Edited by: Catherine Mouneyrac, UCO Angers, France
Reviewed by: Bruno B. Castro, University of Minho, Portugal; Alessio Gomiero, NORCE Norwegian Research Centre, Norway
This article was submitted to Environmental Toxicology, a section of the journal Frontiers in Environmental Science
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
As documented by the numerous publications that have appeared in recent years, plastic pollution of the environment and the effects on the respective ecosystems are currently one of the most intensely discussed issues in environmental science and in society at large. Of special concern are the effects of micro- and nano-sized plastics. A key issue in understanding the fate and potential effects of micro- and nano-sized plastics is their dynamic nature, as the size, shape, and charge of the particles change over time. Moreover, due to various biological processes, such as the aggregation of organic material and/or bacteria (“biofouling”), the density of plastic particles that settle in the sediments of aquatic ecosystems may be several orders of magnitudes higher than that in the surrounding waters. Consequently, the risk posed by plastic pollution to benthic fauna is considerably high. Nonetheless, the vast majority of studies examining the effects of microplastics have focused on pelagic organisms so far. We therefore conducted a comprehensive literature review to examine the impact of micro- and nano-sized plastics on benthic invertebrates, including the physical and chemical effects of leaching and the interactions of plastic particles with contaminants. Overall, 330 papers were reviewed for their fulfillment of different criteria (e.g., test species, plastic material, particle shape, particle size, exposure concentration, exposure route, assay type, assay duration), with 49 publications finally included in our survey. A comprehensive gap-analysis on the effects of plastic particles on benthic invertebrates revealed a wide variety of effects triggered by micro- and/or nano-sized plastics but also distinct differences regarding the plastic materials tested, the size fractions applied, the shape of the respective particles, and the exposure routes tested. Our review concludes with a discussion of the important research gaps concerning freshwater ecosystems and recommendations for future areas of research.
The pollution of aquatic ecosystems with plastic debris is regarded as one of the most serious environmental issues worldwide. Among this debris, small-sized particles have received increasing attention and are recently of particular concern (e.g., Thompson et al.,
An understanding of the environmental fate of small-scale plastic particles is fundamental for the assessment of their potential risks, but this is complicated by the fact that the size, shape, density, and charge of the particles constantly change over time (Galloway et al.,
Direct harmful effects of nano- and microplastics may be of physical (mechanical) and/or chemical (toxicological) nature (Barnes et al.,
In this review we assess current knowledge on the effects of nano- and microplastics on benthic invertebrates in aquatic ecosystems. Our assessment is based on a literature analysis of: (i) the impacts on organisms in freshwater and marine environments, (ii) the harmful effects induced by the physical or chemical impacts of plastic particles, (iii) the various particle materials, shapes, and sizes examined, (iv) the exposure matrix and parameters assessed in the respective assays and (v) the interaction of contaminants with nano- and microplastic particles. Subsequently, a gap analysis based on the obtained findings was conducted and areas in need of further research were identified.
Using the databases Web of Science and Google Scholar, a comprehensive literature review of the physical and chemical effects of leaching processes as well as the interaction of plastic particles with contaminants in terms of their impacts on benthic invertebrates was conducted. The search was based on a query of the key word terms: microplastic* OR nanoplastic* AND benthic* OR benthos* AND invertebrate* AND effect* OR impact* or a combination thereof.
Overall, 330 papers were reviewed, with 49 publications finally included in this survey based upon their relevance to the topic, in agreement with general criteria for peer-reviewed articles and as judged by the authors of this review. Although a comprehensive literature search was carried out, the retrieved studies may not be fully representative of all studies conducted, since the probability that a given study will be published generally increases with the increased statistical significance of its results. This “file drawer problem” was described by Arnqvist and Wooster (
The publications were categorized according to the investigated habitat (freshwater or marine) and the impact (physical or chemical) on the benthic invertebrates assessed. For each publication, the following criteria were analyzed: taxon, species, plastic material, particle shape, particle size, exposure concentration, and matrix endpoints investigated. The general review procedure and the effects identified in those studies are summarized in
Schematic representation of the review process, publication selection and data analysis.
The mechanical hazards posed by the ingestion of micro- and nano-sized plastic particles by organisms in freshwater ecosystems were evaluated in 26 experiments reported in 10 publications (
Effects on micro- and nano-sized plastic particles on benthic freshwater invertebrates.
