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Cited by 481Microplastics and Plastic PollutionEnvironmental Toxicology and EcotoxicologyPharmaceutical and Antibiotic Environmental Impacts

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The Effects of Natural and Anthropogenic Microparticles on Individual Fitness in Daphnia magna

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Ogonowski, Martin, Schür, Christoph, Jarsén, Åsa, Gorokhova, Elena·2016·PLOS ONE
DOI 10.1371/journal.pone.0155063PMC PMC4866784
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Abstract

Concerns are being raised that microplastic pollution can have detrimental effects on the feeding of aquatic invertebrates, including zooplankton. Both small plastic fragments (microplastics, MPs) produced by degradation of larger plastic waste (secondary MPs; SMPs) and microscopic plastic spheres used in cosmetic products and industry (primary MPs; PMPs) are ubiquitously present in the environment. However, despite the fact that most environmental MPs consist of weathered plastic debris with irregular shape and broad size distribution, experimental studies of organism responses to MP exposure have largely used uniformly sized spherical PMPs. Therefore, effects observed for PMPs in such experiments may not be representative for MP-effects in situ. Moreover, invertebrate filter-feeders are generally well adapted to the presence of refractory material in seston, which questions the potential of MPs at environmentally relevant concentrations to measurably affect digestion in these organisms. Here, we compared responses to MPs (PMPs and SMPs) and naturally occurring particles (kaolin clay) using the cladoceran Daphnia magna as a model organism. We manipulated food levels (0.4 and 9 μg C mL-1) and MP or kaolin contribution to the feeding suspension (<1 to 74%) and evaluated effects of MPs and kaolin on food uptake, growth, reproductive capacity of the daphnids, and maternal effects on offspring survival and feeding. Exposure to SMPs caused elevated mortality, increased inter-brood period and decreased reproduction albeit only at high MP levels in the feeding suspension (74% by particle count). No such effects were observed in either PMP or kaolin treatments. In daphnids exposed to any particle type at the low algal concentration, individual growth decreased by ~15%. By contrast, positive growth response to all particle types was observed at the high algal concentration with 17%, 54% and 40% increase for kaolin, PMP and SMP, respectively. When test particles comprised 22% in the feeding suspension, both MP types decreased food intake by 30%, while kaolin had no effect. Moreover, SMPs were found to homoaggregate in a concentration-dependent manner, which resulted in a 77% decrease of the ingested SMPs compared to PMPs. To better understand MP-processing in the gut, gut passage time (GPT) and evacuation rate of MPs were also assayed. SMPs and PMPs differed in their effects on daphnids; moreover, the particle effects were dependent on the MP: algae ratio in the suspension. When the MP contribution to the particle abundance in the medium changed from 1 to 4%, GPT for daphnids exposed to SMPs increased 2-fold. Our results suggest that MPs and, in particular, SMPs, have a greater capacity to negatively affect feeding in D. magna compared to naturally occurring mineral particles of similar size. Moreover, grazer responses observed in experiments with PMPs cannot be extrapolated to the field where SMPs dominate, because of the greater effects caused by the latter.

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Crossref · 10.1371/journal.pone.0155063

