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,

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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.

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

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e50031, enero-diciembre 2023 (Publicado 25 de enero, 2023)

for GLMs. All analyses were run using (R Core

Team, 2016).

Finally, if the accumulation of micro-

plastics affects the structure of the sediment

(Carson et al., 2011), we expect this to favour

certain meiofaunal groups, affecting the overall

meiofaunal community composition in terms

of presence and abundance of each taxon, par-

ticularly in the mid and lower zones—where

competition is expected to be stronger. We

tested these potential differences in species

composition using a permutational multivariate

test (Permanova). A pairwise distance com-

munity matrix calculated with a Bray-Curtis

index at each intertidal level was selected as

a response variable against the same explana-

tory variables that were included in the previ-

ous models. A Bray-Curtis index was selected

as it is a widely used index that accounts for

the abundances of each taxon in the samples

(Somerfield, 2008). The analysis was run using

the function Adonis included R package vegan

v. 2.5.2 (Oksanen et al., 2018).

RESULTS

Microplastic abundance and visual

characterization: We counted a total of 1 131

microplastics on the three beaches. Fibres were

the most abundant (94.8 %), followed by foam

(2.9 %), films (1.2 %), and fragments (1.1 %)

(Fig. 2). The smallest observed microplastic

was 0.15 mm in length. The most predominant

colours were blue (39,1 %), black (28.6 %),

transparent (11.7 %), and red (9.1 %), (Fig.

2). The largest amount of microplastics was

recorded in the Santa Marta Bay (46.7 piec-

es/10 cm2) at the lower intertidal levels (45.9

pieces/10 cm2) (Table 1). However, the differ-

ences in the abundance of microsplastics were

not significant between beaches (ANOVA,

P = 0.421) or within tidal levels in the same

beaches (Table 2).

Characterization of the meiofauna and

the effect of microplastics. A total of 17 taxa

was found in the samples, being Nematoda,

Gastrotricha, Platyhelminthes, and Copepoda

the most abundant groups. It is important to

note that microplastics fibres were occasionally

observed in the intestine of larger meiofaunal

specimens (Fig. 3M, Fig. 3N). A list of the spe-

cies recorded so far for the beaches in the Santa

Marta region is summarized in Appendix 1. The

highest meiofaunal abundances were counted

in El Rodadero (2 151.8 ind/10 cm2), although

there are not significant differences with the

other beaches (ANOVA, P-value = 0.138).

Fig. 2. Types of microplastics particles found in the intertidal zone: A-C. Fibers. D. Foam. E. Fragments. F. Film.

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However, as expected, the abundance of meio-

fauna was significantly affected by intertidal

levels and the granulometric composition, with

the highest abundances registered in the mid

intertidal level (2 085.7 items/10 cm2) (Table

1, Table 2), and towards medium and fine sedi-

ments (Fig. 4, Table 2).

We found a marginally significant, nega-

tive relationship between the abundance of

meiofauna and microplastics, although with

a small estimate (GLM, estimate = -0.012,

P = 0.044). When we isolated this effect in

the different intertidal levels, this relationship

was only retained at the lower intertidal level

TABLE 1

Average and standard deviations of the abundances of microplastics and meiofauna in each beach and intertidal levels.

Beach Intertidal level Sediment

description

Average abundance

of microplastics

(Items/10 cm2)

Average abundance

of meiofauna

(Individuals/10 cm2)

Total abundance

of meiofauna

Bahía de

Santa Marta

Upper Medium Sand 27.3 ± 7.5 1 026.3 ± 470.4 3 079

Mid Coarse Sand 41.0 ± 13.1 2 569.7 ± 1 298.8 7 709

Lower Coarse Sand 37.7 ± 12.0 567.3 ± 871.0 1 702

Rodadero Upper Fine Sand 45.3 ± 22.5 1 860.7 ± 388.4 7 690

Mid Fine Sand 36.0 ± 6.2 3 186.3 ± 2 289.0 12 019

Lower Medium Sand 58.7 ± 19.7 871.7 ± 725.0 3 442

Taganga Upper Fine Sand 42.3 ± 34.4 1 361.0 ± 343.0 4 083

Mid Coarse Sand 47.3 ± 19.9 501.0 ± 184.5 1 503

Lower Coarse Sand 41.3 ± 26.3 575.3 ± 347.1 1 726

TABLE 2

Effect of the abundance of microplastics, together with the confounding factor of the granulometry and beach, on the

abundance of meiofauna at the different beach intertidal levels, according to a type II ANOVA output for generalized linear

models.

LR Chisq Estimate ± s.e. d.f. P

Total Abundance of debris 5.087 -0.013 ± 0.006 10.024

Mean grain size 20.553 0.824 ± 0.172 1< 0.001

Sediment sorting 4.265 1.143 ± 0.499 10.039

Intertidal level 11.990 NA 2< 0.01

Beach 1.912 NA 2 0.385

Upper level Abundance of microplastics 1.984 0.008 ± 0.005 1 0.159

Mean grain size 5.397 0.962 ± 0.412 1 0.021

Sediment sorting 1.583 1.279 ± 1.011 1 0.208

Beach 14.680 NA 2< 0.001

Midlevel Abundance of microplastics 0.003 -0.013 ± 0.018 1 0.9559

Mean grain size 0.203 1.626 ± 0.855 1 0.6521

Sediment sorting 0.901 -1.857 ± 1.793 1 0.3425

Beach 30.385 NA 2< 0.001

Lower level Abundance of microplastics 82.43 -0.029 ± 0.003 1< 0.001

Mean grain size 121.66 0.905 ± 0.081 1< 0.001

Sediment sorting 32.37 1.647 ± 0.282 1< 0.001

Beach 75.63 NA 2< 0.001

Abbreviations: LR Chisq, likelihood ratio chi-square values; d.f., degree of freedom; P, chi-square goodness to fit, s.e.,

standard error.

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(GLM, estimate = -0.03, P < 0.001) (Fig. 4,

Table 2).

The effect of microplastics was more con-

spicuous when the community species compo-

sition was analysed, significantly explaining the

39.3 % of the variation of the samples collected

at the lower intertidal level (PERMANOVA,

R2 = 39.3 %, P < 0.01). Other significant pre-

dictors for the community composition were

the intertidal level of the overall meiofauna

(PERMANOVA, R2 = 16.5 %, P = 0.035) and

the beach for the meiofauna collected in the

Fig. 3. Meiofauna diversity shown by examples from a variety of higher taxa. A. Nematoda, Enoplida; B. Nematoda,

Epsilonematidae; C. Platyhelminthes, Proseriata; D. Platyhelminthes, Dalyelliidae; E. Platyhelminthes, Polycladida; F.

