Abstract
Environmental contaminants and parasites are ubiquitous stressors that can affect animal physiology and derive from similar dietary sources (co-exposure). To unravel their interactions in wildlife, it is thus essential to quantify their concurring drivers. Here, the relationship between blood contaminant residues (11 trace elements and 17 perfluoroalkyl substances) and nonlethally quantified gastrointestinal parasite loads was tested while accounting for intrinsic (sex, age, and mass) and extrinsic factors (trophic ecology inferred from stable isotope analyses and biologging) in European shags Phalacrocorax aristotelis. Shags had high mercury (range 0.65–3.21 μg g–1 wet weight, ww) and extremely high perfluorooctanoic acid (PFOA) and perfluorononanoic acid (PFNA) residues (3.46–53 and 4.48–44 ng g–1 ww, respectively). Males had higher concentrations of arsenic, mercury, PFOA, and PFNA than females, while the opposite was true for selenium, perfluorododecanoic acid (PFDoA), and perfluooctane sulfonic acid (PFOS). Individual parasite loads (Contracaecum rudolphii) were higher in males than in females. Females targeted pelagic-feeding prey, while males relied on both pelagic- and benthic-feeding organisms. Parasite loads were not related to trophic ecology in either sex, suggesting no substantial dietary co-exposure with contaminants. In females, parasite loads increased strongly with decreasing selenium:mercury molar ratios. Females may be more susceptible to the interactive effects of contaminants and parasites on physiology, with potential fitness consequences.
Highlights
Wild animals are concurrently exposed to a suite of natural and anthropogenic stressors that can have additive, synergistic, or antagonistic effects on individuals, with potential consequences on populations
There is some evidence of enhanced susceptibility to infection and parasite pathogenicity linked to trace elements (TEs) and perfluoroalkyl substances (PFAS) exposure in multiple taxa.[1,7]
We considered the alternative hypothesis of lower contaminant residues in the most parasitized individuals, since parasites can act as sinks of contaminants and modify their uptake and metabolism in the hosts, especially for nonessential TEs.[2]
Summary
Wild animals are concurrently exposed to a suite of natural and anthropogenic stressors that can have additive, synergistic, or antagonistic effects on individuals, with potential consequences on populations. Contaminant and parasite interactions and their consequences could be severe for apex predators, especially those with diverse and/or flexible foraging strategies, which can cause them to accumulate a wide range of contaminants and trophically derived parasites.[8,9] Contaminant and parasite burdens in these animals are governed by intrinsic and extrinsic factors that drive variation within and between populations and species This is partly due to the way individuals accumulate and respond to these stressors, which can be linked to intrinsic factors, such as sex, age, reproductive status, and body mass. Advances in biologging[19] and analytical techniques such as compound-specific stable nitrogen isotope analyses on amino acids (δ15NAA)[20] can provide detailed, quantitative data on predator feeding strategies Combining these methods, while taking into account sex and other intrinsic traits, is an emerging and powerful approach to quantify co-exposure to contaminants and parasites and better understand their combined effects on individuals and subsequently populations. We considered the alternative hypothesis of lower contaminant residues in the most parasitized individuals, since parasites can act as sinks of contaminants and modify their uptake and metabolism in the hosts, especially for nonessential TEs.[2]
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