Nelson and Demas, 1996;Buehler et al., 2008b;Pap et al., 2010a;Pap et al., 2010b;Hegemann et al., 2012c). Thus, reorganization of baseline immune function appears to depend on both environmental conditions and competing biotic processes. Data on seasonal variation in induced immune responses are scarce. However, these are the data needed to verify the hypothesis that free-living birds switch from costly inflammatory respo...

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

“…Thus, we found little support for a parasite-mediated change in immune functions and oxidative status. 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.…”

“…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).…”

Immune function and blood parasite infections impact stopover ecology in passerine birds

“…This was expected because natural antibodies are known to be more genetically determined than other immune parameters (Versteegh et al 2014) and do not change during immune challenges (Hegemann et al 2013a). Likewise as predicted, total immunoglobulin levels in circulation, a marker of the constitutive part of acquired immune function that reflects more long-term investment in immune function, was unrelated to stopover duration.…”

Photoperiod but not food restriction modulates innate immunity in an opportunistic breeder,Loxia curvirostra

“…Given that natural antibodies have relatively low developmental, maintenance and use costs (Lee, 2006), are not sensitive as other immune parameters to changes in infection status (Matson et al, 2005), and fluctuate less across the annual cycle in red knots (Buehler et al, 2008) and in free-living red crossbills (Schultz, 2015), it is not surprising that natural antibodies did not respond to LPS injections in the present study. Additionally, despite the fact that increases in haptoglobin activity have been shown in other bird species Hegemann et al, 2013), haptoglobin is only one acute-phase protein that can increase in response to LPSinduced inflammation. Other positive acute-phase proteins such as C-reactive protein (CRP) can activate complement (reviewed in Gruys et al, 2005;Owen-Ashley and Wingfield, 2007), which is involved in mediating hemolysis and E. coli (ATCC 8739) killing ability (Matson et al, 2005;Millet et al, 2007).…”