Gastrotricha, Macrodasyidae; G. Gastrotricha, Chaetonotida; H. Annelida, Sedentaria, Ctenodrilus sp.; I. Arthropoda,

Chelicerata, Acari; J. Mollusca, Gastropoda, Microhedyle sp; K. Annelida, Clitellata, Olygochaeta, L. Tardigrada,

Heterotardigrada, Echiniscoididae; M. Annelida, Sedentaria, Saccocirrus cf. pussicus; N.-O. Saccocirrus cf. pussicus

collected from the Santa Marta region that exhibit microfibers inside their gut. Scales in A., E., H., J., K., M. 200 μm; in

C., D., N., O. 100 μm; and in B., F., G., I., L., 50 μm.

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

mid intertidal level (R2 = 16.5 %, P = 0.035)

(Table 3).

DISCUSSION

The high abundance of microplastics in

the intertidal zone of the sampled beaches is

most likely a consequence of the strong tourist

pressure, the presence of underwater outfalls

that discharge untreated wastewater, the water

from the outlets of the Manzanares and Gaira

rivers, as well as the activity of fishing and

maritime ports (Altamar et al., 2020; Fuentes-

Reines et al., 2021; Mancera-Pineda et al.,

2013). In previous studies in other coastal

areas, all these causes have been identified

as sources of debris and microplastics for the

marine environments (Talvitie et al., 2015;

Fig. 4. Graphical summary of the regression analyses. A. Boxplot showing the meiofaunal abundances in each beach and

intertidal levels. B. Relationship between the meiofaunal abundances and the mean grain size, represented as fi-coefficient

(-1 = very coarse sand, 2 = fine sand). C. Boxplot showing the abundance of microplastics in each beach and intertidal levels.

D. Relationship between the abundance of microplastics and mean grain size expressed as fi-coefficient. E. Relationship

between the abundance of meiofauna and abundance of microplastics. Plots represented with filled colour are significant.

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

Willis et al., 2017; Zubris & Richards, 2005).

Previous reports of microplastics in the Santa

Marta urban beaches (Garcés-Ordóñez et al.,

2020a; Garcés-Ordóñez et al., 2020b), have

recorded lower concentration than those of the

present study, probably because they have been

focused only on large fragments discarding the

fractions below 1 mm (Piperagkas et al., 2019).

Therefore, a comparison of the findings here

with those of these previous studies results

inappropriate due to the lack of methodological

standardization, which is a common problem in

studies associated with microplastics, and other

marine debris (Van Cauwenberghe et al., 2015).

Regarding the distribution of microplastics in

our samples, we found no significant differ-

ences between the abundance of microplastics

across intertidal levels, unlike other studies in

which the highest abundances of microplastics

have been reported for the lower level (Browne

et al., 2011; Claessens et al., 2011; Thompson

et al., 2004). This could be explained by the

high percentage of microfibers present in the

collected sample, since these are more homo-

geneously distributed in the marine environ-

ment than other microplastics, probably due to

their low density (Faraday, 2019; Liebezeit &

Dubaish, 2012; Mathallon & Hill, 2014), and

as a consequence of the small tidal amplitude

in the studied area. There was no relationship

between the grain size and microplastics con-

centrations, which is congruent with previous

studies that suggested that the distribution of

microplastics depends on the density of the

TABLE 3

Effect of the abundance of microplastics and other variables in the meiofaunal community composition.

Predictor R2P

Total Abundance of microplastics 0.021 0.699

Intertidal level 0.165 0.035

Mean grain size 0.068 0.109

Sediment sorting 0.023 0.659

Beach 0.038 0.858

Residuals 0.686

Upper Abundance of microplastics 0.146 0.205

Intertidal level 0.301 0.077

Mean grain size 0.098 0.355

Beach 0.189 0.426

Residuals 0.266

Mid Abundance of microplastics 0.085 0.229

Intertidal level 0.202 0.050

Mean grain size 0.216 0.058

Beach 0.332 0.050

Residuals 0.164

Lower Abundance of microplastics 0.393 < 0.01

Intertidal level 0.149 0.098

Mean grain size 0.142 0.133

Beach 0.128 0.466

Residuals 0.189

Results are reported from permutational multivariate analyses of variance (PERMANOVA) on the effect of different sets of

explanatory variables on community composition calculated as pairwise Bray-Curtis dissimilarities of the occurrence and

abundance of the major meiofaunal groups. Analyses are performed for all the dataset, as well as the upper, mid, and lower

intertidal levels. R2 and P values are reported. P values for significant predictors are marked in bold.

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

material as well as the biological interactions

with microbial films, and coastal physical

processes (Alomar et al., 2016; Browne et al.,

2011; Mathalon & Hill, 2014; Nor & Obbard,

2014; Wang et al., 2020).

Our results agree with other global stud-

ies (Alvarez-Zeferino et al., 2020; Browne et

al., 2011; Claessens et al., 2011; Kutralam-

Muniasamy et al., 2020; Van Cauwenberghe

et al., 2013) that found a predominance of

fibres among the types of microplastics pres-

ent in sandy beaches. However, this differs

with investigations in the Caribbean coast of

Colombia, which reported higher concentra-

tions of fragments rather than fibres; these

differences are likely to be a consequence of

different methodological approaches, as well as

the larger mesh size sieves (1–5 mm) used by

those researchers (Acosta-Coley et al., 2019;

Garcés-Ordoñez et al., 2020a; Portz et al.,

2020). In accordance with our finding, blue is

the most common colour of the microplastic

recovered from other sandy beaches around the

world (Alvarez-Zeferino et al., 2020; Hidalgo-

Ruz et al., 2012; Lots et al., 2017), followed

by black and to a lesser extent red, yellow, and

green (Alvarez-Zeferino et al., 2020; Coley

et al., 2020). Other authors, however, referred

to transparent as the dominant colour (Di &

Wang, 2018; Peng et al., 2017; Tsang et al.,

2017; Zhu et al., 2019), but this variation

could be again a methodological issue related

to the method of classification, especially if a

visual sorting is performed without confirma-

tion with other methods (e.g., Spectrometry,

micro-Raman spectroscopy). We speculate that

the abundance of blue fibres might be related

to the presence of fisheries near the localities,

given that most of the nets used by the fisher-

men in Taganga or Santa Marta Bay are made

of blue plastic polymers. However, specific

chemical analyses are necessary to confirm

this hypothesis.

Regarding the meiofauna, the average of

abundances and number of taxa were like those

recorded in other tropical sandy beaches (Fon-

seca et al., 2014; Liñero-Arana et al., 2012),

whereas the dominance of taxonomic groups

coincided with the findings of McLachlan and

Brown (2006) on reflective beaches. The high

abundances were recovered in the mid intertid-

al level, like previous studies (Ape et al., 2017;

Baia & Venekey, 2019; Fanini et al., 2020).

