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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e50031, enero-diciembre 2023 (Publicado 25 de enero, 2023)
Effects of microplastics pollution on the abundance
and composition of interstitial meiofauna
Ana Milena Lagos1*; https://orcid.org/0000-0002-0009-6036
M. Victoria Leon1; https://orcid.org/0000-0002-0016-2515
Angie Colorado1; https://orcid.org/0000-0002-5883-9197
Daniel Giraldo1; https://orcid.org/0000-0003-2969-458X
Laura Fragozo1; https://orcid.org/0000-0002-6944-0587
Sigmer Y. Quiroga1; https://orcid.org/0000-0002-3321-1360
Alejandro Martínez2; https://orcid.org/0000-0003-0073-3688
1. Grupo de Investigación MIKU, Facultad de Ciencias Básicas, Universidad del Magdalena, Carrera 32 No 22-08, Santa
Marta D.T.C.H., Colombia; anamilagos@gmail.com, mvleon0221@gmail.com, angi.colorado@gmail.com,
danifergiraldo@gmail.com, lau.fragozo@gmail.com, sigmerquiroga@unimagdalena.edu.co
2. Molecular Ecology Group (MEG), Water Research Institute (IRSA), National Research Council of Italy (CNR),
Verbania, Italy; amartinez.ull@gmail.com
Received 02-VI-2022. Corrected 15-IX-2022. Accepted 04-I-2023.
ABSTRACT
Introduction: Pollution by microplastics is a global problem in marine environments, which impacts microor-
ganisms and ecosystems at several spatial levels. Sandy beaches are depositional environments where microplas-
tics tend to accumulate in large quantities. The co-occurrence of interstitial meiofauna and microplastics in sand
grains raises the question on whether the accumulation of microplastics in the sediments affects the abundance
and composition of the meiofaunal communities.
Objective: To test the hypothesis that microplastics affect the meiofauna of urban sandy beaches.
Methods: We studied the three main urban sandy beaches of Santa Marta, Colombia: El Rodadero, Santa Marta
Bay, and Taganga. All are similar in morphology and external pressures, and differ from other beaches in the
region. In April 2019 we collected 81 sand samples, equally distributed in the intertidal zone (upper, mid, and
lower intertidal levels). We applied generalized linear models to abundance, and multivariate permutational tests
to community composition.
Results: We identified 17 taxonomic groups of meiofauna, and microplastic particles (mainly 45-500 micron
fibres) evenly distributed across beaches and intertidal levels. There was more meiofauna at the mid intertidal
level, and in fine and medium grain sediment. At the lower intertidal level, sites with more microplastics had less
meiofauna. Abundance of microplastics explained 39 % of the variation in meiofaunal community composition
at lower intertidal levels.
Conclusions: The accumulation of microplastics might have a negative impact on these meiofaunal interstitial
communities. This is not surprising: if microplastics occupy the same physical space as these animals, they might
presumably modify the structure of sediments and the composition of interstitial water.
Key words: benthos; coastal zone; meiofauna abundance; microplastic abundance; pollution effect; sandy
beaches.
https://doi.org/10.15517/rev.biol.trop..v71i1.50031
AQUATIC ECOLOGY
2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e50031, enero-diciembre 2023 (Publicado 25 de enero, 2023)
INTRODUCTION
The presence of microplastics (particles
of sizes below 5 mm) in marine ecosystems
and even in organisms, has been recognized
for years as a global environmental problem
(MSFD-TSGML, 2013). This problem is par-
ticularly serious in the ocean, where large
amounts of microplastics accumulate and per-
sist for a long time (Thompson et al., 2004;
Van Cauwenberghe et al., 2015). Microplastics
threaten marine ecosystems mainly due to
their inclusion in marine food webs through
ingestion (Wesch et al., 2016; Wright et al.,
2013), causing a negative impact on different
organisms. These impacts are both physical,
due to the accumulation of plastics inside
organisms (Cannon et al., 2016; Desforges et
al., 2015; Fossi et al., 2014; Nadal et al., 2016;
Ogonowski et al., 2016; Strungaru et al., 2019;
Von Moos et al., 2012) and chemical, produced
by the toxicity of plastic additives and contami-
nants that are adsorbed (Fossi et al., 2014; Li et
al., 2016; Lu et al., 2018; Rochman et al., 2013;
RESUMEN
Efectos de la contaminación por microplásticos en la abundancia
y composición de la meiofauna intersticial
Introducción: La contaminación por microplásticos es un problema global en los ecosistemas marinos, con
impacto sobre microorganismos y ecosistemas en varios niveles espaciales. Las playas arenosas son ambientes
de deposición donde se tiende a acumular gran cantidad de microplásticos. La co-ocurrencia de meiofauna
intersticial y microplásticos en granos de arena plantea la pregunta de que si la acumulación de microplásticos
en sedimentos afecta la abundancia y composición de comunidades de meiofauna.
