Sources of variation in innate immunity in great tit nestlings living along a metal pollution gradient: An individual-based approach

Abstract

Excessive deposition of metals in the environment is a well-known example of pollution worldwide. Chronic exposure of organisms to metals can have a detrimental effect on reproduction, behavior, health and survival, due to the negative effects on components of the immune system. However, little is known about the effects of chronic sublethal metal exposure on immunity, especially for wildlife. In our study, we examined the constitutive innate immunity of great tit (Parus major) nestlings (N=234) living in four populations along a metal pollution gradient. For each nestling, we determined the individual metal concentrations (lead, cadmium, arsenic) present in the red blood cells and measured four different innate immune parameters (agglutination, lysis, haptoglobin concentrations and nitric oxide concentrations) to investigate the relationship between metal exposure and immunological condition. While we found significant differences in endogenous metal concentrations among populations with the highest concentrations closest to the pollution source, we did not observe corresponding patterns in our immune measures. However, when evaluating relationships between metal concentrations and immune parameters at the individual level, we found negative effects of lead and, to a lesser extent, arsenic and cadmium on lysis. In addition, high arsenic concentrations appear to elicit inflammation, as reflected by elevated haptoglobin concentrations. Thus despite the lack of a geographic association between pollution and immunity, this type of association was present at the individual level at a very early life stage. The high variation in metal concentrations and immune measures observed within populations indicates a high level of heterogeneity along an existing pollution gradient. Interestingly, we also found substantial within nest variation, for which the sources remain unclear, and which highlights the need of an individual-based approach.

Ambient anthropogenic noise but not light is associated with the ecophysiology of free-living songbird nestlings

“…Such an experimental design (within-individual design with an additional control group) is very powerful to detect possible differences caused by our treatment. Moreover, under natural conditions such as in our current study, the variation in Hp and NOx (amongst other physiological markers) among nestlings of the same nest is higher within the same nest than among nests 40 . This might increase the difficulty of detecting an effect of pollutants which occurs at the nest level 40 .…”

“…Moreover, under natural conditions such as in our current study, the variation in Hp and NOx (amongst other physiological markers) among nestlings of the same nest is higher within the same nest than among nests 40 . This might increase the difficulty of detecting an effect of pollutants which occurs at the nest level 40 . Here we have found that noise was associated with higher levels of Hp.…”

“…Following earlier research on great tits, we determined nestling sex (from red blood cells) and quantified Hp and NOx concentrations (from blood plasma) 36, 40, 41 . Nestling sex was determined genetically 42 .…”

Ground Squirrel Shooting and Potential Lead Exposure in Breeding Avian Scavengers

“…Recent research has shown that Pb can be maternally transferred to avian embryos resulting in inhibited blood delta-aminolevulinic acid dehydratase activity, negative immune responses, and increased oxidative stress levels [57]. Nestling exposure to Pb in their diet can also result in negative effects on immune parameters [67], lower hemoglobin levels [68], less vigorous food-acquisition behaviors and poor coordination [2], among other effects. Furthermore, adult facultative and obligate avian scavengers also scavenge dead ground squirrels [25–27] and would be exposed to lead during the breeding season.…”

Selecting the right bird model in experimental studies on endocrine disrupting chemicals

“…Furthermore, starlings have also been used in exposure studies for EDCs, both in outdoor aviaries (Van den Steen et al, 2009) as well as exposure of nestlings in the field and subsequent transfer to the laboratory (Eng et al, 2014). Other passerines that have often been used in linking exposure to effects in a field context are great tits (Parus major), pied flycatchers (Ficedula hypoleuca), and tree swallows (Tachycineta bicolor) (see for example Rainio et al, 2013;Gilchrist et al, 2014;Cruz-Martinez et al, 2015a;Vermeulen et al, 2015).…”