However, even though our study was carried

out on protected beaches, it is interesting that

the abundance of meiofauna had been signifi-

cantly affected by the intertidal level because

a weak zoning pattern is expected in protected

sandy beaches with a small tidal range (Hour-

ston et al., 2005; Pereira et al., 2018). The

significant relation between the sand grain size

and meiofauna density is also not surprising;

it has been extensively shown in other beaches

that particle size, sorting, shape, and porosity

are key factors that determine the distribution

of the meiobenthic communities (Defeo &

McLachlan, 2005; Giere, 2009; Rodríguez et

al., 2001; Rodríguez, 2004). Despite the pres-

ent study is the first evidence of the impact

of marine microplastics on meiofaunal in the

natural environments, our results agree with

recent experimental work, which have showed

a weak yet significant impact of microplastics

on the meiofauna (Wakkaf et al., 2020) attrib-

uted to the chemical toxicity of these pollut-

ants over certain species. This toxicity could

have a greater effect on organisms belonging

to certain trophic guilds, such as non-selective

filtering, or deposit and suspension feeders

that might accidentally ingest microplastics

and debris fragments (Gusmão et al., 2016).

Additionally, soft-bodied organisms with weak

cuticles that might absorb chemicals accumu-

lated in the interstitial water, or organisms that

adhere particles either directly using adhesive

glands, or indirectly by secreting viscous sub-

stances through dermis for movement can be

highly affected (Cole et al., 2013; Fueser et al.,

2020; Haegerbaeumer et al., 2019).

The impact of microplastic ingestion has

been studied in specific meiofaunal groups

(Gusmão et al., 2016) and this might explain

our results regarding abundance and com-

position at the lower intertidal level, where

some of those species (i.e., polychaete species)

might be concentrated due to the abundance of

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

microplastics. However, we propose that these

changes are not only related to the direct impact

of the microplastics, but also to the indirect

physical effect that their accumulation cause

on the sediment structure and thereby in the

selection of different species assemblages than

those occurring in microplastic free areas. Dis-

entangling such effects and isolating them from

the many other physic-chemical and anthro-

pogenic factors that synergically affect sandy

meiofaunal communities (Giere, 2019; Leasi

et al., 2018; Martínez et al., 2020; Zeppilli et

al., 2015) deserves future studies, desirably

increasing the number of localities and geo-

graphical areas, incorporating a larger number

of taxonomic operational units (morphological

species or molecular sequences produced by

next generation sequencing tools), and adding

functional information. This will alleviate local

confounding factors, as well as species-specific

effects of microplastics, explaining better the

patterns in abundance and species composi-

tion observed here (Mueller et al., 2020). By

publishing these results, yet limited to three

beaches, we hope to stimulate further research

in that direction.

There is a significant relationship between

the presence of microplastics in the sediment,

and the abundance and composition of intersti-

tial meiobenthic communities on three studied

sandy beaches. We are aware that the results

here rely on a limited sampling, and that they

will need to be evaluated more extensively.

We argue, however, that these limitations are

otherwise justified in this specific case by the

geographic particularities of the Santa Marta

region. Since we were able to find a significant

impact even with these limitations, we consider

these results relevant to inspire future research

in other areas, considering that the locations

selected in this study represent iconic examples

of the urban beaches commonly found in tropi-

cal and subtropical areas worldwide. In addi-

tion, we provide an updated checklist on the

meiofaunal taxa known from Colombian Carib-

bean beaches, including several new reports

collected during this project.

Ethical statement: the authors declare

that they all agree with this publication and

made significant contributions; that there is no

conflict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

We would like to thank Grupo de Inves-

tigación MIKU, Facultad de Ciencias Básicas,

Universidad del Magdalena, Colombia, this

study were supported by Fondo Patrimonial

para la Investigación “FONCIENCIAS” 2017

de la Universidad de Magdalena. We are in debt

to Maikon Di Domenico (Universidade Fed-

eral do Paraná), Diego Fontaneto and Stefano

Mammola (IRSA-CNR), for the comments

and suggestion provided during the elaboration

of this manuscript. We thank Anisbeth Daza

Padilla for the tardigrada identifications and

Dr. Marcela Bolanos and Joseph Dunn who

kindly improved the English of the manuscript.

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

APPENDIX 1

List of the species and genus so far recorded for the beaches in Santa Marta region.

Taxa Beach Tidal level Morphological

identification

Metabarcoding

identification Reported by:

Tardigrada Echiniscoides sp.BAH Intertidal X Here

Stygarctidae TAG Intertidal X Here

Halechiniscidae TAG Intertidal X Here

Batillipes sp. BAH Intertidal X Here

Acari Ascidae ROD Intertidal X Sevilla-Hernández

2016

Copidognathus BAH Intertidal X Sevilla-Hernández

2016

Actacarus mollis TAG Intertidal X Bartsch 1996

Actacarus uniscutatus TAG Intertidal X Bartsch 1996

Actacarus minor TAG Intertidal X Bartsch 1996

Platyhelminthes Theama cf. evelinae ROD Intertidal and

subtidal

X Here

Otoplana sp. ROD Intertidal X X Here, Castro

et al., 2021

Dalyelliidae ROD Intertidal X Here

Monocelidae ROD Intertidal X Here

Macrostomum lineare BAH, SIS Intertidal X Castro et al. 2021

Vannuccia sp. BAH Intertidal X Castro et al. 2021

Monocelis fusca ROD Intertidal X Castro et al. 2021

Postbursoplana sp. MON, SIS Intertidal X Castro et al. 2021

Adenopharynx

mitrabursalis

BAH Intertidal X Castro et al. 2021

Kymocarens sp. MON, SIS Intertidal X Castro et al. 2021

Nemertea Ototiplonemertes lactea BAH Intertidal and

subtidal

X Gonzales-Cueto

et al. 2014

Ototiplonemertes erneba BAH, ROD Intertidal X Gonzales-Cueto

et al. 2014

Ototiplonemertes sp. BAH Intertidal X Gonzales-Cueto et

al. 2014; Castro et

al 2021

Ototiplonemertes duplex TAG Intertidal X Castro et al. 2021

Cephalothrix bipunctata BAH, ROD,

MON, SIS

Intertidal X Castro et al. 2021

Annelida Claudrilus cf. corderoi BAH, SIS Intertidal X X Castro et al. 2021

Claudrilus cf. ovarium ROD Intertidal X X Castro et al. 2021

Claudrilus draco SIS Intertidal X X Castro et al. 2021

Ctenodrilus sp. TAG Subtidal X Here

Perkinsyllis sp. TAG Intertidal X Here

Protodrilus smithsoni TAG (MON) Intertidal X X Here, Castro

et al. 2021

Hesiodens gohari ROD, BAH,

TAG

Intertidal X Lagos et al. 2018

Hesionura sp.ROD , TAG Intertidial (near

rocks and algaes)

X Here

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

Taxa Beach Tidal level Morphological

identification

Metabarcoding

identification Reported by:

Mesonerilla sp. ROD Subtidal X Here

Microphthalmus cf.

mahensis

ROD Intertidal and

subtidal

XLagos et al. 2018

Nerilla antennata SIS, MON Intertidal X X Castro et al. 2021

Nerilla cf. mediterránea ROD, TAG Intertidal and

subtidal

XLagos et al. 2018

Neogyptis mediterranea ROD Intertidal X Lagos et al. 2018

Neopetitia

amphphothalma

ROD Intertidal X Lagos et al. 2018

Pettiboneia sp. TAG Intertidal X Here

Pisione

hartmannschroederae

BAH, ROD Sediments

near rocks

(max 0,3 m deep)