Annelida | PS | Fragments | 20–500 μm | 0.1–40% sed. dw | S | Mortality | No effects on mortality | Redondo-Hasselerharm et al., |
|
Development | No effects on growth | ||||||||
Behavior | No effects on feeding rate | ||||||||
PS | Fragments | 20–500 μm | 0.1–40% sed. dw | S | Mortality | No effects on mortality | Redondo-Hasselerharm et al., |
||
Development | No effects on growth | ||||||||
Behavior | No effects on feeding rate | ||||||||
Arthropoda | PS | Fragments | 20–500 μm | 0.1–40% sed. dw | S | Mortality | No effects on mortality | Redondo-Hasselerharm et al., |
|
Development | No effects on growth | ||||||||
Behavior | No effects on feeding rate | ||||||||
PE | Spheres | 1–4 μm | 500 part. kg−1 | S | Mortality | Significantly increased mortality at 1–4, 10–27, and 43–54 μm | Ziajahromi et al., |
||
10–27 μm | Development | Significantly decreased body length at 1–4, 10–27, and 43–54 μm; | |||||||
43–54 μm | Significantly decreased length of head capsule at 10–27 μm; | ||||||||
100–126 μm | Reduced development of head capsule, mouth parts, and antenna at 10–27 μm; | ||||||||
Development delay of organisms at 10–27 μm | |||||||||
Emergence | Significantly lowered emerging rate for all size ranges | ||||||||
PS | Spheres | ≤ 5 μm | 12,500 part. ml−1 | AM | Mortality | No effects on mortality | Blarer and Burkhardt-Holm, |
||
Development | No effects on wet weight | ||||||||
Behavior | No effects on feeding rate | ||||||||
Assimilation | No effects on assimilation efficiency | ||||||||
PA | Fibers | 20 × 500 μm | 2,680 cm−2 | AM | Mortality | No effects on mortality | Blarer and Burkhardt-Holm, |
||
Development | No effects on wet weight | ||||||||
Behavior | No effects on feeding rate | ||||||||
Assimilation | Significantly decreased assimilation efficiency | ||||||||
PMMA | Fragments | 32–64 μm | 100,000 part. ind.−1 | AM | Development | Significantly decreased wet weight | Straub et al., |
||
64–125 μm | Behavior | No effects on feeding rate | |||||||
125–250 μm | Assimilation | Significantly decreased assimilation efficiency | |||||||
PHB | Fragments | 32–64 μm | AM | Development | Significantly decreased wet weight | Straub et al., |
|||
64–125 μm | Behavior | No effects on feeding rate | |||||||
125–250 μm | Assimilation | No effects on assimilation efficiency | |||||||
PS | Fragments | 20–500 μm | 0.1–40% sed. dw | S | Mortality | No effects on mortality | Redondo-Hasselerharm et al., |
||
Development | Significantly reduced growth (Ec10: 1.07% sed. dw, | ||||||||
EC50: 3.57% sed. dw) | |||||||||
Behavior | No effects on feeding rate | ||||||||
PS | Fragments | 20–500 μm | 0.1–40% sed. dw | S | Mortality | No effects on mortality | Redondo-Hasselerharm et al., |
||
Development | No effects on growth | ||||||||
Behavior | No effects on feeding rate | ||||||||
PE | Fragments | 10–27 μm | 10–100,000 part. ml−1 | AM | Mortality | Significant, dose-dependent increase in mortality | Au et al., |
||
(LOEC: 10,000 part. ml−1,!!! LC50: 4.6 × 104 part. ml−1) | |||||||||
Development | No effects on dw | ||||||||
5,000–20,000 part. ml−1 | Reproduction | Reproduction significantly decreased at 5,000 part. ml−1 (day 28) and | |||||||
at 10,000 part. ml−1 (day 28 and 42) | |||||||||
PP | Fibers | 20–75 × 20 μm | 22.5–90 part. ml−1 | AM | Mortality | Significant, dose-dependent increase in mortality | Au et al., |
||
(LOEC: 45 part. ml−1,!!! LC50: 71 part. ml−1) | |||||||||
Development | Significant, dose-dependent decrease in dw (LOEC: 45 part. ml−1) | ||||||||
Mollusca | PA | Fragments | 4.64–602 μm | 30 and 70% | Food | Mortality | No effects on mortality | Imhof and Laforsch, |
|
Development | No effects on adult development | ||||||||
Reproduction | No effects on reproduction | ||||||||
Mortality | No effects on mortality | ||||||||
Development | No effects on juvenile development | ||||||||
PC | Fragments | 4.64–602 μm | 30 and 70% | Food | Mortality | No effects on mortality | Imhof and Laforsch, |
||
Development | No effects on adult development | ||||||||
Reproduction | No effects on reproduction | ||||||||
Mortality | No effects on mortality | ||||||||
Development | No effects on juvenile development | ||||||||
PET | Fragments | 4.64–602 μm | 30 and 70% | Food | Mortality | No effects on mortality | Imhof and Laforsch, |
||
Development | No effects on adult development | ||||||||
Reproduction | No effects on reproduction | ||||||||
Mortality | No effects on mortality | ||||||||
Development | No effects on juvenile development | ||||||||
PS | Fragments | 4.64–602 μm | 30 and 70% | Food | Mortality | No effects on mortality | Imhof and Laforsch, |
||
Development | No effects on adult development | ||||||||
Reproduction | No effects on reproduction | ||||||||
Mortality | No effects on mortality | ||||||||
Development | No effects on juvenile development | ||||||||
PVC | Fragments | 4.64–602 μm | 30 and 70% | Food | Mortality | No effects on mortality | Imhof and Laforsch, |
||
Development | No effects on adult development | ||||||||
Reproduction | No effects on reproduction | ||||||||
Mortality | No effects on mortality | ||||||||
Development | No effects on juvenile development | ||||||||
PS | Fragments | 20–500 μm | 0.1–40% sed. dw | S | Mortality | No effects on mortality | Redondo-Hasselerharm et al., |
||
Development | No effects on growth | ||||||||
Behavior | No effects on feeding rate | ||||||||
PS | Spheres | 1 and 10 μm | 5 × 105 + 5 × 105 part. l−1, | AM | Cellular response | No effects on GST and SOD activity; | Magni et al., |
||
2 × 106 + 2 × 106 part. l−1 | CAT and gpx activity significantly affected at 5 × 105 + 5 × 105 part. l−1; | ||||||||
