Correlates of immune defenses in golden eagle nestlings

Abstract

An individual's investment in constitutive immune defenses depends on both intrinsic and extrinsic factors. We examined how Leucocytozoon parasite presence, body condition (scaled mass), heterophil-to-lymphocyte (H:L) ratio, sex, and age affected immune defenses in golden eagle (Aquila chrysaetos) nestlings from three regions: California, Oregon, and Idaho. We quantified hemolytic-complement activity and bacterial killing ability, two measures of constitutive immunity. Body condition and age did not affect immune defenses. However, eagles with lower H:L ratios had lower complement activity, corroborating other findings that animals in better condition sometimes invest less in constitutive immunity. In addition, eagles with Leucocytozoon infections had higher concentrations of circulating complement proteins but not elevated opsonizing proteins for all microbes, and eagles from Oregon had significantly higher constitutive immunity than those from California or Idaho. We posit that Oregon eagles might have elevated immune defenses because they are exposed to more endoparasites than eagles from California or Idaho, and our results confirmed that the OR region has the highest rate of Leucocytozoon infections. Our study examined immune function in a free-living, long-lived raptor species, whereas most avian ecoimmunological research focuses on passerines. Thus, our research informs a broad perspective regarding the evolutionary and environmental pressures on immune function in birds.

Evolution of heterophil/lymphocyte ratios in response to ecological and life‐history traits: A comparative analysis across the avian tree of life

“…Although innate and adaptive immune systems of vertebrates are not fully independent of each other and there are intricate innate‐adaptive connections in the immune response (Fearon & Locksley, ; Hoebe, Janssen, & Beutler, ), heterophils and lymphocytes are traditionally classified as primary constitutive components of innate and adaptive immune defences, respectively (Lee, ; Palacios, Cunnick, Vleck, & Vleck, ). Although there is empirical evidence for H/L ratios correlating positively with the strength of innate immune response (MacColl et al., ; but see Parejo, Silva, & Avilés, for lack of correlations) and negatively with humoral adaptive response in wild birds (Kerimov et al., ; Krams et al., ), it must be acknowledged that H/L ratio does not measure an immune response per se (Davis et al., ). However, elevated H/L ratios should be associated with a state of readiness to cope with infection through injury (via heterophils) rather than with a communicable disease (via lymphocytes) (Johnstone, Reina, & Lill, ).…”

Introduction to ecoimmunology: An integrative approach

“…Their findings demonstrate that rapid temperature changes constrain immunity in ectothermic vertebrates, which has implications for global climate change (Goessling et al, 2017). Two of the studies in this special issue fall into this final theme but are focused on species of conservation con- and age did not affect immune defenses, eagles with Leucocytozoon infections had higher concentrations of circulating complement proteins but not elevated opsonizing proteins for all microbes, suggesting that some eagles elevate immune defenses because they are exposed to more parasites (MacColl et al, 2017). Similarly, Neuman-Lee et al…”

“…Invertebrate species investigated in this current issue are the bumblebee ( Bombus impatiens ), the weevil ( Curculio sp., Coleoptera), the gallfly ( Eurosta solidaginis , Diptera), and larvae of the lepidopteran Pyrrharctia isabella (Czerwinski & Sadd, ; Ferguson & Sinclair, ). Avian species include the house wren ( Troglodytes aedon ), the golden eagle ( Aquila chrysaetos ), the song sparrow ( Melospiza melodia ), the European starling ( Sturnus vulgaris ), and the zebra finch ( Taeniopygia guttata ) (Bowers, Sakaluk, & Thompson, ; Grindstaff & Merrill, ; Kelly et al., ; MacColl et al., ; Pryor & Casto, ). Reptilian species represented in the current issue are the green anole ( Anolis carolinensis ), the gopher tortoise ( Gopherus polyphemus ), and the snapping turtle ( Chelydra serpentina ) (Beck, Thompson, & Hopkins, ; Goessling et al., ; Tylan & Langkilde, ).…”

“…() examined how Leucocytozoon parasite presence and body condition affected immune defenses in golden eagle populations. While body condition and age did not affect immune defenses, eagles with Leucocytozoon infections had higher concentrations of circulating complement proteins but not elevated opsonizing proteins for all microbes, suggesting that some eagles elevate immune defenses because they are exposed to more parasites (MacColl et al., ). Similarly, Neuman‐Lee et al.…”

Fitness outcomes in relation to individual variation in constitutive innate immune function

“…We measure three immune indices frequently measured in wild animals and known to be important for front-line defences (haptoglobin (Hp), natural antibodies (NAbs), complement activity (CA); [42][43][44]). Although these indices could partly vary as a result of the unknown disease environment of wild animals, they are constitutively maintained and vary among individuals even in the absence of infection [45,46]. Using this approach, we implicitly interpret fitness outcomes as a subsequent consequence of individual variation in the maintenance of immune function.…”