X Here

Pisionidens ixazaluohae MON Intertidal X X Castro et al. 2021

Pisionidens indica ROD Intertidal X Fauchald 1973

Pharyngocirrus cf.

gabriellae

ROD, BAH,

TAG

Intertidal and

subtidal

XLagos et al. 2018

Polygordius sp. BAH, TAG, Intertidal and

subtidal

X Here

Protodrilus cf. smithsoni ROD, TAG,

SIS, MON

Intertidal and

subtidal (near rocks)

X X Lagos et al. 2018;

Castro et al. 2021

Saccocrirrus cf. pussicus BAH, ROD Intertidal X X Here, Castro

et al. 2021

Schistomeringos sp. TAG Subtidal (near

rocks and algae)

X Here

Salvatoria clavata TAG Subtidal (near

rocks and algae)

X Here

Gastrotrichia Aspidiophorus sp. TAG (MON) Intertidal X Castro et al. 2021

Cephalodasys mahoae BAH, ROD Intertidal X Castro et al. 2021

Anandrodasys agadasys BAH, ROD XCastro et al. 2021

Turbanella corderoi ROD Intertidal X Hummon 1974

Cephalodasys miniceraus ROD Intertidal X Hummon 1974

Chaetonotus

(Marinochaetus) chicous

ROD Intertidal X Hummon 1974

Nematoda Desmodorella sinuata GAYR Intertidal X Reported as

Desmodora sinuata

by Lorenzen 1976a

Calomicrolaimus rugatus IS Intertidal X Lorenzen 1976b

Axonolaimus

paraspinosus

BAH Intertidal X Castro et al. 2021

Cylindrolaimus sp.BAH Intertidal X Castro et al. 2021

Punctodora ratzeburgensi BAH, MON Intertidal X Castro et al. 2021

Rhips sp. SIS Intertidal X Castro et al. 2021

Microlaimus sp.BAH, ROD,

TAG

Intertidal X Castro et al. 2021

Panagrolaimus sp. MON, SIS Intertidal X Castro et al. 2021

Siphonolaimus sp. ROD Intertidal X Castro et al. 2021

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

Taxa Beach Tidal level Morphological

identification

Metabarcoding

identification Reported by:

Diplolaimelloides meyli MON Intertidal X Castro et al. 2021

Bathylaimus sp. ROD Intertidal X Castro et al. 2021

Enoploides sp. BAH, ROD Intertidal X Castro et al. 2021

Cylicolaimus sp. SIS Intertidal X Castro et al. 2021

Mesacanthion sp. MON, SIS Intertidal X Castro et al. 2021

Halalaimus sp.BAH, ROD Intertidal X Castro et al. 2021

Xenacoelomorpha Praeconvoluta tigrina ROD Intertidal X Castro et al. 2021

Otocelis sandara ROD Intertidal X Castro et al. 2021

Paratomella unichaeta ROD Intertidal X Castro et al. 2021

Bold font: New report for Colombia. BAH: Santa Marta Bay; ROD: Rodadero Beach; TAG: Taganga Bay; MON:

Monoguaca beach; SIS: Sisiguaca Beach; Gayr: Gayraca beach, IS: Isla Salamanca.

REFERENCES

Acosta-Coley, I., Mendez-Cuadro, D., Rodríguez-Cavallo,

E., de la Rosa, J., & Olivero-Verbel, J. (2019). Trace

elements in microplastics in Cartagena: a hotspot for

plastic pollution at the Caribbean. Marine Pollution

Bulletin, 139, 402–411.

Acosta-Coley, I., & Olivero-Verbel, J. (2015). Microplastic

resin pellets on an urban tropical beach in Colombia.

Environmental Monitoring and Assessment, 187, 435.

https://doi.org/10.1007/s10661-015-4602-7

Alexeev, D. K., & Galtsova, V. V. (2012). Effect of

radioactive pollution on the biodiversity of marine

benthic ecosystems of the Russian Arctic shelf.

Polar Science, 6, 183–195. https://doi.org/10.1016/j.

polar.2012.04.001

Alves, A. S., Caetano, A., Costa, J. L., Costa, M. J., & Mar-

ques, J. C. (2015). Estuarine intertidal meiofauna and

nematode communities as indicators of ecosystem

recovery following mitigation measures. Ecological

Indicators, 54, 184–196. https://doi.org/10.1016/j.

ecolind.2015.02.013

Altamar, J., Correa-Helbrum, J., Restrepo-Leal, D., &

Robles-Algarín, C. (2020). Reconstructed data of

landings for the artisanal beach seine fishery in

the marine-coastal area of Taganga, Colombian

Caribbean Sea. Data in Brief, 30, 105604. https://doi.

org/10.1016/j.dib.2020.105604

Alomar, C., Estarellas, F., & Deudero, S. (2016).

Microplastics in the Mediterranean Sea: Deposi-

tion in coastal shallow sediments, spatial variation

and preferential grain size. Marine Environmen-

tal Research, 115, 1–10. https://doi.org/10.1016/j.

marenvres.2016.01.005

Ape, F., Sará, G., Airoldi, L., Mancuso, F., & Mirto,

S. (2017). Influence of environmental factors and

biogenic habitats on intertidal meiofauna. Hydro-

biologia, 807, 349–366. https://doi.org/10.1007%2

Fs10750-017-3410-1

Álvarez-Zeferino, J., Ojeda-Benítez, S., Cruz-Salas, A.

A., Martínez-Salvador, C., & Vázquez-Morillas, A.

(2020). Microplastics in Mexican beaches. Resou-

rces, Conservation & Recycling, 1551, 104633.

https://doi.org/10.1016/j.resconrec.2019.104633

Buchanan, J. B. (1984). Sediment analysis. In N. A.,

Holme, & A. D. McIntyre (Eds.), Methods for the

Study of Marine Benthos (pp. 41–63). Blackwell

Scientific Publications.

Browne, M. A., Crump, P., Niven, S. J., Teuten, E. L.,

Tonkin, A., Galloway, T., & Thompson, R. C. (2011).

Accumulations of microplastic on shorelines world-

wide: sources and sinks. Environmental Science &

Technology, 45, 9175−9179. https://doi.org/10.1021/

es201811s

Bezerra, T. N. C., Genevois, B., & Fonsêca-Genevois, V.

(1997). Influência da granulometria na distribuição

e adaptação da meiofauna na praia arenosa do Istmo

de Olinda PE. In S. A. Silva, P. A. Grohmann & A.

M. Esteves (Eds.), Ecologia de Praias Arenosas do

Litoral Brasileiro (pp. 107–116). Programa de Pós-

Graduação em Ecologia da UFRJ.

