Pollutant Exposure Shapes Mitochondrial Bioenergetics in a Wild

Overview

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Key numbers

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“Mannarazza” (Figure 1b). We investigated a total of 52 adults (n =
resource partitioning.39 Moreover, unlike mammals, birds retain 21 in 2020 and n = 31 in 2021), capturing them in their nests at night
into 1 mL of cold Mir05 buffer for washing, which contained 0.5 mmol was 0.005 μg g−1 dw. Results are given in μg g−1 dw as means ± SD.
at pH 7.1. To minimize contamination with other blood cells, the RBC shearwaters (females n = 12, males n = 9) in 2020 only. The PFAS
inhibiting ATP synthase through the addition of 1 μg mL−1 oligomycin. methanol containing 1% ammonium formate (w/v) was added.
CMR respiration: (LEAK/CMR). All measurements were normalized corresponding lowest value (see Table S1 for the detection limits of
2.4. Hg and Stable Isotope Analyses We analyzed variation in contaminant levels using an LMM for Hg and
2020 (females n = 12, males n = 9) and 2021 (females n = 17, males n =
13C or 15N = ((R sample/R standard) 1) × 103 ICC.47 All analyses were performed in R 4.3.248 using lme449 and plots
relative SD < 10%. Measurement quality was assessed by the certified
values were 0.301 ± 0.003 (n = 24). Blanks were analyzed regularly at shearwaters, stratified by sex and summarized using descriptive
Table 1. Estimates Derived from (a) a LMM for Mercury (Hg) Concentrations (ng mg−1) and from (a, b) GLMM (Gamma
β (95% CrI)a pb β (95% CrI)a pb
regression lines are shown as a thick line with shaded 95% CrI areas. In (b), predicted means are plotted as solid shapes and 95% CrI is indicated by
statistics (sample size, mean ± SD, median, minimum, and 3.1. Variation of Hg and PFAS Concentrations in Relation to
maximum values) (Supporting Information, Table S1). Addi-
with sex, age, and body mass based on models that exclude concentrations and age (Table 1a and Figure 2a). Males also
showed higher Hg concentrations than females (Table 1a and
Figure 2b). In contrast, we found no meaningful associations
Table 2. Effect of δ15N and δ13C on (a) Mercury (Hg) (ng/mg) and (b) Σ PFAS (ng/g) Concentrations Measured in Blood
β (95% CrI)b pc β (95% CrI)b pc
the body mass (Table 1a). Similarly, Σ PFAS concentrations The limited variation in δ13C, likely reflecting the restricted
statistically meaningful (Table 1b). (Supporting Information: Figure S2) indicate redundant dietary
and either δ15N or δ13C (Table 2b). PFAS levels influence mitochondrial bioenergetic traits
3d and Figure 3a), while no meaningful associations were position and foraging habitat use, as these factors can influence
ETS, or FCR1 (Table 3a−c,e, respectively). We observed no for Hg and specific PFAS compounds but not for summed
mitochondrial bioenergetic traits (Table 4). However, when PFHXS, PFNA, PFDODA, PFOA, PFHPS, PFDA) meaningfully
negatively associated with LEAK (Table 5 and Figure 3bi). were positively associated with LEAK respiration (Figure 2),
with LEAK but also with FCR1 (Table 5 and Figure 4). PFDA mitochondrial inefficiency in producing ATP. To the best of
was negatively associated with LEAK and CMR (Table 5 and our knowledge, this is the first study to explore the potential
LEAK but also with FCR1, CMR, and ETS (Table 5 and Figure exposure, and stable isotope signatures in wild animals. Below,
3.4. Relationships between SIs Related to Hg Exposure and mean (±sd) concentration of 4.91 ± 1.90 μg g−1 (range: 1.91−
δ15N was associated with higher LEAK (Table 6d and Figure 6a) reported in feathers and livers of other Mediterranean
and FCR1 levels (i.e., mitochondrial inefficiency) (Table 6e and seabirds,34 even though those tissues typically accumulate
were also evident, with CMR (Tables 3a and 6a), OXPHOS (range: 1.41−2.40 μg g−1).52 Further, the Hg concentrations
Table 3. Comparison of Linear Mixed-Effects Models: Estimates of the Effect of Hg Concentrations (μg g−1) on Mitochondrial Bioenergetic Traits in Blood Samples of Adult
β (95% CrI)a pb β (95% CrI)a pb β (95% CrI)a pb β (95% CrI)a pb β (95% CrI)a pb
0.001, **p < 0.01, and *p < 0.05. Note that we did not calculate p-values for effects whose CrI overlapped zero. cScaled/centered around the mean.
95% CrI areas. Female data points are presented in yellow and male in blue.
documented with concentrations of 7.7 ± 3.6 μgg−1 (range: on δ15N and did not pursue additional analyses linking δ13C to
ranged from 7.42‰ to 9.98‰, indicating some trophic mitochondrial efficiency in coupling oxygen respiration to
diet, including pelagic fish, crustaceans, and cephalopods,37,55 did not result in a meaningful change in overall mitochondria

Methods (brief)

hypothesized that contaminant concentrations would be recorded nest sites. After capture, we collected a blood sample of a
a 25-gauge needle. We only considered blood samples taken within 5
associated with increased LEAK respiration, reflecting mito- samples were immediately transferred into heparinized tubes and kept
production. Given the biphasic nature of PFAS effects (mean blocks, one at the bottom and one on top of the samples. Based on our
exposures acting as uncouplers that increase LEAK, and high experience, this setup effectively maintains samples at a low and stable
at the concentrations of PFAS expected for this population; (4) to the lab, the samples were centrifuged at 2000 g (relative centrifugal
Orobos Instruments, Innsbruck, Austria). The RBCs were transferred the beginning of each working unit, and the limit of detection (LoD)
sample was collected from the bottom of the tube. The cells were analyses were carried out at the NTNU Trondheim, Norway. Standards
Austria). Mitochondria respiration was quantified as oxygen (O2) detection limits is presented in Michel et al.13 Sample extraction
the coupling of respiration with ATP production relative to the maximal for the target analytes in the samples, and are reported in ng g−1 dry
carbon and nitrogen were measured in freeze-dried RBCs sampled in
peptone (Sigma-Aldrich), were analyzed together with the samples,
13C or 15N = ((R sample/R standard) 1) × 103 ICC.47 All analyses were performed in R 4.3.248 using lme449 and plots
A sample amount of 0.2−0.8 mg (mean 0.4 mg) of freeze-dried RBCs provided in the Supplementary Methods.
was analyzed using an Advanced Mercury Analyzer spectrophotometer
(Altec AMA 254). Each sample was measured 2−3 times until having a 3. RESULTS
whose certified Hg concentration was 0.292 ± 0.022, and our measured as values of SIs (δ15N and δ13C), in blood samples of Scopoli’s
statistics (sample size, mean ± SD, median, minimum, and 3.1. Variation of Hg and PFAS Concentrations in Relation to

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The five most recent substantive edits to this page, classified major (evidence or structure moved), correction (a published value or statement was wrong and has been fixed), or minor (narrative rewritten without changing the underlying evidence). Each description is derived from what the edit did to this page; the linked commit is the authoritative record, routine regeneration passes are excluded, and the full version history lives in git. When DOI minting comes online (see schema docs), each entry below will also link to a version-pinned DataCite DOI.

Commit	Date	Change	Description
b01ec52c	2026-08-04	major	2 sections added
d49e450f	2026-08-03	major	5 sections added; narrative text revised