No effects on levels of LPO and PCC; | |||||||||
DOP significantly increased at 5 × 105 + 5 × 105 part. l−1 (day 3) and | |||||||||
2 × 106 + 2 × 106 part. L−1 (day 6); | |||||||||
No effects on SER and GLU; | |||||||||
No effects on the activity of ache, MAO and micronuclei frequency | |||||||||
Nematoda | PA | Fragments | ~70 μm | 0.5–10 mg m−2, | AM | Mortality | Significantly increased mortality (LOEC: 0.5 mg m−2) | Lei et al., |
|
5 mg m−2 | Development | Significantly decreased body length | |||||||
Reproduction | Number of embryos significantly lowered; No effect on brood size | ||||||||
Cellular Response | Calcium level in intestines significantly lowered; | ||||||||
No effect on expression of |
|||||||||
PP | Fragments | ~70 μm | 0.5–10 mg m−2, | AM | Mortality | Significantly increased mortality (LOEC: 0.5 mg m−2) | Lei et al., |
||
5 mg m−2 | Development | Significantly decreased body length | |||||||
Reproduction | Number of embryos significantly lowered; No effect on brood size | ||||||||
Cellular Response | No effect on calcium level in intestines; | ||||||||
Expression of |
|||||||||
PE | Fragments | ~70 μm | 0.5–10 mg m−2, | AM | Mortality | Significantly increased mortality (LOEC: 0.5 mg m−2) | Lei et al., |
||
5 mg m−2 | Development | Significantly decreased body length | |||||||
Reproduction | Number of embryos significantly lowered; Brood size significantly decreased | ||||||||
Cellular Response | Calcium level in intestines significantly lowered; | ||||||||
Expression of |
|||||||||
PVC | Fragments | ~70 μm | 0.5–10 mg m−2 | AM | Mortality | Significantly increased mortality (LOEC: 1 mg m−2) | Lei et al., |
||
Reproduction | Number of embryos significantly lowered; Brood size significantly decreased | ||||||||
Cellular Response | Calcium level in intestines significantly lowered; | ||||||||
Expression of |
|||||||||
Nematoda | PS | Spheres | 0.1 μm | 1–10,000 μg l−1 | AM | Cellular Response | Significant, dose-dependent induction of intestinal ROS production from up 10 μg l−1; | Zhao et al., |
|
Significant, dose-dependent increase in defecation cycle length from up 10 μg l−1 | |||||||||
Behavior | Significant, dose-dependent decrease of locomotion (head trash, body bend) from up 10 μg l−1 | ||||||||
Reproduction | Significant, dose-dependent decrease of reproduction (brood size) from up 10 μg l−1 | ||||||||
Development | Significant, transgenerational effects on F1-generation in terms of intestinal ROS production, | ||||||||
locomotion behavior and reproduction form up 100 μg l−1 | |||||||||
Spheres | 0.1 μm | 0.5–10 mg m−2, | AM | Mortality | Significantly increased mortality (LOEC: 0.5 mg m−2), | Lei et al., |
|||
1 μm | 5 mg m−2 | Effects significantly size-depending, with slight effects induced by 0.1 μm part., | |||||||
5 μm | strongest effects induced by 1 μm part. | ||||||||
Development | Significantly decreased body length | ||||||||
Reproduction | Number of embryos significantly lowered for 0.1 and 1 μm part.;Brood size significantly lowered for 0.1 and 1 μm part. | ||||||||
Cellular Response | Calcium level in intestines significantly lowered for 1 μm;Expression of |
||||||||
Rotifera | PS | Spheres | 0.05 μm | 0.1–20 μg ml−1, | AM | Reproduction | Reproduction time significantly increased for 0.05 μm at 10 μg ml−1; | Jeong et al., |
|
0.5 μm | 10 μg ml−1 | Fecundity significantly affected for 0.05 and 0.5 μm (LOEC 0.05 μm: 1 μg ml−1, LOEC 0.5 μm: 20 μg ml−1); | |||||||
6 μm | Population growth significantly retarded for 0.05 and 0.5 μm | ||||||||
Life-Span | Life-span significantly affected for 0.05 and 0.5 μm (LOEC 0.05 μm: 0.1 μg ml−1, LOEC 0.5 μm: 20 μg ml−1) | ||||||||
Cellular Response | ROS level significantly increased under microplastic treatments; | ||||||||
Significantly affected exposure of antioxidant-related enzymes; | |||||||||
Phosphorylation status of p-JNK and p-p38 increased for 0.05 μm |
Toxicity assays examining physical effects in organisms in (i) freshwater studies, (ii) marine studies and (iii) total. Data depict the groups of organisms (taxa) used
Among the 26 experiments examining the mechanical hazards posed by micro- and nano-sized plastics on benthic organisms in freshwater, 46% (
As shown in
Lethal effects of nano- and micro-sized plastics were investigated in 81% (
The effects of small-scale plastics on the development of organisms were investigated most frequently, by being of concern in 88% (
The effects on reproduction were investigated in 50% (
Behavioral alterations induced by small-scale plastic particles were investigated in 11 assays, being tantamount with 42% of the experiments described in the included studies (
Cellular responses, including alterations in gene expression, reactive oxygen species (ROS) production, and enzyme activity, were the assessed end points of 31% (
The parameters assimilation efficiency (
Mechanically induced effects have also been investigated frequently in marine settings, with 50 studies being included in the review process. Organisms belonging to Mollusca were most commonly used (36%,
Effects on micro- and nano-sized plastic particles on benthic marine invertebrates.
Annelida | PS | Fragments | 400–1,300 μm | 0.074–7.4% sed. dw | S | Mortality | No effects on mortality | Besseling et al., |
|
Behavior | Significant, dose-dependent decrease of feeding activity | ||||||||
Development | Significant, dose-dependent decrease of dw, no effects on ww, and AFDW | ||||||||
PVC | Fragments | 63–500 μm | 0.5–5% sed. dw | S | Egestion | Significantly prolonged gut residence time at 5% sed. | Wright et al., |