Baia, E., & Venekey, V. (2019). Distribution patterns of

meiofauna on a tropical macrotidal sandy beach,

with special focus on nematodes (Caixa d’Água,

Amazon Coast, Brazil). Brazilian Journal of Ocea-

nography, 67, e19230. https://doi.org/10.1590/

s1679-87592019023006701

Bartsch, I. (1996). Halacarid mites (Acari) from the Mid-

Atlantic Ridge. New Records. Cahiers de Biologie

Marine, 37, 159–167.

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

Botero, C. M., & Zienliski, S. (2020). The implementation

of a world-famous tourism ecolabel triggers political

support for beach management. Tour Management

Perspectives, 35, 100691. https://doi.org/10.1016/j.

tmp.2020.100691

Curini-Galletti, M., Artois, T., Delogu, V., De Smet, W.

H., Fontaneto, D., Jondelius, U., Leasi, F., Martínez,

A., Meyer-Wachsmuth, I., Nilsson, K. S., Tongiorgi,

P., Worsaae, K., & Todaro, M. A. (2012). Patterns

of Diversity in Soft-Bodied Meiofauna: Dispersal

Ability and Body Size Matte. PLoS One, 7, e33801.

https://doi.org/10.1371/journal.pone.0033801

Carson, H. S., Colbert, S. L., Kaylor, M. J., & McDermid,

K. J. (2011). Small plastic debris changes water

movement and heat transfer through beach sediments.

Marine Pollution Bulletin, 62, 1708–1713. https://doi.

org/10.1016/j.marpolbul.2011.05.032

Claessens, M., De Meester, S., Van Landuyt, L., De

Clerck, K., & Janssen, C. R. (2011). Occurrence

and distribution of microplastics in marine sedi-

ments along the Belgian coast. Marine Pollution

Bulletin, 62, 2199–2204. https://doi.org/10.1016/j.

marpolbul.2011.06.030

Coley, R., Hardiman, G., & O’Driscolla, K. (2020).

Microplastics in the marine environment: A review

of their sources, distribution processes, uptake and

exchange in ecosystems. Case Studies in Chemical

and Environmental Engineering, 2, 100010. https://

doi.org/10.1016/j.cscee.2020.100010

Cannon, S. M. E., Lavers, J., & Figueireda, B. (2016).

Plastic ingestion by fish in the southern hemisphere: a

baseline study and review of methods. Marine Pollu-

tion Bulletin, 107, 286–291. https://doi.org/10.1016/j.

marpolbul.2016.03.057

Cole, M., Lindeque, P. K., Fileman, E. S., Halsband, C.,

Goodhead, R., Moger, J., & Galloway, T. S. (2013).

Microplastic ingestion by zooplankton. Environmen-

tal Science & Technology, 47, 6646–6655. https://doi.

org/10.1021/es400663f

Cole, M., Lindeque, P., Halsband, C., & Galloway, T.

S. (2011). Microplastics as contaminants in the

marine environment: a review. Marine Pollution

Bulletin, 62, 2588–2597. https://doi.org/10.1016/j.

marpolbul.2011.09.025

Correa, I., & Morton, R. (2010). Caribbean Coast of

Colombia. In E.C. F. Bird (Ed.), Encyclopedia of the

World’s Coastal Landforms (pp. 259–264). Springer.

Castro, L. R., Meyer, R. S., Shapiro, B., Shirazi, S.,

Cutler, S., Lagos, A. M., & Quiroga, S. Y. (2021).

Metabarcoding meiofauna biodiversity assessment

in four beaches of Northern Colombia: effects of

sampling protocols and primer choice. Hydrobio-

logia, 848, 3407–3426. https://doi.org/10.1007/

s10750-021-04576-z

Derraik, J. G. B. (2002). The pollution of the marine envi-

ronment by plastic debris: a review. Marine Pollu-

tion Bulletin, 44, 842–852. https://doi.org/10.1016/

S0025-326X(02)00220-5

Desforges, J. P. W., Galbraith, M., & Ross, P. S. (2015).

Ingestion of microplastics by zooplankton in the

northeast Pacific Ocean. Archives of Environmental

Contamination and Toxicology, 69, 320–330. https://

doi.org/10.1007/s00244-015-0172-5

Defeo, O., & McLachlan, A. (2005). Patterns, processes and

regulatory mechanisms in sandy beach macrofauna: a

multiscale analysis. Marine Ecology Progress Series,

295, 1–20. https://doi.org/10.3354/meps295001

Di, M., & Wang, J. (2018). Microplastic in surface waters

and sediments of the Three Gorges Reservoir, China.

Science of the Total Environment, 616, 1620–1627.

https://doi.org/10.1016/j.scitotenv.2017.10.150

Faraday, S. (2019). Microplastics as a new, ubiquitous

pollutant: Strategies to anticipate management and

advise seafood consumers. Marine Policy, 104, 103–

107. https://doi.org/10.1016/j.marpol.2019.02.020

Fauchald, K. (1973). Polychaetes from Central American

sandy beaches. Bulletin of the Southern California

Academy of Sciences, 72(1), 19–31.

Fossi, M. C., Coppola, D., Baini, M., Giannetti, M.,

Guerranti, C., Marsili, L., Panti, C., de Sabata, E.,

& Clo, S. (2014). Large filter feeding marine orga-

nisms as indicators of microplastic in the pelagic

environment: the case studies of the Mediterra-

nean basking shark (Cetorhinus maximus) and fin

whale (Balaenoptera physalus). Marine Environmen-

tal Research, 100, 17-24. https://doi.org/10.1016/j.

marenvres.2014.02.002

Fanini, L., Defeo, O., & Elliott, M. (2020). Advances in

sandy beach research – Local and global perspectives.

Estuarine, Coastal and Shelf Science, 234, 106646.

https://doi.org/10.1016/j.ecss.2020.106646

Fonseca, G., Norenburg, J., & Di Domenico, M. (2014).

Diversity of marine meiofauna on the coast of Bra-

zil. Marine Biodiversity, 44, 459–462. https://doi.

org/10.1007/s12526-014-0261-0

Folk, R. L., & Ward, W. C. (1957). A study in the

significance of grain-size parameters. Jour-

nal of Sedimentary Petrology, 27, 3–26. https://

doi.org/10.1306/74D70646-2B21-11D7-

8648000102C1865D

Fueser, H., Mueller, M. T., & Traunspurger, W. (2020).

Ingestion of microplastics by meiobenthic communi-

ties in small-scale microcosm experiments. Science

of the Total Environment, 746, 141276. https://doi.

org/10.1016/j.scitotenv.2020.141276

Fueser, H., Mueller, M. T., Weiss, L., Höss, S., & Trauns-

purger, W. (2019). Ingestion of microplastics by

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

nematodes depends on feeding strategy and buccal

cavity size. Environmental Pollution, 255, 113227.

https://doi.org/10.1016/j.envpol.2019.113227

Fuentes-Reines, J. M., Suárez-Morales, E., & Eslava-

Eljaiek, P. (2021). Occurrence of Notodiaptomus

maracaibensis Kiefer, 1954 (Copepoda, Calanoida,

Diaptomidae) from an ephemeral pond in northern

Colombia. Intropica, 16(2), 125–132. https://doi.

org/10.21676/23897864.3977

Giere, O. (2009). Meiobenthology: The microscopic motile

fauna of aquatic sediments (2nd ed.). Springer-Verlag.