Objetivo: Probar la hipótesis de que microplásticos afectan la meiofauna de playas arenosas urbanas.
Métodos: Estudiamos las tres principales playas arenosas urbanas de Santa Marta, Colombia: El Rodadero,
Bahía Santa Marta y Taganga. Estas son similares en morfología y presiones externas, y difieren de las otras pla-
yas de la región. En abril 2019 recolectamos 81 muestras de arena, distribuidas de manera equidistante en la zona
intermareal (nivel intermareal superior, medio y bajo). Aplicamos modelos lineales generalizados de abundancia,
y pruebas permutacionales multivariantes a la composición de comunidades.
Resultados: Identificamos 17 grupos taxonómicos de meiofauna, y partículas de microplástico (principalmente
fibras de 45-500 micras) distribuidos equitativamente a lo largo de las playas y niveles intermareales. Hubo más
meiofauna en el nivel intermareal medio, y en sedimentos de grano mediano y fino. A niveles intermareales más
bajos, sitios con más microplásticos tuvieron menos meiofauna. La abundancia de los microplásticos explicó el
39 % de la variación en comunidades de meiofauna a niveles intermareales bajos.
Conclusión: La acumulación de microplásticos podría tener un impacto negativo sobre las comunidades de mei-
ofauna intersticial. Esto no es de sorprender: si los microplásticos ocupan el mismo volumen físico que estos ani-
males, estos podrían presuntamente modificar la estructura de sedimentos y la composición del agua intersticial.
Palabras clave: bentos; zona costera; abundancia de meiofauna; abundancia de microplásticos; efecto de con-
taminación; playas arenosas.
Setälä et al., 2014). Although microplastics are
ubiquitous in the water column and sediments
across a wide bathymetric range, including
deep water (Faraday, 2019), these problems are
more acute along populated coastlines (Cole
et al., 2011), where microplastics are more
abundant. In these areas, the accumulation of
microplastics is influenced by their own physi-
cal characteristics, such as size and density, but
also by external environmental factors, such as
rainfall, hydrological changes, tidal zones, and
even stochastic storm (Lusher, 2015).
The general risk of microplastic contami-
nation along seacoasts is increased by the
proximity of land-based sources of contamina-
tion (Mathallon & Hill, 2014), which include
infrastructures linked to the port industry, tour-
istic development, and coastal urbanization.
In Latin America, the problem is exacerbated
by the high population density in the coastal
areas combined with a poor waste manage-
ment and lack of wastewater treatment in many
regions (Derraik, 2002; Kutralam-Muniasamy
et al., 2020). In this sense, urban beaches are
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environments that are especially susceptible to
this type of pollution. On one hand, beaches are
in fact, depositional environments that natural-
ly accumulate particles carried by surrounding
areas, including microplastics (Acosta-Coley
& Olivero-Verbel, 2015). In Latin America,
urban beaches are not only exploited as mass
tourist destinations but are also highly urban-
ized and subject to heavy industrial activi-
ties, such as ports or fisheries, making them
particularly vulnerable (Wright et al., 1979;
Wright & Short ,1984). Therefore, the impact
of microplastics pollution on urban beaches
often acts synergically with other human-driv-
en impacts, such as erosion and trampling,
collectively affecting local conditions, leading
to changes in the composition and variation of
the structure of the benthic communities and, in
particular the interstitial meiofauna (Gheskiere
et al., 2005; Martínez et al., 2020; Rangel-
Buitrago et al., 2015).
Interstitial meiofauna is an important com-
ponent of the biodiversity on marine sand
beaches, due to its high taxonomic richness and
abundance. Unfortunately, meiofaunal animals
are often neglected in biodiversity studies,
as their characterization requires specialized
sampling techniques and taxonomic expertise
(Curini-Galletti et al., 2012; Martínez et al.,
2019). This neglect is problematic not only
because it produces biased information about
actual biodiversity in many regions, but also
an incomplete view of ecosystem functioning.