||
Behavior | Significantly reduced feeding activity at 5% sed. | ||||||||
Cellular response | Significantly increased phagocytic activity at 0.5 and 5% sed. | ||||||||
Energy reserves | Significantly reduced energy reserves (J g−1 ww.) at 1 and 5% sed.; | ||||||||
Significantly lowered lipid reserves for UPVC-exposure | |||||||||
Fragments | 2.5–316 μm | 0.02–2% sed. ww | S | Mortality | No effects on mortality | Green et al., |
|||
Development | No effects on dw biomass | ||||||||
Behavior | Significantly less casts produced at 2% sed. ww | ||||||||
O2 consumption | Significantly increased O2 consumption at 2% sed. ww | ||||||||
PLA | Fragments | 1.4–707 μm | 0.02–2% sed. ww | S | Mortality | No effects on mortality | Green et al., |
||
Development | No effects on dw biomass | ||||||||
Behavior | No effects on bioturbation | ||||||||
O2 consumption | Significantly increased O2 consumption at 2% sed. ww | ||||||||
HDPE | Fragments | 8.7–478 μm | 0.02–2% sed. ww | S | Mortality | No effects on mortality | Green et al., |
||
Development | No effects on dw biomass | ||||||||
Behavior | No effects on bioturbation | ||||||||
O2 consumption | Significantly increased O2 consumption at 2% sed. ww | ||||||||
PS | Spheres | 8–12 μm | 100 and 1,000 part. ml−1 | AM | Mortality | Smaller spheres increased mortality significantly | Leung and Chan, |
||
32–38 μm | Regeneration | Significantly reduced regeneration rate at 1000 part. ml−1, | |||||||
smaller particles being significantly more detrimental | |||||||||
PVC | Fragments | 250 μm | 200 and 2,000 part. kg−1 | S | Mortality | No effects on mortality | Gomiero et al., |
||
Cellular response | Significantly increased phagocytic activity at 200 part. kg−1 (10 d) | ||||||||
and 2,000 part. kg−1 (10 and 28 d); | |||||||||
No effects on extracellular lysosome release, lysosomal | |||||||||
membrane stability (LMS) and oxyradical production; | |||||||||
No effects micronuclei frequency and on DNA strand breaks; | |||||||||
No effects on Lipofuscin content and Catalase activity | |||||||||
Arthropoda | PS | Spheres | 15 μm | 50 and 500 part. ml−1 | AM | Mortality | No effects on mortality | Vroom et al., |
|
PS | Spheres | 20 μm | 75 part. ml−1 | AM | Behavior | Feeding rate significantly reduced; Significant shift to small sized prey | Cole et al., |
||
Mortality | No significant effects on mortality | ||||||||
Reproduction | No significant effects on egg production rate;Hatching success significantly decreased from up day 6 | ||||||||
Development | Significantly smaller eggs produced from up day 7 | ||||||||
O2 consumption | No effects on O2 consumption | ||||||||
Assimilation | 2-fold greater energetic losses expected | ||||||||
PP | Fibers | 1,000–5,000 μm | 0.3–1.0% by weight | AM | Behavior | Feeding rate significantly decreased | Watts et al., |
||
Assimilation | Significantly reduced scope for growth | ||||||||
PS | Spheres | 8 μm | 106 and 107 part. l−1 | AM | Mortality | No effects on mortality | Watts et al., |
||
O2 consumption | O2 consumption significantly reduced (1 h) at 107 PS part. l−1 | ||||||||
Cellular response | Significant effects on Na+-Ions and Ca2a+-Ions (24 h) at 107 PS part. l−1, | ||||||||
no effects on K+-Ion concentration; | |||||||||
Significant, dose-dependent effects on hemocyanin concentration | |||||||||
No effect on hemolymph protein concentration; | |||||||||
PS-COOH | Spheres | 8 μm | 106 and 107 part. l−1 | AM | Mortality | No effects on mortality | Watts et al., |
||
O2 consumption | No effects on O2 consumption | ||||||||
Cellular response | No cellular responses induced | ||||||||
PS-NH2 | Spheres | 8 μm | 106 and 107 part. l−1 | AM | Mortality | No effects on mortality | Watts et al., |
||
O2 consumption | No effects on O2 consumption | ||||||||
Cellular response | No cellular responses induced | ||||||||
PS | Spheres | 7.3 μm | 4,000–25,000 part. ml−1 | AM | Behavior | Significantly, dose-dependently reduced total algae feeding rate | Cole et al., |
||
PS | Spheres | 10 μm | 12 part. mg food−1 | Food | Mortality | No effects on survival | Hämer et al., |
||
Behavior | No effects on feeding rate | ||||||||
Development | No effects on the duration of intermolt periods and growth | ||||||||
Arthropoda | PS | Fragments | 1–100 μm | 20 part. mg food−1 | Food | Mortality | No effects on mortality | Hämer et al., |
|
Behavior | No effects on feeding rate | ||||||||
Development | No effects on the duration of intermolt periods and growth | ||||||||
PA | Fibers | 20–2,500 μm | 0.3 mg part. mg food−1 | Food | Mortality | No effects on mortality | Hämer et al., |
||
Behavior | No effects on feeding rate | ||||||||
Development | No effects on the duration of intermolt periods and growth | ||||||||
PE | Spheres | 35–165 μm | 50,000 part. l−1 | AM | Mortality | Significantly increased mortality by larger particles (>75 μm) | Gray and Weinstein, |
||
PS | Spheres | 30 and 75 μm | 50,000 part. l−1 | AM | Mortality | Significantly increased mortality by larger particles (75 μm) | Gray and Weinstein, |
||
PP | Fragments | 34 and 93 μm | 50,000 part. l−1 | AM | Mortality | Significantly increased mortality by larger particles (93 μm) | Gray and Weinstein, |
||
Fibers | 34 and 93 μm | 50,000 part. l−1 | AM | Mortality | Significantly increased mortality | Gray and Weinstein, |
|||
PS | Spheres | 0.05 μm | 0.1–20 μg ml−1 | AM | Development | Development significantly delayed for 0.05 μm (LOEC: 10 μg ml−1) | Jeong et al., |
||
0.5 μm | Reproduction | Fecundity significantly reduced for 0.05 μm (LOEC: 10 μg ml−1) and | |||||||