Giere, O. (2019). Future trend lines in ecological meio-

benthos research. In O. Giere (Ed.), Perspectives in

Meiobenthology Reviews, Reflections and Conclu-

sions (pp. 37–49). Springer-Verlag.

González-Cueto, J., Quiroga, S., & Norenburg, J. (2014).

A shore-based preliminary survey of marine rib-

bon worms (Nemertea) from the Caribbean coast

of Colombia. ZooKeys, 439, 83–108. https://doi.

org/10.3897/zookeys.439.5965

Gusmão, F., Domenico, M. D., Amaral, A. C. Z., Martí-

nez, A., Gonzalez, B. C., Worsaae, K., do Sul, J. A.

I., & da Cunha-Lana, P. (2016). In situ ingestion

of microfibres by meiofauna from sandy beaches.

Marine Pollution Bulletin, 216, 584-590. https://doi.

org/10.1016/j.envpol.2016.06.015

Garcés-Ordóñez, O., Espinosa, L., Pereira, R., Barroso, B.,

& Meigikos, R. (2020b). Plastic litter pollution along

sandy beaches in the Caribbean and Pacific coast of

Colombia. Environmental Pollution, 267, 115495.

Garcés-Ordóñez, O., Espinosa, L., Pereira, R., & Costa, M.

(2020a). The impact of tourism on marine litter pollu-

tion on Santa Marta beaches, Colombian Caribbean.

Marine Pollution Bulletin, 160, 111558. https://doi.

org/10.1016/j.marpolbul.2020.111558

García, F., Palacio, C., & García, U. (2011). Constituyentes

de marea en la bahía de Santa Marta (Colombia).

Dyna, 78, 142–150.

Gheskiere, T., Vincx, M., Weslawski, J. M., Scapini, F.,

& Degraer, S. (2005). Meiofauna as descriptor of

tourism-induced changes at sandy beaches. Marine

Environmental Research, 60, 245–265. https://doi.

org/10.1016/j.marenvres.2004.10.006

Haegerbaeumer, A., Mueller, M. T., Fueser, H., & Trauns-

purger, W. (2019). Impacts of micro- and nano-sized

plastic particles on benthic invertebrates: A literature

review and gap analysis. Frontiers of Environmen-

tal Science & Engineering, 7, 1–33. https://doi.

org/10.3389/fenvs.2019.00017

Hourston, M., Warwick, R. M., Valesini, F. J., & Potter, I.

C. (2005). To what extent are the characteristics of

nematode assemblages in nearshore sediments on the

west Australian coast related to habitat type, season

and zone? Estuarine, Coastal and Shelf Science, 64,

601–612. https://doi.org/10.1016/j.ecss.2005.04.001

Hidalgo-Ruz, V., Gutow. L., Thompson, R. C., & Thiel,

M. (2012). Microplastics in the marine environment:

a review of the methods used for identification and

quantification. Environmental Science & Technology,

46, 3060–3075. https://doi.org/10.1021/es2031505

Hummon, W. (1974). Intertidal marine Gastrotricha from

Colombia. Bulletin of Marine Science, 24, 396–408.

de Jonge, V. N., & Bouwman, L. A. (1977). A simple den-

sity Kennedy: A rapid-freezing method separation

technique for quantitative isolation of meiobenthos

using the colloidal silica Ludox-TM. Marine Biology,

42, 143–148.

Kutralam-Muniasamy, G., Pérez-Guevara, F., Elizalde-

Martínez, I., & Shruti, V. C. (2020). Review of

current trends, advances and analytical challenges

for microplastics contamination in Latin America.

Environmental Pollution, 267, 115463. https://doi.

org/10.1016/j.envpol.2020.115463

Lagos, A. M. (2018). Meiofauna intermareal de la región

de Santa Marta (Tesis de Maestría). Universidad

Nacional de Colombia, Colombia.

Lagos, A. M., Leon, M. V., Quiroga, S., & Martínez, A.

(2018). Interstitial annelids from the Caribbean coast

of Colombia. Revista de Biología Tropical, 66, 658-

673. http://doi.org/10.15517/rbt.v66i2.33399

Leasi, F., Sevigny, J. L., Laflamme, E. M., Artois, T.,

Curini-Galletti, M., Navarrete, A., Di Domenico,

M., Goetz, F., Hall, J. A., Hochberg, R., Jörger, K.

M., Jondelius, U., Todaro, M. A., Wirshing, H. H.,

Norenburg, L. J., & Thomas, W. K. (2018). Biodi-

versity estimates and ecological interpretations of

meiofaunal communities are biased by the taxonomic

approach. Communications Biology, 1, 1-12. http://

doi.org/10.1038/s42003-018-0119-2

Li, H. X., Getzinger, G. J., Ferguson, P. L., Orihuela, B.,

Zhu, M., & Rittschof, D. (2016). Effects of toxic lea-

chate from commercial plastics on larval survival and

settlement of the barnacle Amphibalanus amphitrite.

Environmental Science & Technology, 5, 924–931.

https://doi.org/10.1021/acs.est.5b02781

Liebezeit, G., & Dubaish, F. (2012). Microplastics in

beaches of the East Frisian islands Spiekeroog and

Kachelotplate. Bulletin of Environmental Conta-

mination and Toxicology, 89, 213-217. https://doi.

org/10.1007/s00128-012-0642-7

Liñero-Arana, I., Ojeda, S., & Amaro, M. E. (2012).

Variación espacio-temporal de la meiofauna subma-

real en una playa arenosa nororiental de Venezuela.

Revista de Biología Tropical, 61, 59-73.

Lorenzen, S. (1976a). Desmodoridae (nematoden) mit

extrem lange spicula aus South America. Mitteilungen

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

aus dem Instituto Colombo-Alemán Investigaciones

Científicas Punta Betín, 8, 63–78.

Lorenzen, S. (1976b). Calomicrolaimus rugatus n. gen.,

n.sp. (Desmodoridae, nematodos) in Sandy beaches.

Mitteilungen aus dem Instituto Colombo-Alemán

Investigaciones Científicas Punta Betín, 8, 79–82.

Lots, F. A. E., Behrens, P., Vijver, M. G., Horton, A. A.,

& Bosker, T. (2017). A large-scale investigation of

microplastic contamination: Abundance and charac-

teristics of microplastics in European beach sediment.

