As intensive research on microplastics enters its second decade, the issue of plastic pollution has emerged alongside climate change as one of the most pressing environmental challenges. Plastic waste is predicted to increase exponentially out to 2050 and beyond (Borrelle et al., 2020), and scientists have recently called for a cap on virgin plastic production by 2040 (Bergmann et al., 2022). The ocean continues to be a sink for microplastic pollution, and is now documented to be a secondary source of microplastics to atmospheric and terrestrial ecosystems as well (Allen et al., 2020). Marine organisms are exposed to this complex suite of microplastic pollutants (Rochman et al., 2019) via water, sediment, and consumption of prey items, with a sizeable portion of these microscopic particles tracked back to stormwater, road wear, and laundering/waste treatment practices (Brahney et al., 2021; Brander et al., 2021; Miller et al., 2021; Ross et al., 2021; Granek et al., 2022). The impacts of microplastics on organisms are diverse and dependent partially on trophic level and life history, but the mechanisms of toxicity most consistently observed include (1) food dilution, resulting in reduced nutrient absorption and thus reduced growth, and (2) oxidative damage caused by small microplastics that can potentially translocate between organs of the organisms that ingest or inhale them (Jacob et al., 2020; Mehinto et al., 2022; Thornton Hampton et al., 2022). Microplastic presence has been demonstrated in many marine organisms, particularly those consumed as seafood (Li et al., 2019; Baechler et al., 2020a), but also in wild zooplankton that form the base of many marine trophic webs (Desforges et al., 2015; Botterell et al., 2022). Given that lower trophic level organisms are estimated to ingest higher levels of microplastics (Walkinshaw et al., 2020) and that microplastics-driven food dilution is occurring across organisms of all sizes (Siddiqui et al., 2022), investigations of microplastic loads in zooplankton and their potential impact on food webs are critical to more comprehensively understand ecological impacts.

The Pacific Northwest (PNW) seaboard of North America is an important habitat for a variety of ecologically important marine species, including gray whales (Eschrichtius robustus) that use the coastal region as a foraging ground from June through October each year (Calambokidis et al., 2019). Although much of the PNW coast is relatively pristine compared to more industrialized regions, microplastics have been confirmed in a number of different sample types collected in the region (Baechler et al., 2020b; Harris et al., 2021; Talbot et al., 2022; Lasdin et al., 2023). The majority of these microplastics are fibers, which aligns with other studies globally (Athey and Erdle, 2021; Granek et al., 2022). Given that fibers may be more toxic than other polymer shapes (Stienbarger et al., 2021; Mehinto et al., 2022), this abundance of fibers is of great concern, especially for zooplankton which form the base of marine food webs and are a primary dietary component for marine mammals including gray whales. [Hereafter we refer to microplastics as microparticles (MPs) given that not all microparticles are synthetic in composition, as recommended in (Miller et al., 2021; Lasdin et al., 2023)].

Zooplankton are important to multiple predator types, including invertebrates, fish, seabirds, and marine mammals that depend on their abundance to support their energetic demands. Therefore, trophic transfer of MP and the potential for bioaccumulation of associated contaminants from zooplankton through the food web is a significant concern (Nelms et al., 2018; Zantis et al., 2021). In the coastal region of Oregon, USA, zooplankton are key species in the nearshore ecosystem where they form the food base for commercially and recreationally harvested fish (Bosley et al., 2014) and gray whales during their ~6 month foraging season (Torres et al., 2018; Hildebrand et al., 2021). Fishing and whale watching in coastal Oregon play critical economic and food resource roles for coastal communities (O'Connor et al., 2009; Cramer et al., 2018). Thus, it is important to understand the rates and variability of MP loads in this coastal food web to establish baselines, identify species or areas of concern, and inform next steps of research and management to reduce harmful impacts of MP on wildlife populations and human communities.

Baleen whales are mega-filter feeders that engulf large amounts of ambient water while consuming their target prey. This feeding method exposes baleen whales to both direct ingestion of MP from ambient water, and indirect MP ingestion via consumption of contaminated prey through trophic transfer (Germanov et al., 2018; Zantis et al., 2021). Gray whales are a unique lineage of baleen whales, as they use suction feeding (rather than ram or lunge feeding; Goldbogen et al., 2017) to feed benthically on zooplankton and amphipods. Thus, gray whales frequently ingest benthic substrate (e.g., mud, sand, shell) while feeding in addition to ambient water and prey items, which may increase this taxa’s MP exposure. This study focuses on the Pacific Coast Feeding Group (PCFG) of gray whales, which is a small sub-group (abundance estimated to be 230 individuals) of the larger Eastern North Pacific (ENP) population of gray whales that migrate from breeding grounds in Baja California, Mexico to the Arctic where they feed (Rice and Wolman, 1971). The PCFG diverges from this migration pattern by foraging in coastal habitats from northern California, USA, to southern British Columbia, Canada (Calambokidis et al., 2002). PCFG whales are generalist feeders, foraging in nearshore areas <20 m (Hildebrand et al., 2021) with primary prey in our study region of coastal Oregon, USA being benthic and epibenthic mysids and amphipods (Hildebrand et al., 2021; Hildebrand et al., 2022).