6 μm | 0.5 μm (LOEC: 20 μg ml−1) | ||||||||
20 μg ml−1 | Cellular response | Significant increase in intracellular ROS level by 0.05 μm spheres; | |||||||
Significantly increased phosphorylation of p-ERK, p-p38 and Nrf2; | |||||||||
Significantly increased activity of GPx (0.05 μm), GR, GST, and SOD | |||||||||
PET | Fragments | 5–10 μm | 10,000–80,000 part. ml−1 | AM | Reproduction | Significantly reduced egg production (LOEC 80,000 part. ml−1) | Heindler et al., |
||
20,000 part. ml−1 | Relative population size significantly reduced after 6 and 24 d | ||||||||
20,000 part. ml−1 | Cellular response | Significantly down regulated |
|||||||
PS | Spheres | 0.05 μm | 6–313 μg ml−1 | AM | Mortality | No effects on mortality | Lee et al., |
||
0.5 μm | 0.125–25 μg ml−1 | Mortality | Survival of F0 generation significantly effected for 0.05 μm | ||||||
6 μm | (LOEC: 1.25 μg ml−1, LC50: 2.15 μg ml−1), | ||||||||
Survival of F1 generation significantly effected for 0.05 μm | |||||||||
(LOEC: 1.25 μg ml−1, LC50: 0.16 μg ml−1) and 0.5 μm | |||||||||
(LOEC: 25 μg ml−1, LC50: 23.5 μg ml−1) | |||||||||
Reproduction | Fecundity of F0 generation significantly decreased for 0.5 μm | ||||||||
(LOEC: 0.125 μg ml−1, EC50: 0.07 μg ml−1) and 6 μm | |||||||||
(LOEC: 0.125 μg ml−1, EC50: 0.10 μg ml−1), | |||||||||
Fecundity of F1 generation significantly decreased for 0.5 μm | |||||||||
(LOEC: 0.125 μg ml−1, EC50: 0.04 μg ml−1) and 6 μm | |||||||||
(LOEC: 0.125 μg ml−1, EC50: 0.04 μg ml−1) | |||||||||
Development | Nauplius phase of F0 generation significantly delayed for 0.05 μm at 1.25 μg ml−1, | ||||||||
Generation time of F1 generation significantly delayed for 0.05 μm | |||||||||
at 1.25 μg ml−1 and for 0.5 μm at 25 μg ml−1 (EC50 21.2–21.4 μg ml−1) | |||||||||
Chordata | PS | Spheres | 10 μm | 0.125–25 μg ml−1 | AM | Development | Significantly delayed juvenile development, no effects on larvae | Messinetti et al., |
|
Mortality | No effects on larval and juvenile mortality | ||||||||
Echinodermata | PS | Spheres | 10 μm | 0.125–25 μg ml−1 | AM | Development | Significantly effected body length from up 12.5 μg ml−1, | Messinetti et al., |
|
Significantly reduced body weight at 0.125 μg ml−1, | |||||||||
Significantly effected arm length at 0.125, 12.5 and 25 μg ml−1 | |||||||||
Mortality | No effects on larval mortality | ||||||||
Spheres | 6 μm | 103-105 part. ml−1 | AM | Reproduction | Significantly reduced fertilization rate (LOEC 103 part. ml−1) | Martínez-Gómez et al., |
|||
Development | Significantly affected larval development of pre-exposed zygotes, | ||||||||
Significantly reduced larval growth of pre-exposed gametes, | |||||||||
Significantly affected embryo development at 103 and 104 part. ml−1 | |||||||||
of virgin PS and at each concentration for aged particles | |||||||||
PS-COOH | Spheres | 0.04 μm | 25 μg ml−1 | AM | Cellular response | Significantly up regulated |
Della Torre et al., |
||
2.5–50 μg ml−1 | Development | No significant effects on development | |||||||
PS-NH2 | Spheres | 0.05 μm | 3 μg ml−1 | AM | Cellular response | Significantly up regulated |
|||
1–50 μg ml−1 | Development | Significantly increased malformations (EC50 24 hpf 3.82 μg ml−1, 48 hpf 2.61 μg ml−1) | |||||||
HDPE | Fragments | >0–80 μm | 0.005–5 g l−1 | AM | Development | Significantly affected larval development of pre-exposed zygotes, | Martínez-Gómez et al., |
||
Significantly reduced larval growth of pre-exposed gametes, | |||||||||
Significantly affected embryo development at 103 and 105 part. ml−1 | |||||||||
of virgin HDPE and at each concentration for aged particles | |||||||||
PE | Spheres | 10–45 μm | 1–300 part. ml−1 | AM | Development | Significantly reduced body width at 300 part. ml−1 | Kaposi et al., |
||
Mortality | No effects on larval mortality | ||||||||
Mollusca | PS | Fragments | 63–250 μm | 10 and 1,000 part. l−1 | AM | Behavior | Feeding rate significantly reduced at 1,000 part. l−1 | Xu et al., |
|
Assimilation | No effects on absorption efficiency | ||||||||
O2 consumption | No effects on respiration rate | ||||||||
PS | Spheres | 1 and 10 μm | 1–1,000 part. ml−1 | AM | Behavior | No significant effects on feeding rate | Cole and Galloway, |
||
100 part. ml−1 | Development | No effects on growth | |||||||
2 and 6 μm | 0.023 mg l−1 | Behavior | Significantly increased feeding rate | Sussarellu et al., |
|||||
Assimilation | Significantly increased absorption efficiency | ||||||||
Reproduction | Significantly reduced oocyte number | ||||||||
Development | Significantly reduced oocyte diameter and quality (D-larval yield); | ||||||||
Significantly reduced sperm velocity; | |||||||||
Significantly reduced larval growth | |||||||||
Cellular response | Significantly increased sizes of hyalinocytes and granulocytes; | ||||||||
Significant effects on transcript expression in digestive glands, gonads and oocytes; | |||||||||
Significant effects on the proteome of oocytes | |||||||||
PLA | Fragments | 0.6–363 μm | 2.5 and 25 μg l−1 | Food | Behavior | Significantly decreased feeding rate at 25 μg l−1 | Green et al., |
||
HDPE | Fragments | 0.48–316 μm | 2.5 and 25 μg l−1 | Food | Behavior | Significantly decreased feeding rate at 25 μg l−1 | Green et al., |
||
Mortality | No effects on mortality | ||||||||
Fragments | >0–80 μm | 2.5 g l−1 | AM | Cellular response | Significantly increased granulocytoma formation, | von Moos et al., |
|||
Significantly decreased lysosomal membran stability (LMS) | |||||||||
Mortality | No effects on mortality | ||||||||
PS | Spheres | 3 and 9.6 μm | AM | Behavior | No effects on feeding rate | Browne et al., |