Marine Pollution Bulletin, 123, 219-226. https://doi.

org/10.1016/j.marpolbul.2017.08.057

Lu, K., Qiao, R., An, H., & Zhang, Y. (2018). Influence of

microplastics on the accumulation and chronic toxic

effects of cadmium in zebrafish (Danio rerio). Che-

mosphere, 202, 514–520. https://doi.org/10.1016/j.

chemosphere.2018.03.145

Lusher, A. (2015). Microplastics in the Marine Environ-

ment: Distribution, Interactions and Effects, In M.

Bergmann, L. Gutow, & M. Klages (Eds.), Marine

Anthropogenic Litter (pp. 245–307). Springer Inter-

national Publishing.

Mathalon, A., & Hill, P. (2014). Microplastic f ibers in the inter-

tidal ecosystem sur- rounding Halifax Harbor, Nova

Scotia. Marine Polluttion Bulletin, 81, 69–79. https://

doi.org/10.1016/j.marpolbul.2014.02.018

McLachlan, A., & Brown, A. C. (2006). The ecology of

sandy shores. Academic Press.

Martínez, A., Di Domenic, M., Leasi, F., Curini-Galletti,

M., Todaro, M. A., Dal Zotto, M., Gobert, S., Artois,

T., Norenburg, J., Jörger, K., Núñez, J., Fontaneto, D.,

& Worsaae, K. (2019). Patterns of diversity of soft-

bodied meiofauna in an oceanic island, Lanzarote

(Canary Islands). Marine Biodiversity, 49, 2033–

2055. https://doi.org/10.1007/s12526-019-01007-0

Martínez, A., Eckert, E. M., Artois, T., Careddu, G., Casu,

M., Curini-Galletti, M., Gazale, V., Gobert, S., Iva-

nenko, V. N., Jondelius, U., Marzano, M., Pesole, G.,

Zanello, A., Todaro, M. A., & Fontaneto, D. (2020).

Human access impacts biodiversity of microscopic

animals in sandy beaches. Communications Biology,

3, 1-9. https://doi.org/10.1038/s42003-020-0912-6

Mueller, M. T., Fueser, H., Höss, S., & Traunspurger,

W. (2020). Species-specific effects of long-term

microplastic exposure on the population growth

of nematodes, with a focus on microplastic inges-

tion. Ecological Indicators, 118, 106698. https://doi.

org/10.1016/j.ecolind.2020.106698

Mancera-Pineda, J. E. M., Pinto, G., & Vilardy, S. (2013).

Patrones de distribución estacional de masas de agua

en la bahía de Santa Marta, Caribe colombiano:

importancia relativa del upwelling y outwelling.

Bulletin of Marine and Coastal Research, 2, 329–360.

https://doi.org/10.25268/bimc.invemar.2013.42.2.55

MSFD-TSGML. (2013). Guidance on monitoring of mari-

ne litter in European Seas: a guidance document

within the common implementation strategy for the

marine strategy framework directive. EUR-26113 EN.

JRC Scientific and Policy Reports JRC83985. https://

mcc.jrc.ec.europa.eu/documents/201702074014.pdf

Nadal, M. A., Alomar, C., & Deudero, S. (2016). High

levels of microplastic ingestion by the semipelagic

fish Bogue Boops boops (L.) around the Balea-

ric Islands. Environmental Pollution, 214, 517–523.

https://doi.org/10.1016/j.envpol.2016.04.054

Nor, N. H. M., & Obbard, J. (2014). Microplastics in

Singapore’s coastal mangrove ecosystem. Mari-

ne Pollution Bulletin, 79, 278–283. https://doi.

org/10.1016/j.marpolbul.2013.11.025

Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R.,

Legendre, P., McGlinn, D., Minchin, P. R., O’Hara, R.

B., Simpson, G. L., Solymos, P., Stevens, M. H. H.,

Szoecs, E., & WagnerVegan, H. (2018). Community

Ecology Package. R package version 2, 5–2. https://

CRAN.R-project.org/package=vegan

Ogonowski, M., Schür, C., Jarsén, Å., & Gorokhova,

E. (2016). The effects of natural and anthropoge-

nic microparticles on individual fitness in Daph-

nia magna. PLoS One, 11, e0155063. https://doi.

org/10.1371/journal.pone.0155063

Pereira, T. J., Gingold, R., Villegas, A. D. M., & Rocha-

Olivares, A. (2018). Patterns of spatial variation of

meiofauna in sandy beaches of Northwestern Mexico

with contrasting levels of disturbance. Thalassas, 34,

53–63. https://doi.org/10.1007/s41208-017-0038-x

Piperagkas, O., Papageorgiou, N., & Karakassis, I. (2019).

Qualitative and quantitative assessment of micro-

plastics in three sandy Mediterranean beaches, inclu-

ding different methodological approaches. Estuarine,

Coastal and Shelf Science, 219, 169–175. https://doi.

org/10.1016/j.ecss.2019.02.016

Portz, L., Portantiolo-Manzolli, R., Vasquez-Herrera, G.,

Laiton-Garcia, L., Villate, D. A., & do Sul, J. A. I.

(2020). Marine litter arrived: Distribution and poten-

tial sources on an unpopulated atoll in the Seaflower

Biosphere Reserve, Caribbean Sea. Marine Pollution

Bulletin, 157, 111323.

Peng, G., Zhu, B., Yang, D., Su, L., Shi, L., & Li, D.

(2017). Microplastic in sediments of the Changjaiang

Estuary, China. Environmental Pollution, 225, 283–

290. https://doi.org/10.1016/j.envpol.2016.12.064

R Core Team. (2016). R: A language and environment for

statistical computing. R Foundation for Statistical

Computing. Vienna, Austria. https://www.R-project.

org/

Rodríguez, J. G. (2004). Community structure of intertidal

meiofauna along a gradient of morphodynamic states

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

on an exposed North Sea beach. Sarsia, 89, 22–32.

https://doi.org/10.1080/00364820310003307

Rochman, C. M., Hoh, E., Kurobe, T., & The, S. J. (2013).

Ingested plastic transfers hazardous chemicals to fish

and induces hepatic stress. Scientific Reports, 3, 1–7.

https://doi.org/10.1038/srep03263

Rodríguez, J. G., López, J., & Jaramillo, E. (2001). Com-

munity structure of the intertidal meiofauna along

a gradient of morphodynamic sandy beach types in

southern Chile. Revista Chilena de Historia Natural,

74, 885–897.

Rangel-Buitrago, N. G., Anfuso, G., & Williams, A. T.

(2015). Coastal erosion along the Caribbean coast

of Colombia: magnitudes, causes and management.

Ocean & Coastal Management, 114, 129–144.

https://doi.org/10.1016/j.ocecoaman.2015.06.024

Rangel-Buitrago, N. G., Ruiz, A. G., & López, N. T. (2019).

Grain–size analysis and characterization of sedimen-

tary environments of the Sierra Nevada de Santa

Marta (SNSM) coastal zone, caribbean of Colombia.

Revista ITTPA, 1, 13–19.

Rubio-Polanía, J. C., & Trujillo-Arcila, C. A. (2013).