Research on cetacean exposure to MPs is still in its relative infancy, especially on baleen whales. MPs have been found in the gastrointestinal tract of one humpback whale (Megaptera novaeangliae, Besseling et al., 2015) and in the blubber of fin whales (Balaenoptera physalus; Fossi et al., 2012; Fossi et al., 2014). Additionally, fin whale foraging grounds in the Mediterranean Sea were found to have high spatial overlap with areas containing elevated densities of microplastics (Fossi et al., 2016; Fossi et al., 2017). A recent study quantified MP ingestion rates of Bryde’s (Balaenoptera edeni brydei) and sei (Balaenoptera borealis) whales that feed on pelagic zooplankton in the Hauraki Gulf of New Zealand (Zantis et al., 2022). These initial studies demonstrate baleen whale exposure to MPs and the potential for negative consequences, including sub-lethal individual level effects that may impact energetic gains and health (Nelms et al., 2018). MPs can impact whales and other marine mammals by blockage of internal organs, mechanical damage of digestive tract, false feeling of satiation, and potentially leaching of toxicants depending on the length of the digestive period (Donohue et al., 2019; Hudak and Sette, 2019; Zhu et al., 2019; Novillo et al., 2020). These impacts could reduce an individual’s overall resilience to injury and disturbance, reproductive capacity, and possibly even survival. While it is critical to consider the population level effects of MP exposure to cetacean populations for a holistic and cumulative assessment of risks, we must first reliably estimate individual MP exposure rates and understand these impacts on vital rates.

Despite the likelihood of high MP ingestion by baleen whales, there remains a paucity of studies on rates of ingestion or impacts, likely due to the inherent challenges of ethically and effectively sampling such a large, free ranging, marine animal. However, fecal sample collection is effectively used to non-invasively assess hormone variation from baleen whales (Hunt et al., 2013; Lemos et al., 2020a) and recently to estimate MP ingestion rates (Zantis et al., 2022). Here, we quantify MP loads in Oregon coastal zooplankton, including from within primary PCFG gray whale foraging habitat and their known target prey species, and we extrapolate these findings to estimate the daily MP ingestion rates of gray whales based on energetic demands. As a case study of trophic transfer, we also conduct MP analysis of fecal samples collected from several PCFG gray whales feeding in the same spatio-temporal area. We hypothesize that MPs with similar characteristics will be detected in both sample types. To our knowledge, this study is the first to look at MP exposure of baleen whales from “zoop to poop” and to quantify baleen whale MP consumption rates from empirically counted MP loads in zooplankton prey (i.e., not modeled). Our results further develop the understanding of MP loads in marine ecosystems across trophic levels.

Our estimated daily consumption of MPs by a pregnant or lactating PCFG gray whale is astounding, ranging between 6.45 and 21.2 million, especially when considering that a gray whale’s foraging season lasts ~6 months (180 days). Although this amount may appear to be an overestimate, it is aligned with the modeled estimates for other baleen whales that target zooplankton, such as Kahane-Rapport et al. (2022); a blue whale consumes 10 million MP per day) and Zantis et al. (2022) that estimated Bryde’s and sei whales consume 3.4 million MP per day (95% CI: 295,810 – 10,031,370). Blue, Bryde’s, and sei whales are all pelagic feeding whales rather than benthic feeding like gray whales. While MPs are commonly detected in surface water and throughout the water column, it is widely documented that the benthos is the biggest sink for marine MPs due to weathering and aggregation processes that increase particle density over time (Bergmann et al., 2017; Zhang, 2017; Shupe et al., 2021). Additionally, we produced estimates for the most energetically demanding life history phases of pregnant and lactating females. However, our estimates are derived from MP loads found in the main prey items of gray whales and do not account for MP ingested due to consumption of either ambient water or benthic sediments. Therefore, it is possible that the actual daily consumption rate of MP by gray whales during these sensitive life history stages is higher.

The differences in morphology and size of MPs found in the zooplankton and fecal samples are interesting. We theorize that these differences may be due to (1) the gape size limitation of zooplankton compared to whales, and (2) ambient consumption by benthically feeding gray whales of the heavier and larger MPs that are primarily found in the benthos (Zhang, 2017). Although the large mesh size (300 μm) of the net used to collect fecal samples may have under sampled smaller MPs, our protocols for zooplankton assessment (immediate digestion and filtration) would have collected larger MPs had they been present. Therefore, the finding of larger MPs in gray whale fecal samples than their zooplankton prey is likely accurate. Also, given that the amount of anthropogenic cellulosic material (e.g., cotton) was similar between whales and zooplankton, we do not think that the coffee filters (identified as cellulose via FTIR) added any contamination to the fecal samples.