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Figures

Fig 1 Study outline. Study outline showing the linkages between the experiments. In Experiments I-II and V, the effects of MP and kaolin exposure on fitness were studied in adults (Exp. I-II) and their offspring (Exp. V). In Experiments III-IV, food intake and MP behavior in the gut were examined and used to explain the MP effects on growth and reproduction observed in Experiments I-II and V.
Fig 1 Study outline. Study outline showing the linkages between the experiments. In Experiments I-II and V, the effects of MP and kaolin exposure on fitness were studied in adults (Exp. I-II) and their offspring (Exp. V). In Experiments III-IV, food intake and MP behavior in the gut were examined and used to explain the MP effects on growth and reproduction observed in Experiments I-II and V.CC BY · PubMed Central
Fig 2 Reproductive effects. Total reproductive output (A) and number of broods (B) standardized to the number of survived days (Exp. I). In the controls, daphnids were incubated with only algae. PMP and SMP are primary and secondary MPs, respectively. Bars denote mean value ± 95% CI.
Fig 2 Reproductive effects. Total reproductive output (A) and number of broods (B) standardized to the number of survived days (Exp. I). In the controls, daphnids were incubated with only algae. PMP and SMP are primary and secondary MPs, respectively. Bars denote mean value ± 95% CI.CC BY · PubMed Central
Fig 3 Integrated fitness responses. Radar plot of the life history traits from Exp. I averaged across all test concentrations and z-score normalized to the control (zero mean, unit variance). Positive values denote a positive response on fitness. Reciprocal transformation was applied to Age at first reproduction so that positive values correspond to earlier reproduction compared to the control.
Fig 3 Integrated fitness responses. Radar plot of the life history traits from Exp. I averaged across all test concentrations and z-score normalized to the control (zero mean, unit variance). Positive values denote a positive response on fitness. Reciprocal transformation was applied to Age at first reproduction so that positive values correspond to earlier reproduction compared to the control.CC BY · PubMed Central
Fig 4 Growth at different food levels. Individual dry weight (DW) of daphnids normalized to the control (z-scores, zero mean, unit variance) at low (0.4 μg C mL-1, Exp. II) and high (9 μg C mL-1, Exp. IV) algal concentrations. Bars denote average difference from their respective controls ± 95% CI. NS = no significance, * = p < 0.05, ** = p < 0.01, **** = p < 0.0001.
Fig 4 Growth at different food levels. Individual dry weight (DW) of daphnids normalized to the control (z-scores, zero mean, unit variance) at low (0.4 μg C mL-1, Exp. II) and high (9 μg C mL-1, Exp. IV) algal concentrations. Bars denote average difference from their respective controls ± 95% CI. NS = no significance, * = p < 0.05, ** = p < 0.01, **** = p < 0.0001.CC BY · PubMed Central
Fig 5 MPs decrease food consumption. Total food intake of daphnids incubated in feeding media containing algae without (control) or with addition of either spherical microplastics (PMP), ground microplastics (SMP) or kaolin. Bars denote average carbon consumption (mg C) over 72-h ± 95% CI. NS denotes non-significant difference compared to the control and ** indicates p ≤ 0.01.
Fig 5 MPs decrease food consumption. Total food intake of daphnids incubated in feeding media containing algae without (control) or with addition of either spherical microplastics (PMP), ground microplastics (SMP) or kaolin. Bars denote average carbon consumption (mg C) over 72-h ± 95% CI. NS denotes non-significant difference compared to the control and ** indicates p ≤ 0.01.CC BY · PubMed Central
Fig 6 MP processing in the gut. Relative weight-specific integrated microplastic (MP) particle area in the gut as a function of time. The values are relative the average gut particle area at t = 0. Gut evacuation measured at (A) Low (104 MPs mL-1) and (B) High (3 × 104 MPs mL-1) particle concentrations. Grey bands represent 95% CI.
Fig 6 MP processing in the gut. Relative weight-specific integrated microplastic (MP) particle area in the gut as a function of time. The values are relative the average gut particle area at t = 0. Gut evacuation measured at (A) Low (104 MPs mL-1) and (B) High (3 × 104 MPs mL-1) particle concentrations. Grey bands represent 95% CI.CC BY · PubMed Central

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Research works printed but not linked: 1

  1. CW Blemishev, 1962, Superfluous feeding of marine herbivorous zooplankton, Rapp Procès-Verbaux La Réun Cons Perm Int Pour Explor Mer, 153, 108

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Metadata

Authors
Ogonowski, M., Schür, C., Jarsén, Å., & Gorokhova, E.
Affiliations
Stockholm University (SE)
Corresponding author
Ogonowski, Martin
ORCID
Venue
PLOS ONE
Publisher
Public Library of Science (PLoS)
Published
2016-05-13
Volume
11
Issue
5
Pages
e0155063
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0155063
PMC
PMC4866784
OpenAlex
W2368279972
Cited by
480
References
65
Citations by year
2026: 28 · 2025: 51 · 2024: 54 · 2023: 69 · 2022: 56 · 2021: 63 · 2020: 56 · 2019: 49 · 2018: 33 · 2017: 19 · 2016: 2
FWCI
18.75
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
Svenska Forskningsrådet Formas (216-2013-1010)
Topics
  • Physical Sciences › Environmental Science › Pollution › Microplastics and Plastic Pollution
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Environmental Toxicology and Ecotoxicology
  • Physical Sciences › Environmental Science › Pollution › Pharmaceutical and Antibiotic Environmental Impacts
Keywords
microplastics, primary microplastics, secondary microplastics, kaolin clay, zooplankton grazing, dietary intake, particle aggregation, gut transit time, maternal effects, reproduction, growth, mortality, microplastic pollution, particle size and shape, Daphnia magna, filter feeders, algal concentration
MeSH terms
Animals, Daphnia, Digestive System, Feeding Behavior, Human Activities, Kaolin, Particle Size, Reproduction, Water Pollutants, Chemical, Survival Analysis

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