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

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e50031, enero-diciembre 2023 (Publicado 25 de enero, 2023)

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,

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e50031, enero-diciembre 2023 (Publicado 25 de enero, 2023)

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.

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