Extraordinary levels of per- and polyfluoroalkyl substances (PFAS) in vertebrate animals at a New Mexico desert oasis: multiple pathways for wildlife and human exposure

Abstract

Per- and polyfluoroalkyl substances (PFAS) threaten human and wildlife health, but their movement through food webs remains poorly understood. Contamination of the physical environment is widespread, but particularly concentrated at military installations. Here we measured 17 PFAS in wild, free-living mammals and migratory birds at Holloman Air Force Base (AFB), New Mexico, USA, where wastewater catchment lakes form biodiverse oases. PFAS concentrations were among the highest ever reported in animal tissues, and high levels have persisted for at least three decades. The hazardous long carbon-chain form, perfluorooctanosulfonic acid (PFOS), was most abundant, with liver concentrations averaging tens of thousands of ng/g wet weight (ww), reaching as high 97,000 ng/g (ww) in a 1994 specimen of white-footed mouse (Peromyscus leucopus) and 38,000 ng/g ww in a duck, the American wigeon (Mareca americana). Perfluorohexanesulfonic acid (PFHxS) averaged thousands of ng/g ww in the livers of birds and house mice, but one order of magnitude lower in the livers of upland desert rodent species. PFAS levels were strikingly lower at control sites, even for highly mobile migratory species. Tissue concentrations were correlated within individuals, and consistently higher in liver than in muscle or blood. Twenty of 23 vertebrate species sampled at Holloman AFB were heavily contaminated, representing multiple trophic levels and microhabitats, and implicating a range of pathways for PFAS spread: ingestion of surface water, sediments, and dust; foraging on aquatic invertebrates and plants by secondary consumers; and preying upon small vertebrates by higher level consumers, including consumption of game species by hunters. Unlike in other aquatic systems, piscivory was not an important pathway of PFAS uptake. In sum, legacy PFAS at a desert wetland have permeated the local food web across a period of decades, severely contaminating resident and migrant animals, and likely exposing humans via game meat consumption and outdoor recreation. Five highlightsO_LIA biodiverse, wetland food web at a military base is heavily contaminated with PFAS. C_LIO_LILittoral-zone mice and aquatic birds had high liver PFOS, up to 97,000 ng/g ww. C_LIO_LISpecies and ecological variation were high among 16 PFAS detected in animal tissues. C_LIO_LIGame species had dangerously contaminated meat and can transport it long distances. C_LIO_LIBiorepositories provide key temporal and spatial sampling for contaminant studies. C_LI Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=130 SRC="FIGDIR/small/561778v1_ufig1.gif" ALT="Figure 1"> View larger version (75K): org.highwire.dtl.DTLVardef@96a640org.highwire.dtl.DTLVardef@7cd7f4org.highwire.dtl.DTLVardef@45fb67org.highwire.dtl.DTLVardef@7c33a4_HPS_FORMAT_FIGEXP M_FIG C_FIG