skip to main content


Title: Heterotrophic Dinoflagellate Growth and Grazing Rates Reduced by Microplastic Ingestion
Microplastics are ubiquitous contaminants in marine ecosystems worldwide, threatening fisheries production, food safety, and human health. Ingestion of microplastics by fish and large zooplankton has been documented, but there are few studies focusing on single-celled marine predators, including heterotrophic dinoflagellates. In laboratory experiments, the heterotrophic dinoflagellate species Oxyrrhis marina and Gyrodinium sp. readily ingested both algal prey and polystyrene microplastic spheres (2.5–4.5 μm), while Protoperidinium sp. did not ingest microplastics. Compared to algae-only fed dinoflagellates, those that ingested microplastics had growth rates reduced by 25–35% over the course of 5 days. Reduced growth resulted in a 30–50% reduction of secondary production as measured as predator biomass. Ingestion rates of algal prey were also reduced in the microplastic treatments. When given a mixture of microplastics and algal prey, O. marina displayed a higher selectivity for algal prey than Gyrodinium sp. Observations in the coastal ocean showed that phylogenetically diverse taxa ingested microplastic beads, and thus heterotrophic dinoflagellates could contribute to trophic transfer of microplastics to higher trophic levels. The results of this study may suggest that continued increase in microplastic pollution in the ocean could lead to reduced secondary production of heterotrophic protists due to microplastic ingestion, altering the flow of energy and matter in marine microbial food webs.  more » « less
Award ID(s):
1736635 1655686
NSF-PAR ID:
10333561
Author(s) / Creator(s):
;
Date Published:
Journal Name:
Frontiers in Marine Science
Volume:
8
ISSN:
2296-7745
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Microplastics are ubiquitous in marine systems; however, knowledge of the effects of these particles on marine fauna is limited. Ocean‐borne plastic debris accumulates in littoral ecosystems worldwide, and invertebrate infauna inhabiting these systems can ingest small plastic particles and fibers, mistaking them for food. We examined the effect of microplastic fibers on physiological and reproductive outcomes in a nearshore organism by exposing Pacific mole crabs (Emerita analoga) to environmentally relevant concentrations of microsized polypropylene rope fibers. We compared adult gravid female crab mortality, reproductive success, and embryonic developmental rates between microfiber‐exposed and control crabs. Pacific mole crabs exposed to polypropylene rope had increased adult crab mortality, and decreased retention of egg clutches, causing variability in embryonic development rates. These effects of microplastic ingestion on a nearshore prey species have implications for predators such as surf perf and shore birds, as plastic use, and resultant microplastic presence in nearshore environments increases. Microplastics are ubiquitous in marine and sandy beach environments, posing a significant threat to the marine organisms that reside therein. The most predominant classification of microplastics found have been microfibers. Although a number of biological effects of microplastics have been measured, with documented effects on growth, little research has examined how microplastic fibers affect reproductive output and subsequent development of offspring. We examined the effects of exposure to microfibers on adult mortality, reproductive output, and embryonic development of the filter feeding Pacific mole crab (E. analoga), a dominant infaunal organism on sandy beaches. We demonstrate the effects of microplastic ingestion on mole crab mortality and embryonic development, filling a gap in the current knowledge on the impact of microplastics.

     
    more » « less
  2. Abstract

    Microplastics are of increasing concern as they are readily ingested by aquatic organisms. This study investigated microplastic trophic transfer using larval inland silversides (Menidia beryllina) (5 d posthatch) and unicellular tintinnid (Favellaspp.) as a model food chain relevant to North American estuaries. Low‐density polyethylene microspheres (10–20 μm) were used to compare direct ingestion of microplastics by larval fish and trophic transfer via tintinnid prey. Dichlorodiphenyltrichloroethane (DDT)‐treated microspheres were used to determine sorbed pollutant effects on microplastic ingestion. Larval fish exposed directly to microspheres ingested significantly fewer than those exposed via contaminated prey. Larvae ingested significantly more ciliates containing DDT‐treated microspheres than ciliates containing untreated plastics but did not discriminate when exposed directly. Larvae reared for 16 d following a direct 2 h exposure had significantly lower wet weight values than unexposed controls. Our results demonstrate that trophic transfer is a significant route of microplastic exposure that can cause detrimental effects in sensitive life stages.