|||
Cellular response | No effects on oxidative status of hemolymph, viability and | ||||||||
phagocytic activity of hemocytes | |||||||||
Spheres | 2 and 6 μm | 32 μg l−1 | AM | Cellular response | Significantly increased number of dead hemocytes; | Paul-Pont et al., |
|||
Significantly increased ROS production; | |||||||||
Significantly reduced catalase (CAT) activity, | |||||||||
Significantly reduced lipid peroxidation (LPO), | |||||||||
Significantly reduced glutathione reductase (GR); | |||||||||
Significantly effected anti-oxidant gene expression | |||||||||
Development | Significantly increased histopathological observations | ||||||||
Spheres | 0.03 μm | 0.1–0.3 g l−1 | AM | Egestion | Significantly increased production of pseudofeces | Wegner et al., |
|||
Behavior | Significantly decreased feeding rates | ||||||||
PS | Spheres | 2 and 6 μm | 32 μg l−1 | AM | Cellular response | Significantly increased number of dead hemocytes; | Paul-Pont et al., |
||
Significantly increased ROS production; | |||||||||
Significantly reduced catalase (CAT) activity, | |||||||||
Significantly reduced lipid peroxidation (LPO), | |||||||||
Significantly reduced glutathione reductase (GR); | |||||||||
Significantly effected anti-oxidant gene expression | |||||||||
Development | Significantly increased histopathological observations | ||||||||
Fragments | < 100 μm | 1.5 g l−1 | AM | Mortality | No effects on mortality | Avio et al., |
|||
Cellular response | Significantly decreased LMS | ||||||||
No effects on hemocytes and phagocytosis activitySignificantly decreased AChE levels in gills | |||||||||
Significantly inhibited Se-dependent glutathione peroxidase | |||||||||
PS-NH2 | Spheres | 0.05 μm | 1–50 μg ml−1 | AM | Cellular response | Significantly decreased lysosomal membrane stability (LMS; LOEC 5 μg ml−1) | Canesi et al., |
||
Significant increase in lysozyme release (LOEC: 1 μg ml−1) | |||||||||
Significantly increased ROS production (LOEC: 1 μg ml−1) | |||||||||
Significantly increased NO production | |||||||||
Significantly decreased phagocytosis (LOEC: 1 μg ml−1) | |||||||||
Significantly effected apoptotic parameters (ANX+, ANX+/PI+, TMRE, NAO; LOEC: 50 μg ml−1) | |||||||||
Spheres | 0.05 μm | 0.001–20 mg l−1 | AM | Development | Significantly decreased larval development (LOEC: 0.01 mg l−1, EC50: 0.142 mg l−1) | Balbi et al., |
|||
0.15 mg l−1 | Cellular response | Significantly effected gene expression (CS, CA, EP, ABCB and LYSO) | |||||||
Mollusca | PE | Fragments | < 100 μm | 1.5 g l−1 | AM | Mortality | No effects on mortality | Avio et al., |
|
Cellular response | Significantly reduced Granulocytes/Hyalinocytes ratio | ||||||||
No effects on hemocytes and phagocytosis activity | |||||||||
Significantly decreased |
|||||||||
HDPE | Fragments | 0.48–316 μm | 2.5 and 25 μg l−1 | Food | Behavior | Significantly increased feeding rates at 25 μg l−1 | Green et al., |
||
Mortality | No effects on mortality | ||||||||
Fragments | 0.48–316 μm | 80 μg l−1 | Food | Behavior | No effects on feeding rate | Green, |
|||
Development | No effects on shell growth | ||||||||
O2 consumption | No effects on respiration rates | ||||||||
PLA | Fragments | 0.6–363 μm | 2.5 and 25 μg l−1 | Food | Behavior | Significantly increased feeding rates at 2.5 and 25 μg l−1 | Green et al., |
||
Mortality | No effects on mortality | ||||||||
Fragments | 0.6–363 μm | 80 μg l−1 | Food | Behavior | No effects on feeding rate | Green, |
|||
Development | No effects on shell growth | ||||||||
O2 consumption | No effects on respiration rates | ||||||||
Rotifera | PS | Spheres | 0.05–3 μm | 0.72–5.74 μg ml−1 | AM | Behavior | Feeding rate dose-dependently reduced by plastic particles, effects size-dependent up to particles of 0.5 μm | Snell and Hicks, |
|
Reproduction | Significantly reduced population growth rate at 1.14 μg ml−1 for 0.05 μm particles (NOEC 0.57 μg ml−1), | ||||||||
no effects for larger particles; | |||||||||
No effects on population growth rate of F1 generation |
Most studies of marine benthic organisms investigated PS exposure, including 10 experiments assessing the mechanical impact of functionalized PS-particles PS-COOH (4%,
The main application route was via aqueous medium (70%,
Lethal effects were examined in 56% (
Effects on the development of benthic organisms in marine environments were examined in 46% of the studies (
Behavioral alterations of benthic marine organisms due to nano- and micro-sized plastics were assessed in 46% of the studies (
Closely linked to changes in feeding behavior are changes in egestion, being assessed in two experiments (2%;
The cellular responses of marine organisms to small-scale plastics were assessed in 36% (
The effects induced by the mechanical hazards of micro- and nano-sized plastics on oxygen (O2) consumption by marine organisms were examined in 20% (
The mechanical hazards affecting reproduction (egg production, fecundity, fertilization rates, oocyte number, and population size and growth rate) were assessed in 7 (14%) of the marine studies (
Sussarellu et al. (
Finally, the regeneration potential of
Among the 24 experiments focusing on leachates of micro- and nanoplastics, a single one (4%) targeted a freshwater organism (
Effects of plastic leachates on benthic invertebrates.
Marine | Arthropoda | HDPE | Fragments | 0.004–0.5 m2m l−1 | AM | 24 h | Mortality | Significantly increased mortality (LOEC: 0.1 m2m l−1) | Li H. X. et al., |
|
Development | Significantly inhibited settlement (LOEC: 0.004 m2m l−1) | |||||||||