Meiofaunal organisms provide important ser-
vices in marine ecosystems, such as the transfer
of energy from microbial production to higher
trophic levels, thus catalysing many geochemi-
cal processes in coastal environments (Giere,
2009). Meiofaunal assemblages comprise
almost all animal phyla, responding differential-
ly to specific physical-chemical environmental
factors and often showing a faster response
to changes (Zeppilli et al., 2015). Therefore,
studying the abundance and composition of
meiofaunal communities remains as a valuable
tool for environmental assessments, since they
allow a rapid detection of different types of
impacts at different temporal and spatial scales
(Alexeev & Galtsova, 2012; Alves et al., 2015).
Surprisingly, although experimental work has
shown that meiofauna are affected by micro-
plastics in different marine habitats (Fueser et
al., 2019; Fueser et al., 2020; Mueller et al.,
2020; Wakaff et al., 2020), few studies have
focused on the specific impact of microplastics
on the interstitial meiofaunal communities in
natural environments. Large accumulations of
microplastics in the marine sediment affects its
structure, and therefore (Carson et al., 2011)
could also affect the meiofauna.
Our case of study relies on several quali-
tative surveys done over the last ten years
around the coastal areas of Santa Marta, in
which different beaches have been sampled to
describe the diversity of organisms. These stud-
ies collectively forecasted the richness of the
meiofaunal communities in the sandy beaches
of Santa Marta region (Castro et al., 2021;
González-Cueto et al., 2014; Lagos et al., 2018;
Lagos, 2018; Sevilla-Hernández, 2016), and
highlighted the presence of microfibers and
debris. The co-occurrence of meiofauna and
microplastics raises the question on whether the
accumulation of microplastics in the sediments
might affect the abundance and composition of
the meiofaunal communities inhabiting those
beaches (Carson et al., 2011).
The main goal of this study is to investigate
the distribution of microplastics, in the three
main urban sandy beaches of the Santa Marta
region (Colombia), all with similar impacts in
terms of tourism, population, and wastewater
discharge. Our main hypothesis is that, since
microplastics are deposit in the sediment modi-
fying its structure, they might have an effect on
the abundance and composition of the intersti-
tial meiofaunal communities on these beaches.
MATERIALS AND METHODS
Area of study: This study was focused on
the only three beaches accessible in a radius
of 10 km from Santa Marta, Northern Colom-
bia, which exhibit a comparable sedimentary
regime and are affected by similar human-driv-
en impacts, such as erosion and trampling,
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allowing us to isolate the changes produced
only by the local variation of debris in the
sediment (Gheskiere et al., 2005; Martínez et
al., 2020; Rangel-Buitrago et al., 2015). These
urban sandy beaches in Santa Marta are: El
Rodadero, Santa Marta Bay, and Taganga (Fig.
1). All of them are pocket reflective beaches
with sparse swell, and narrow tide range, com-
posed of coarse to medium-fine sand eroded
from adjacent foothills of the Sierra Nevada
de Santa Marta (Correa & Morton, 2010; Gar-
cía et al., 2011; Rangel-Buitrago et al., 2019;
Rubio-Polanía & Trujillo-Arcila, 2013). They
are all subjected to strong tourism, population,
and fishermen pressure (Botero & Zienliski,
2020). The three investigated beaches are simi-
lar to each other, while they differ from other
sandy beaches in the region.
Sampling: Sampling was performed in
April 2019. Three sites were selected along
each beach. Three spots were sampled in each
site, corresponding to the lower, mid and upper
level of the intertidal zone. Three adjacent
samples were collected in each spot: one for
microplastics quantification, another for the
meiofaunal community characterization, and
a third for granulometric analysis. A total of
81 samples were studied, 27 for each beach.
Samples for microplastics and meiofauna were
collected using a 10-cm-high steel corer with
3.5 cm of inner diameter (Buchanan, 1984;
Piperagkas et al., 2019). Granulometric sam-
ples were collected using a steel shovel.
Sample processing: Debris were extract-
ed using the flotation method adapted from
Thompson et al. (2004). Each sample was
deposited in a 1 l glass conical flask, gauged
with a supersaturated saline solution (1.2 kg/l),
and stirred during 3 min at 200 rpm. After
allowing the mixture to settle for 10 min, the
supernatant was vacuum filtered through a
membrane filter (MCE). This process was
repeated four times for each sample. All parti-
cles were separated from the filter and visually
categorized using a DIC microscope (Hidalgo-
Ruz et al., 2012). To avoid contamination, we
minimized the exposure of each sample, which
remained sealed during most of the processing.