The majority of MPs found in zooplankton were smaller fibers (<2 mm), which are likely more easily ingestible compared to larger items. While whale fecal samples also contained fibers, there was also a large amount of films, fragments, and pellets. The sea water blanks we collected at the surface were dominated by fibers with few films and fragments, indicating that the heavier and larger MPs may sink faster and accumulate in the benthos (ter Halle et al., 2016). This difference in sinking rates has also been widely documented in the literature (Horton and Dixon, 2018). Fibers also eventually sink to the bottom once weathered (Woodall et al., 2015). Therefore, we hypothesize that gray whales are exposed to MPs via trophic transfer from their zooplankton prey and indiscriminate consumption of ambient MPs in the benthos while foraging benthically ( Figure 4 ). Yet our estimated daily MP consumption rates are only based on prey ingestion and therefore are likely conservative.

Gray whales feeding in this region use variable foraging tactics to feed on a variety of prey (Torres et al., 2018; Hildebrand et al., 2021), which may explain the variation in MP types within fecal samples and also implies that the “composite prey” estimate of daily MP consumption ( Table 1 ) may be the most realistic to consider MP exposure across a whole foraging season. While the examination of MP morphotypes and size in fecal samples is useful, we do not attempt to calculate MP loads or consumption rates based on the fecal samples due to several reasons. We only collected a small and unknown portion of each fecal plume, so the estimation of MP consumption rate is fraught. Furthermore, whale fecal samples were collected using a 300 um net that may not have retained smaller MP types and sizes. Additionally, in contrast to the zooplankton samples which were processed under HEPA in a laminar flow hood, contamination of fecal samples may have occurred because we used plastic jars to store these samples and HEPA filters were not used during initial step of sample filtration through a coffee filter (HEPA was used for additional processing steps that followed). Thus, the five fecal samples analyzed in this study represent a pilot effort to better understand MP morphotype and sizes consumed, and as a proof of methods.

The predominance of microfibers in zooplankton species consumed by PCFG gray whales is concerning as evidence is accumulating across taxa that fibers may be more toxic and more difficult to excrete than other MP types (Stienbarger et al., 2021; Bucci and Rochman, 2022; Granek et al., 2022; Thornton Hampton et al., 2022). Although evidence of fiber impacts in megafauna such as whales is lacking, it could be predicated that fibers are similarly problematic. Further, the accumulation and internalization of microfibers by zooplankton likely impacts other important coastal species in addition to whales. The same zooplankton species are commonly fed upon by salmonids and other fishes commonly consumed by humans. Concerningly, a recent study focused on Oregon seafood species found that microfibers are common in the fillet tissue of salmonids, lingcod, herring (Brander pers. obs.), and in the fillet and gut of rockfish (Lasdin et al., 2023) frequently consumed by humans. Additionally, our estimates of MPs in zooplankton are likely also conservative, since current microscopy and FTIR approaches are limited to the detection of MPs > 20 microns in size (Cowger et al., 2020).

Although this study provides a first, baseline estimate of MP consumption by gray whales, there are many necessary next steps. Methodologically, whale fecal samples should be collected with a smaller mesh net and processed in a more controlled manner to minimize contamination. This added control would provide more robust estimates of MP types consumed, yet abundance estimates of MP consumption rates will remain challenging without estimates of the fecal sample proportion collected. More importantly though, is to extend these and other findings on the high rates of MP consumption by baleen whales to assess the population level impacts on the health of individuals and subsequent scaled-up effects on population dynamics (Senko et al., 2020). MP consumption may significantly impair the fitness of individuals through multiple pathways (e.g., reduced energetic gain, increased pollutant loads, organ damage), which may have long-term impacts across a population if reproductive capacity and calf survival is negatively impacted. Additionally, the impacts of MPs on zooplankton prey are also unknown; zooplankton with unsustainable levels of MP ingestion may not survive or reproduce as well as less contaminated individuals, and these impacts would have prey availability consequences to whales. Therefore, much more research is needed on the physiological impacts of MP ingestion on both zooplankton prey and whale predators. While our study demonstrates the potential for alarming rates of MP consumption by gray whales, it is also important to recognize that MP exposure is just one of many threats whales face in an increasingly anthropogenically impacted ocean. Hence, it is the cumulative impacts of these threats that must be holistically evaluated and managed to truly sustain and improve the health and viability of whale populations.

The original contributions presented in the study are included in the article and Supplementary Material . Further inquiries can be directed to the corresponding author.

The animal study was reviewed and approved by Oregon State University Animal Program Office.

LT, SB, and LH contributed to conception and design of the study. LT led field work and sample collection. SB oversaw laboratory analysis, which LH led with assistance from JP, EB, RN, JVB, and KL. LH conducted statistical analyses. LT wrote the first draft of the manuscript, with contributions from SB and LH. All authors contributed to manuscript revision, read, and approved the submitted version. Project funding was acquired and managed by LT.