Effects of Maternal Reproductive Investment on Sex-Specific Pollutant Accumulation in Seabirds: A Meta-Analysis

Abstract

Avian egg production demands resources such as lipids and proteins. Relative egg size and mass varies across species, reflecting differences in maternal investment. This variability may affect the maternal transfer of anthropogenic pollutants including lipophilic polychlorinated biphenyls (PCBs) and protein-associated per- and polyfluoroalkyl substances (PFASs) and mercury (Hg). We conducted a meta-analysis on seabirds and investigated whether interspecies variation in maternal investment contributes toward skewed pollutant concentration ratios between males and females, as Cmale/Cfemale (80 studies). Overall concentrations of PCBs and perfluorooctanesulfonic acid (PFOS) were 1.6 and 1.3 times higher, respectively, in males than females, whereas mercury was similar between sexes. Few studies compared females and eggs (n = 6), highlighting a knowledge gap. We found that an increasing maternal investment as a clutch-to-female mass ratio resulted in lower PCB concentrations in females than in males during the incubation period, but no sex-specific differences were observed for mercury and PFOS. Egg production is both a lipid dominated and protein-limited process. Females transfer lipophilic pollutants more easily to eggs, and to a higher degree with increasing maternal investment, but feeding ecology may be more important. Interspecies variation in maternal pollutant transfer may lead to negative effects scaling from an offspring to population level.

Common Eider and Herring Gull as Contaminant Indicators of Different Ecological Niches of an Urban Fjord System

“…This is also in accordance with the remobilization explanation, as Hg is not lipid‐associated and thus not remobilized to the blood stream along with the lipids. Furthermore, protein is thought to be the limiting nutrient in egg production, and maternal transfer is higher for lipophilic than for protein‐associated contaminants (Mallory et al 2004; Hitchcock et al 2019a).…”

“…Our study had the same outcome for lipid weight normalized and wet weight concentrations, and when accounting for lipids as a covariate in the PCA, which indicate robust results. The difference in the lipid content of the eggs of the 2 species may reflect the more precocial breeding strategy of the eiders, which have a greater maternal investment, including investing more lipids in their clutch than the herring gull (Hitchcock et al 2019a). The variable numbers of detected contaminants in the matrices, following the concentration trends, shows that the number of lipophilic OHCs detected does not follow the lipid content of the matrices but is likely more affected by the remobilization of contaminants to the blood stream during incubation in the common eider.…”

“…Egg production reflects the maternal transfer of contaminants from the reproducing mothers to the eggs, and the eggs can reflect female contaminant levels at the time of, or before, egg production (Verreault et al 2006). As a result, contaminants in eggs can originate from contamination at the breeding site and at the overwintering site (Hitchcock et al 2019a). Avian maternal transfer of contaminants vary with several factors, including contaminant properties and life history factors such as migration and lipid dynamics (Verreault et al 2006).…”

“…It is important that species selected for this role represent the monitored ecosystem (Baert et al 2013; Elliott et al 2015). In addition to diet, interspecies differences in physiology and life history traits affecting energy allocation, remobilization of contaminants, and elimination processes affect contaminant concentrations (Borgå et al 2004; Hitchcock et al 2019a).…”

“…Furthermore, species differences in tissue distribution and dynamics of lipids can lead to interspecies differences in contaminant occurrence in the same matrix. For example, differing maternal investment and lipid content in the eggs of 2 species can result in different transfers of contaminants from mother to egg (Hitchcock et al 2019a).…”