LDPE | Fragments | 0.004–0.5 m2m l−1 | AM | 24 h | Mortality | Significantly increased mortality (LOEC: 0.1 m2m l−1) | Li H. X. et al., |
|||
Development | Significantly inhibited settlement (LOEC: 0.004 m2m l−1) | |||||||||
PC | Fragments | 0.004–0.5 m2m l−1 | AM | 24 h | Mortality | Significantly increased mortality (LOEC: 0.1 m2m l−1) | Li H. X. et al., |
|||
Development | Significantly inhibited settlement (LOEC: 0.004 m2m l−1) | |||||||||
PET | Fragments | 0.004–0.5 m2m l−1 | AM | 24 h | Mortality | Significantly increased mortality (LOEC: 0.1 m2m l−1) | Li H. X. et al., |
|||
Development | Significantly inhibited settlement (LOEC: 0.004 m2m l−1) | |||||||||
PP | Fragments | 0.004–0.5 m2m l−1 | AM | 24 h | Mortality | Significantly increased mortality (LOEC: 0.1 m2m l−1) | Li H. X. et al., |
|||
Development | Significantly inhibited settlement (LOEC: 0.004 m2m l−1) | |||||||||
PS | Fragments | 0.004–0.5 m2m l−1 | AM | 24 h | Mortality | Significantly increased mortality (LOEC: 0.5 m2m l−1) | Li H. X. et al., |
|||
Development | Significantly inhibited settlement (LOEC: 0.004 m2m l−1) | |||||||||
PVC | Fragments | 0.004–0.5 m2m l−1 | AM | 24 h | Mortality | Significantly increased mortality (LOEC: 0.1 m2m l−1) | Li H. X. et al., |
|||
Development | Significantly inhibited settlement (LOEC: 0.004 m2m l−1) | |||||||||
Bio-bag | Fragments | 100 g l−1 | AM | 72 h | Mortality | Significantly induced mortality (LC10 Bio: 24 g l−1 (0 h), 12 g l−1 (96 h), 29 g l−1 (192 h), | Bejgarn et al., |
|||
18 g l−1 (288 h); LC50 Bio: >100 g l−1 (0 h), 24 g l−1 (96 h), 36 g l−1 (192 h), 26 g l−1 (288 h)) | ||||||||||
Bio-PET | Fragments | 100 g l−1 | AM | 72 h | Mortality | No effects on mortality | Bejgarn et al., |
|||
HDPE | Fragments | 100 g l−1 | AM | 72 h | Mortality | No effects on mortality | Bejgarn et al., |
|||
LDPE | Fragments | 100 g l−1 | AM | 72 h | Mortality | No effects on mortality | Bejgarn et al., |
|||
PET | Fragments | 100 g l−1 | AM | 72 h | Mortality | No effects on mortality | Bejgarn et al., |
|||
PLA | Fragments | 100 g l−1 | AM | 72 h | Mortality | No effects on mortality | Bejgarn et al., |
|||
PP | Fragments | 100 g l−1 | AM | 72 h | Mortality | LC10 PP: 37 g l−1 (192 h), 16 g l−1 (288 h), LC50 PP: 71 g l−1 (192 h), 21 g l−1 (288 h) | Bejgarn et al., |
|||
PS | Fragments | 100 g l−1 | AM | 72 h | Mortality | No effects on mortality | Bejgarn et al., |
|||
PUR | Fragments | 100 g l−1 | AM | 72 h | Mortality | LC10 PUR: 26 g l−1 (0 h), 40 g l−1 (96 h), >100 g l−1 (192 h), | Bejgarn et al., |
|||
LC5C0 PUR: 85 g l−1 (0 h), >100 g l−1 (96 h), >100 g l−1 (192 h) | ||||||||||
PVC | Fragments | 100 g l−1 | AM | 72 h | Mortality | LC10 PVC: 16–43 g l−1 (0 h), 23–35 g l−1 (96 h), 12–87 g l−1 (192 h), 11 g l−1 (288 h), | Bejgarn et al., |
|||
LC50 PVC: 35–>100 g l−1 (0 h), 35–60 g l−1 (96 h), 24–52 g l−1 (192 h), 21 g l−1 (288 h) | ||||||||||
Rubber | Fragments | 100 g l−1 | AM | 72 h | Mortality | LC1C0 Rubber: 6 g l−1 (0 h), 6 g l−1 (96 h), LC50 PUR: 8 g l−1 (0 h), 7 g l−1 (96 h) | Bejgarn et al., |
|||
Echinodermata | PE | Fragments | 250 ml l−1 | AM | 24 h | Development | Significantly affected embryo development in the pellet-water interface assay, | Nobre et al., |
||
Significantly affected embryo development in elutriate assay for virgin pellets exclusively | ||||||||||
PS | Spheres | 103-105 part. ml−1 | AM | 30 d | Development | Significantly affected embryo development | Martínez-Gómez et al., |
|||
HDPE | Fragments | 0.005–5 g l−1 | AM | 30 d | Development | Significantly affected embryo development in leachate assays of 0.005 and 5 g l−1 | Martínez-Gómez et al., |
|||
Mollusca | PP | Fragments | 50–200 ml l−1 | AM | 24 h | Development | Significantly affected embryo development in leachate assays with PP (LOEC 50 ml l−1), | Gandara E Silva et al., |
||
Effects significantly higher in tube assays compared to beaker assays, | ||||||||||
PP | Fragments | 200 ml l−1 | AM | 24 h | Development | Significantly affected embryo development in leachate assays, | Gandara E Silva et al., |
|||
unknown | Effects of beach-collected fragments significantly higher compared to PP fragments | |||||||||
Freshwater | Arthropoda | PS | Fragments | 4 EPS cups l−1 | AM | 30 min | Mortality | Significantly increased mortality | Thaysen et al., |
|
Reproduction | Significantly decreased total number of offspring; | |||||||||
Delay in time to first brood | ||||||||||
Nematoda | PS | Spheres | 10–10,000 μg l−1 | AM | 1 w | Cellular response | Significantly reduced intestinal ROS production at 10,000 μg l−1 | Zhao et al., |
||
Behavior | Significantly decreased locomotion (head trash, body bend) at 10,000 μg l−1 | |||||||||
Reproduction | Significantly decreased reproduction (brood size) at 10,000 μg l−1 |
All of the remaining studies (96%,
Toxicity assays examining chemical effects by leachates of plastic particles in organisms in (i) freshwater studies, (ii) marine studies, and (iii) total. Data depict the groups of organisms (taxa) used
Li H. X. et al. (
The development of juvenile
Studies on effects induced by the interaction of micro- and nanoplastics with pollutants on benthic organisms are scarce. The eight experiments included in the present review were conducted with marine organisms exclusively, three (38%) using annelids and arthropods and two (25%) using molluscs (
Toxicity assays examining chemical effects posed by the interaction of chemicals and plastic particles in marine benthic invertebrates. Data depict the groups of organisms (taxa) used
Devriese et al. (
Effects of contaminated plastic particles on benthic (marine) invertebrates.
