Limited reproductive impairment in a passerine bird species exposed along a perfluoroalkyl acid (PFAA) pollution gradient

Abstract

Although bird eggs have been used in biomonitoring studies on perfluoroalkyl acids (PFAAs), effects of environmental concentrations on reproduction remain largely unknown in wild birds. In the present study we examined the associations between the concentrations of 4 perfluoroalkyl sulfonic acids (PFSAs) and 11 perfluoroalkyl carboxylic acids (PFCAs) in the eggs of great tits (Parus major), collected along a distance gradient from a pollution source, and multiple reproductive parameters (including the start of egg laying, clutch size, hatching success, fledging success and total breeding success) along with egg shell thickness and body condition of the nestlings.The PFAA concentrations measured at the plant site were among the highest ever reported in wild bird eggs. PFAA concentrations decreased sharply with increasing distance (0 -11 km) from the plant, but remained relatively elevated in the adjacent sites. PFAAs were grouped into principal components (PCs) to prevent collinearity. High concentrations of PFOS, PFDS, PFDoDA, PFTrDA and PFTeDA (grouped as PC1) were associated with a reduced hatching success of nests where at least one egg hatched, thinner egg shells and increased survival of the hatched chicks. High concentrations of PFDA (PC2) were associated with a reduced hatching success, especially in nests where no eggs hatched, an earlier start of egg laying and a reduction of total breeding success, mainly caused by the failure in hatching.Although the major manufacturer of PFAAs phased out the production of perfluorooctane sulfonate (PFOS), perfluorooctanoic acid (PFOA) and related products in 2002, concentrations appear to have increased since previous measurements. Surprisingly, despite the very high concentrations close to the fluorochemical plant, there was no clear evidence for reproductive impairment as the observed associations between PFAA concentrations and reproductive parameters were rather limited compared to previous studies in songbirds. These findings also suggest potential differences in sensitivity between species.

Linking field and laboratory studies: Reproductive effects of perfluorinated substances on avian populations

“…No association was found between reproduction and total PFAS concentrations in eggs (Custer et al 2019; Figure 3) despite much higher exposure to total PFAS. This lack of an effect at very high PFAS concentrations was similar to a study of great tits in Belgium where there was only a slight reduction in hatching success in nests that hatched at least one egg (successful nests) at their site near a fluorochemical plant (Groffen et al 2019). Perfluorooctane sulfonate exposure in that study was 50 times higher in eggs at the site nearest the plant (34 251 ng/g wet wt) than present at Wurtsmith, the site with the highest known exposure in North America (Custer et al 2019).…”

“…Although many studies document exposure to PFASs in birds (see review in Ankley et al 2021), there are still relatively few field, or even laboratory, studies on PFAS reproductive effects when compared to other contaminants, such as polychlorinated biphenyls (PCBs), mercury (Hg), and p,p ‐DDE. Field reproductive effect studies on PFASs include studies on tree swallows ( Tachycineta bicolor ; Custer et al 2012, 2014, 2017, 2018, 2019), black‐legged kittiwakes ( Rissa tridactyla ; Tartu et al 2014), great tits ( Parus major ; Groffen et al 2019), and lesser black‐backed gulls ( Larus fuscus ; Bustnes et al 2008).…”

“…Two field studies (Custer et al 2012, 2014; Figures 1 and 2) using tree swallows found a significant negative association with perfluorooctane sulfonate (PFOS) and hatching success with numerous total clutch failures becoming prevalent at around 150 ng/g wet weight (wet wt) PFOS in eggs. Another set of field studies (Tartu et al 2014; Custer et al 2019; Groffen et al 2019), however, which included one on tree swallows but also on other avian species, found few or no reproductive effects. A field study with tree swallows, conducted at the former Wurtsmith Air Force Base, Oscoda, Michigan, USA, hereafter called “Wurtsmith,” reported considerably higher PFAS exposure (geometric means in eggs between 554 and 954 ng/g wet wt and a maximum concentration of 1781 ng/g) than was found in the two previous tree swallow studies.…”

Assessing the Ecological Risks of Per‐ and Polyfluoroalkyl Substances: Current State‐of‐the Science and a Proposed Path Forward

“…One key challenge in conducting field studies lies in endpoint selection. Endpoints reported from studies on avian species have covered a range from suborganismal responses, including biomarkers and measures of oxidative stress (e.g., Blévin et al 2017a, 2017b; Lopez‐Antia et al 2017, 2019), to effects related to reproductive success such as eggshell thinning (Miljeteig et al 2012) and hatching success (e.g., Tartu et al 2014; Custer et al 2019; Groffen et al 2019). The avian studies that have included measures of reproductive success are especially valuable given the clear link between reproduction and potential population‐level impacts.…”

Spatiotemporal Analysis of Perfluoroalkyl Substances in White-Tailed Eagle (Haliaeetus albicilla) Nestlings from Northern Norway—A Ten-Year Study

“…64 In great tits (Parus major), high concentrations of PFAS interfered with reproduction success, by failure in hatching in particular. 65,66 Conversely, some studies found no consequences of PFAS concentrations on wild birds.…”