All containers and beakers were rinsed with
distilled water prior and after being used, and
reagents were prepared with molecular graded
milli-q water and periodically tested to confirm
they were plastic-free.
Fig. 1. Santa Marta region. The three sampled urban beaches are highlighted in red.
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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e50031, enero-diciembre 2023 (Publicado 25 de enero, 2023)
Samples for meiofauna were anesthetized
for 10 minutes in an isotonic 7.4 % magnesium
chloride solution, fixed using a 4 % solution of
buffered formalin, and dyed with Rose Bengal
to facilitate the counting. Fixed samples were
rinsed over a two-sieve stack of 500 and 45 μm.
The fraction retained by the 45 μm sieve was
mixed with LUDOX-TM solution (specific
density 1.15 g/cm3), successively centrifuge,
and decanted four times to extract all the
meiofaunal organisms (De Jonge & Bouwman,
1977), which were then identified and counted
under a Leica WILD M8 stereomicroscope.
Granulometry was evaluated from 300 g
of sediment, previously homogenized and dried
in an oven at 80 °C for 24 hours. The sediment
was sieved through a standard stack of six
sieves, and after 15 min, the fraction retained
in each sieve was weighted. Mean grain size
and sorting coefficient were calculated with the
software Gradistat (Bezerra et al., 1997; Folk &
Ward, 1957). The results were expressed using
the Wentworth fi coefficients for the mean
grain size (Giere, 2009).
Statistical analyses: Our first goal was to
understand the variation of microplastics and
meiofauna in our samples, accounting for the
effect across beaches, as well as for the different
intertidal levels and granulometry within each
beach. We expect that comparable amounts of
microplastics will arrive to each beach, as well
as a homogeneous deposition in the sediment
across the intertidal zone favoured by the small
tidal amplitude in the Santa Marta region. We
tested this hypothesis in two steps. First, we
assessed whether the homogeneous distribution
of marine microplastics and meiofauna across
beaches held true using an analysis of variance
(ANOVA); and then, we tested the effect of the
granulometry and tidal level at each beach on
the meiofauna and microplastics abundances
using generalized linear models (GLM). Abun-
dance of microplastics and meiofauna were
selected as response variable for those models,
while we considered the intertidal levels (cate-
gorical: upper, mid, lower) and the two continu-
ous granulometric parameters (mean grain size,
sorting coefficient) as response variables. The
abundance of microplastics was included as an
additional explanatory variable when the total
abundance of meiofauna was the response vari-
able. Beaches were included explicitly in each
model to account for unmeasured differences
between them. Beaches were not included as
a random effect due to the low number of rep-
licates. A negative binomial distribution was
assumed for each model to account for the over
dispersion of our response variable consisting
of counting data.
Our second goal was to explicitly investi-
gate the effect of the abundance of microplastics
at each intertidal level on the meiofaunal abun-
dances. Meiofauna and microplastics occur
together in the spaces amongst the sand, poten-
tially competing for the same space. There-
fore, we expect a reduction, yet small, of the
meiofaunal abundances in those samples with a
higher amount of microplastics. We expect this
reduction to be stronger in the mid and lower
levels, where meiofauna achieved the highest
abundances thereby increasing competition for
the space. We used again generalized linear
models to test this hypothesis, selecting the
abundances of meiofauna at each tidal zone
as the response variable. Total abundance of
microplastics and the two granulometric con-
tinuous variables (mean grain size, sorting) in
each intertidal level were selected as explana-
tory variables. As above, beaches were included
as an additional explicit factor; and a negative
binomial distribution was included to account
for the over dispersion of the counting data.
Before performing these two sets of anal-
yses, we checked whether the explanatory
variables were not correlated. After obtaining
the results, we checked the model fit by visu-
ally confirming the normal distribution of
the residuals, the absence of deviation in the
residual versus fitted plot, Q-Q plot, and plot of
Cook’s distances. The results are presented in
Analyses of Deviance Tables, as they show the
effect of each variable, calculating the signifi-
cance using likelihood ratio (LR) chi-square
tests for GLMs and Wald (W) chi-square tests