Marine | Annelida | PS | Fragments | 0.074–7.4% sed. dw | PCBs | 1.84 μg kg−1 | S | Accumulation | Significantly increased accumulation of PCBs | Besseling et al., |
|
Behavior | No effects on feeding activity | ||||||||||
Mortality | No effects on mortality | ||||||||||
PVC | Fragments | 50 mg l−1 | Nonylphenol | 0.69 μg g−1 | S | Accumulation | Significantly less chemicals accumulated under PVC exposure | Browne et al., |
|||
Phenanthrene | 0.11 μg g−1 | Mortality | Significantly increased mortality by Triclosan, | ||||||||
Triclosan | 57.3 μg g−1 | no effects by Nonylphenol, Phenanthrene, PBDE-47 | |||||||||
PBDE-47 | 9.49 μg g−1 | Cellular response | Significantly reduced phagocytic activity by Nonylphenol, no effects by Phenanthrene, PBDE-47 and Triclosan; | ||||||||
Significantly reduced oxidative status by Phenanthrene, no effects by Nonylphenol, Phenanthrene PBDE-47 | |||||||||||
Behavior | Significantly reduced feeding activity by Triclosan, no effects by Nonylphenol, Phenanthrene PBDE-47 | ||||||||||
PVC | Fragments | 200 and 2,000 part. kg−1 | B(a)P | 4.58 μg kg−1 | S | Accumulation | Significantly increased accumulation of B(a)P | Gomiero et al., |
|||
Mortality | No effects on mortality | ||||||||||
Cellular response | Significantly decreased phagocytic activity at 200 part. kg−1 (28 d), and at 2,000 part. kg−1 (10 and 28 d); | ||||||||||
No effects on extracellular lysosome release; | |||||||||||
Significantly decreased mitochondrial activity at 200 part. kg−1 (28 d) and at 2,000 part. kg−1 (10 and 28 d); | |||||||||||
Significantly decreased lysosomal membrane stability (LMS); | |||||||||||
Significantly increased oxyradical production | |||||||||||
Significantly increased micronuclei frequency and DNA strand breaks; | |||||||||||
Significantly increased Lipofuscin content (28 d) and | |||||||||||
Catalase activity (10 d) | |||||||||||
Arthropoda | PE | Fragments | 0.1 g l−1 | PBDEs | 50 and 500 ng g−1 MP | AM | Accumulation | Significantly lowered accumulation of PBDEs, | Chua et al., |
||
Higher-brominated PBDEs accumulated in greater rates than lower-brominated congeners | |||||||||||
PE | Spheres | 3.1 mg l−1 | PCBs | 8.7 μg g−1 MP | Food | Accumulation | Limited effects of PE on accumulation of PCBs | Devriese et al., |
|||
Development | No effects on condition factor and nutritional state | ||||||||||
PS | Spheres | 3.1 mg l−1 | PCBs | 8.7 μg g−1 MP | Food | Accumulation | No effects of PS on accumulation of PCBs | Devriese et al., |
|||
Development | No effects on condition factor and nutritional state | ||||||||||
Mollusca | PS | Spheres | 32 μg l−1 | Fluoranthene | 30 μg l−1 | AM | Accumulation | No effects on accumulation after 7 d, significantly higher concentrations after depuration (7 d) | Paul-Pont et al., |
||
Development | Significantly higher histopathological lesions after depuration | ||||||||||
Cellular response | Lowered no. of dead hemocytes; | ||||||||||
Significantly decreased phagocytosis activity and ROS production; | |||||||||||
No effects on hemocyte and granulocyte concentration; | |||||||||||
Significantly reduced CAT activity and LPO, | |||||||||||
Significantly increased SOD, GST and GR activity after depuration; | |||||||||||
Significantly increased |
|||||||||||
Significantly increased |
|||||||||||
PS | Spheres | 32 μg l−1 | Fluoranthene | 30 μg l−1 | AM | Accumulation | No effects on accumulation after 7 d, significantly higher concentrations after depuration (7 d) | Paul-Pont et al., |
|||
Development | Significantly higher histopathological lesions after depuration | ||||||||||
Cellular response | Lowered no. of dead hemocytes; | ||||||||||
Significantly decreased phagocytosis activity and ROS production; | |||||||||||
No effects on hemocyte and granulocyte concentration; | |||||||||||
Significantly reduced CAT activity and LPO, | |||||||||||
Significantly increased SOD, GST and GR activity after depuration; | |||||||||||
Significantly increased |
|||||||||||
Significantly increased |
The cellular responses of the lugworm
Paul-Pont et al. (
An effect of combined exposure on mortality was determined in three studies (
Behavioral alterations, measured as effects on feeding activity, in the lugworm
POP accumulation and the consequences of POP co-contamination with plastic particles were examined in every study included in this part of the review (
The present review is a comprehensive analysis of studies investigating the (eco) toxicological effects of micro- and nanoplastics on benthic invertebrates in marine and in freshwater ecosystems. However, 80% (
Among the polymers used in the various assays, PS was the most commonly used: 42 vs. <10% each for other polymers, including PP, HDPE, and PVC (
Regarding the various shapes of plastic particles used to investigate the environmental burden posed, fragments were the most frequent shape (60% of overall studies), whereas spheres still accounted for around 36% of the analyzed studies, and fibers for 5% only. However, particles of primary sources, mainly manufactured as spheres, are of minor relevance in nature and rather irregularly-shaped particles, resulting from the fragmentation of larger plastic items and of materials containing synthetic polymers, are much more prevalent (e.g., Duis and Coors,
Furthermore, the exposure of benthic organisms to plastics in nature is doubtless dominated by particles in the sediments, both in marine and in freshwater ecosystems (Moore,
Even though the reviewed studies generally investigated effects of particles in a huge size range, the vast majority of studies applied microplastics, defined as particles ranging between 0.1 μm and 5 mm respectively (e.g., Thompson et al.,
The current lack of methodological standardization and harmonization greatly hampers inter-study comparisons, as already noted by Van Cauwenberghe et al. (
Even though a general comparison between the various assessed parameters in terms of their susceptibility toward nano- and microplastic exposure is difficult due to varying experimental conditions, sub-lethal parameters indicated to be more sensitive than mortality (
In conclusion, the present review identified several shortcomings that have limited a comprehensive risk assessment of the impact of micro- and nanoplastics, as well as future areas of research:
- Few studies have focused on the organisms in freshwater ecosystems, especially chemical effects are widely neglected so far. - In both marine and freshwater systems, micro- and meiobenthic organisms must be more extensively assessed. - Greater attention should be devoted to micro- and nano-sized plastics whose polymer composition, shape, surface properties, and exposure routes are those characterizing plastic particles contaminating the natural environment. - Nano-sized particles should be of concern when assessing potential effects of plastics. - Long-term assays of multiple species (e.g., model ecosystems) should be conducted to examine effects with higher ecological relevance. - Standardization of concentrations and exposure conditions are needed together with quality assessments to obtain more reliable and comparable data.
AH contributed conception and design of the review. AH, M-TM, HF, and WT organized and contributed to the database. AH wrote the first draft of the manuscript. M-TM, HF, and WT contributed to manuscript revision, read, and approved the submitted version.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
This work was supported by the German Federal Ministry of Education and Research (BMBF) as part of the Project MikroPlaTaS—Microplastics in Dams and Reservoirs: Sedimentation, Spread, Effects (BMBF grant 02W22WPL1L448D88D). We further acknowledge support for the Article Processing Charge by the Deutsche Forschungsgemeinschaft and the Open Access Publication Fund of Bielefeld University. Additionally, we would like to thank Catherine Mouneyrac and the reviewers for their comments and editorial work on the manuscript.