Características granulométricas de los fondos blan-

dos en un área de la bahía de Taganga (Colombia)

influenciada por la instalación de refugios bentó-

nicos. Revista U.D.C.A, 16, 193-203. https://doi.

org/10.31910/rudca.v16.n1.2013.875

Somerfield, P. (2008). Identification of the Bray-Curtis

similarity index: Comment on Yoshioka (2008). Mari-

ne Ecology Progress Series, 372, 303-306. https://doi.

org/10.3354/meps07841

Sevilla-Hernández, M. (2016). Ácaros marinos (Arach-

nida: Acari) asociados al alga Ulva lactuca de la

bahía de Taganga (Santa Marta, Colombia) (Tesis de

Bachillerato). Universidad del Magdalena, Colombia.

Setälä, O., Fleming-Lehtinen, V., & Lehtiniemi, M. (2014).

Ingestion and transfer of microplastics in the plank-

tonic food web. Environmental Pollution, 185, 77–83.

https://doi.org/10.1016/j.envpol.2013.10.013

Strungaru, S. A., Jijie, R., Nicoara, M., Plavan, G., &

Faggio, C. (2019) Micro- (nano) plastics in fres-

hwater ecosystems: abundance, toxicological impact

and quantification methodology. TrAC Trends in

Analytical Chemistry, 110, 116–128. https://doi.

org/10.1016/j.trac.2018.10.025

Talvitie, J., Heinonen, M., Pääkkönen, J. P., Vahtera, E.,

Mikola, A., Setälä, O., & Vahala, R. (2015). Do

wastewater treatment plants act as a potential point

source of microplastics? Preliminary study in the

coastal Gulf of Finland, Baltic Sea. Water Science &

Technology, 72, 1495–1504. https://doi.org/10.2166/

wst.2015.360

Tsang, Y. Y., Mak, C. W., Liebich, C., Lam, S. W., Sze,

E. T., & Chan, K. M. (2017). Microplastic pollution

in the maine eater and sediments of Hong Kong.

Marine Pollution Bulletin, 115, 20–28. https://doi.

org/10.1016/j.marpolbul.2016.11.003

Thompson, R. C., Olsen, Y., Mitchell, R. P., Davis, A.,

Rowland, S. J., John, A. W. G., McGonigle, D., &

Russell, A. E. (2004). Lost at sea: where is all the

plastic? Science, 304, 838.

Van Cauwenberghe, L., Claessens, M., Vandegehuchte, M.

B., & Janssen, C. R. (2015). Microplastics are taken

up by mussels (Mytilus edulis) and lugworms (Areni-

cola marina) living in natural habitats. Environmen-

tal Pollution, 199, 10–17. https://doi.org/10.1016/j.

envpol.2015.01.008

Van Cauwenberghe, L., Vanreusel, A., Mees, J., Janssen,

C. R. (2013). Microplastic pollution in deep-sea

sediments. Environmental Pollution, 182, 495–499.

https://doi.org/10.1016/j.envpol.2013.08.013

Von Moos, N., Burkhardt-Holm, P., & Koehler, A. (2012).

Uptake and effects of microplastics on cells and

tissue of the blue mussel Mytilus edulis L. after an

experimental exposure. Environmental Science &

Technology, 46, 327–335. https://doi.org/10.1021/

es302332w

Wakkaf, T., Allouche, M., Harrath, A. H., Mansour, L.,

Alwasel, S., Thameemul-Ansari, K. G. M., Beyrem,

H., Sellami, B., & Boufahja, F. (2020). The individual

and combined effects of cadmium, polyvinyl chloride

(PVC) microplastics and their polyalkylamines modi-

fied forms on meiobenthic features in a microcosm.

Environmental Pollution, 266, 115263. https://doi.

org/10.1016/j.envpol.2020.115263

Wesch, C., Bredimus, K., Paulus, M., & Klein, R. (2016)

Towards the suitable monitoring of ingestion of

microplastics by marine biota: a review. Envi-

ronmental Pollution, 218, 1200-1208. https://doi.

org/10.1016/j.envpol.2016.08.076

Wright, L. D., Chappell, J., Thom, B. G., Bradshaw, M. P.,

& Cowell, P. (1979). Morphodynamics of reflective

and dissipative beach and inshore systems: southeas-

tern Australia. Marine Geology, 32, 105–140. https://

doi.org/10.1016/0025-3227(79)90149-X

Willis, K. A., Eriksen, R., Wilcox, C., & Hardesty, B. D.

(2017). Microplastic distribution at different sediment

depths in an urban estuary. Frontiers in Marine Scien-

ce, 4, 419. https:/doi.org/10.3389/fmars.2017.00419

Wang, T., Hu, M., Song, L., Yu, J., Liu, R., Wang, S., Wang,

Z., Sokolova, I. M., Huang, W., & Wang, Y. (2020).

Coastal zone use influences the spatial distribution of

microplastics in Hangzhou Bay, China. Environmen-

tal Pollution, 266, 115137. https://doi.org/10.1016/j.

envpol.2020.115137

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

Wright, S. L., Rowe, D., Thompson, R. C., & Galloway,

T. S. (2013). Microplastic ingestion decreases

energy reserves in marine worms. Current Bio-

logy, 23, R1031-R1033. https://doi.org/10.1016/j.

cub.2013.10.068

Wright, L. D., & Short, A. D. (1984). Morphodynamic

variability of surf zones and beaches: a synthe-

sis. Marine Geology, 56, 93–118. https://doi.

org/10.1016/0025-3227(84)90008-2

Zubris, K. A. V., & Richards, B. K. (2005). Synthetic

fibers as an indicator of land application of sludge.

Environmental Pollution, 138, 201–211. https://doi.

org/10.1016/j.envpol.2005.04.013

Zeppilli, D., Sarrazin, J., Leduc, D., Martinéz-Arbizu,

P., Fontaneto, D., Fontanier, C., Gooday, A. J.,

Kristensen, R. M., Ivanenko, V. N., Sørensen, M. V.,

Vanreusel, A., Thébault, J., Mea, M., Allio, N., Andro,

T., Arvigo, A., Castrec, J., Danielo, M., Foulon, V.,

Fumeron, R., Hermabessiere, L., Hulot, V., James, T.,

Langonne-Augen, R., Le Bot, T., Long, M., Maha-

bror, D., Morel, Q., Pantalos, M., Pouplard, E., Rai-

mondeau, L., Rio-Cabello, A., Seite, S., Traisnel, G.,

Urvoy, K., Van Der Stegen, T., Weyand, M., & Fer-

nandes, D. (2015). Is the meiofauna a good indicator

for climate change and anthropogenic impact. Marine

Biodiversity, 45, 505–535. https://doi.org/10.1007/

s12526-015-0359-z

Zhu, L., Wang, H., Chen, B., Sun, X., Qu, K., & Xia,

B. (2019). Microplastic ingestion in deep-sea fish

from the South China Sea. Science of the Total Envi-

ronment, 677, 493–501. https://doi.org/10.1016/j.

scitotenv.2019.04.380