     
    more » « less
  3. Abstract In the global ocean, more than 380 species are known to ingest microplastics (plastic particles less than 5 mm in size), including mid-trophic forage fishes central to pelagic food webs. Trophic pathways that bioaccumulate microplastics in marine food webs remain unclear. We assess the potential for the trophic transfer of microplastics through forage fishes, which are prey for diverse predators including commercial and protected species. Here, we quantify Northern Anchovy ( Engraulis mordax ) exposure to microplastics relative to their natural zooplankton prey, across their vertical habitat. Microplastic and zooplankton samples were collected from the California Current Ecosystem in 2006 and 2007. We estimated the abundance of microplastics beyond the sampled size range but within anchovy feeding size ranges using global microplastic size distributions. Depth-integrated microplastics (0–30 m depth) were estimated using a depth decay model, accounting for the effects of wind-driven vertical mixing on buoyant microplastics. In this coastal upwelling biome, the median relative exposure for an anchovy that consumed prey 0.287–5 mm in size was 1 microplastic particle for every 3399 zooplankton individuals. Microplastic exposure varied, peaking within offshore habitats, during the winter, and during the day. Maximum exposure to microplastic particles relative to zooplankton prey was higher for juvenile (1:23) than adult (1:33) anchovy due to growth-associated differences in anchovy feeding. Overall, microplastic particles constituted fewer than 5% of prey-sized items available to anchovy. Microplastic exposure is likely to increase for forage fishes in the global ocean alongside declines in primary productivity, and with increased water column stratification and microplastic pollution. 
    more » « less
  4. Abstract

    Mixotrophic nanoflagellates can account for more than half of the bacterivory in the sunlit ocean, yet very little is known about their ecophysiology. Here, we characterize the grazing ecology of an open‐ocean mixotroph in the genusFlorenciella(class Dictyochophyceae). Members of this class were indirectly implicated as major consumers ofProchlorococcusandSynechococcusin the oligotrophic North Pacific Subtropical Gyre, but their phagotrophic capabilities have never been investigated. Our studies showed thatFlorenciellareadily consumedProchlorococcus,Synechococcus, and heterotrophic bacteria, and that the ingested prey relieved nutrient limitations on growth.Florenciellagrew faster (3 d−1) in nitrogen‐deplete medium given sufficient liveSynechococcus, than in nitrogen‐replete K medium (2 d−1), but it did not grow in continuous darkness. Grazing rates were substantially higher under nutrient limitation and showed a hint of diel variability, with rates tending to be highest near the end of the light period. An apparent trade‐off between the maximum clearance rate (5 nLFlorenciella−1h−1) and the maximum ingestion rate (up to ∼ 10 prey cellsFlorenciella−1h−1) across experiments suggests that grazing behavior may also vary in response to prey concentration. If the observed grazing rates are representative of other open‐ocean mixotrophs, their collective activity could account for a significant fraction of the daily cyanobacterial mortality. This study provides essential parameters for understanding the grazing ecology of a common marine mixotroph and the first characterization of mixotrophic nanoflagellate functional responses when feeding on unicellular cyanobacteria, the dominant marine primary producers in the oligotrophic ocean.

     
    more » « less
  5. The ocean continues to be a sink for microparticle (MP) pollution, which includes microplastics and other anthropogenic debris. While documentation of MP in marine systems is now common, we lack information on rates of MP ingestion by baleen whales and their prey. We collected and assessed MP loads in zooplankton prey and fecal samples of gray whales ( Eschrichtius robustus ) feeding in coastal Oregon, USA and produced the first estimates of baleen whale MP consumption rates from empirical data of zooplankton MP loads (i.e., not modeled). All zooplankton species examined were documented gray whale prey items ( Atylus tridens, Holmesimysis sculpta, Neomysis rayii ) and contained an average of 4 MP per gram of tissue, mostly of the microfiber morphotype. We extrapolated MP loads in zooplankton prey to estimate the daily MP consumption rates of pregnant and lactating gray whales, which ranged between 6.5 and 21 million MP/day. However, these estimates do not account for MP ingested from ambient water or benthic sediments, which may be high for gray whales given their benthic foraging strategy. We also assessed MP loads in fecal samples from gray whales feeding in the same spatio-temporal area and detected MP in all samples examined, which included microfibers and significantly larger morphotypes than in the zooplankton. We theorize that gray whales ingest MP via both indirect trophic transfer from their zooplankton prey and directly through indiscriminate consumption of ambient MPs when foraging benthically where they consume larger MP morphotypes that have sunk and accumulated on the seafloor. Hence, our estimated daily MP consumption rates for gray whales are likely conservative because they are only based on indirect MP ingestion via prey. Our results improve the understanding of MP loads in marine ecosystems and highlight the need to assess the health impacts of MP consumption on zooplankton and baleen whales, particularly due to the predominance of microfibers in samples, which may be more toxic and difficult to excrete than other MP types. Furthermore, the high estimated rates of MP consumption by gray whales highlights the need to assess health consequences to individuals and subsequent scaled-up effects on population vital rates. 
    more » « less