Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58577, enero-diciembre 2024 (Publicado Ago. 22, 2024)

Supralittoral isopod (Oniscidea) diversity at three ecoregions along the

Colombian Caribbean: useful data for environmental management

Carlos Mario López-Orozco1,2*; https://orcid.org/0000-0002-3251-7739

Yesenia M. Carpio-Díaz1,2; https://orcid.org/0000-0001-5116-9736

Ricardo Borja-Arrieta1,2; https://orcid.org/0000-0002-5064-5080

Ivanklin Soares Campos-Filho3; https://orcid.org/0000-0001-6139-8241

Carlos Taboada-Verona4; https://orcid.org/0000-0002-0341-4845

Gabriel R. Navas-S.5; https://orcid.org/0000-0001-9554-6345

1. Laboratório de Estudos Subterrâneos, Universidade Federal de São Carlos, São Carlos, São Paulo, Brazil; clopezo1610@

gmail.com (*Correspondence), ycarpiodiaz@gmail.com; rborjaa@unicartagena.edu.co

2. Grupo de Investigación en Biología Descriptiva y Aplicada, Universidad de Cartagena, Programa de Biología, Campus

San Pablo, Cartagena de Indias, Colombia.

3. Department of Biological Sciences, University of Cyprus, Lefkosia (Nicosia), Cyprus; ivanklin.filho@gmail.com

4. Universidad de Sucre, Sincelejo, Colombia; carlostaboada87@gmail.com

5. Grupo de Investigación Hidrobiología, Universidad de Cartagena, Programa de Biología, Campus San Pablo,

Cartagena de Indias, Colombia; gnavass@unicartagena.edu.co

Received 30-I-2024. Corrected 23-V-2024. Accepted 12-VIII-2024.

ABSTRACT

Introduction: Terrestrial isopods (Oniscidea) play important roles in the ecological processes of the soil in tropi-

cal ecosystems and are employed as indicators of environmental impact. Despite their importance, studies on the

ecology of this suborder in the Neotropics are scarce.

Objective: To assess spatial changes in alpha and beta diversity of Oniscidea in the supralittoral zone across

Archipiélagos Coralinos (ARCO), Magdalena (MAG), and Morrosquillo (MOR) ecoregions in the Colombian

Caribbean.

Methods: We conducted Direct Intuitive Searches of specimens and measured soil temperature and moisture in

19 transects with logs, leaf litter, coral remains, and decomposing plant material.

Results: A total of 1 970 individuals representing 17 species were collected, with Tylidae, Halophilosciidae,

and Ligiidae being the most abundant families. Alpha diversity orders were higher in ARCO than MAG and

MOR ecoregions. MAG and MOR differed in observed richness. The structure of the assemblage varied in

dominant species and abundances. In ARCO, the indicator species were Tylos niveus, Littorophiloscia denticu-

lata, Halophiloscia trichoniscoides, and Ligia baudiniana; in MOR, it was Tylos marcuzzii, and in MAG, it was

Littorophiloscia tropicalis. High beta diversity (> 60 %), with significant differences in the assemblage structure

among ecoregions, was confirmed by the NMDS, which distinctly separated each group. CCA analysis revealed

a negative relationship between most species with soil temperature and moisture, with a positive relationship

observed with T. marcuzzii.

Conclusions: This is the first effort to describe spatial changes in the diversity of oniscideans in the supralittoral

zone of the Neotropical region, providing a baseline for future studies. This information could be instrumental

in identifying priority areas for conservation efforts.

Key words: terrestrial isopods; woodlice; coastal ecosystems; Caribbean ecoregions; spatial diversity.

https://doi.org/10.15517/rev.biol.trop..v72i1.58577

CONSERVATION

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e58577, enero-diciembre 2024 (Publicado Ago. 22, 2024)

INTRODUCTION

Knowledge of Colombia’s marine biodi-

versity has improved in recent decades due to

expeditions in the Colombian Caribbean rang-

ing from 20 to 900 m (Díaz & Acero, 2003).

These efforts have significantly contributed to

our understanding of marine biodiversity, espe-

cially in deeper areas. Several studies along this

coastal zone revealed a high species richness

within taxonomic groups like corals, crusta-

ceans, mollusks, and echinoderms (Benavides-

Serrato et al., 2011; Díaz & Puyana, 1994;

Lemaitre, 1981; Martínez-Campos et al., 2017;

Núñez et al., 1999; Reyes et al., 2010). However,

there are still gaps in information regarding the

spatial patterns of diversity in the assemblages

of other faunal groups along the marine coast of

the Caribbean and the Colombian Pacific, par-

ticularly those associated with the supralittoral

zone (Batista-Morales & Díaz-Sánchez, 2011).

This zone is defined as the area of the coastline

above the high tide line, including the high tide

berm where plant material and debris deposited

by the sea accumulate. The supralittoral zone

extends up to the cliffs, dunes, coastal ridges,

and both rocky and sandy coastlines (Ceballos-

Fonseca, 2009). In this area, various types of

microhabitats favorable for edaphic fauna may

be found, including decomposing plant mate-

rial (such as logs, leaf litter, algae), bark of living

trees and their roots, herbaceous plants, rocks,

coral remains, and sand (Núñez et al., 1999;

Schultz, 1972).

Terrestrial isopods (Oniscidea) are a

unique lineage among crustaceans, adapting

entirely to terrestrial habitats and considered

an important detritivore component of the

edaphic fauna, particularly in tropical habitats

(Leistikow, 2001; Schmalfuss, 2003; Hornung,

2011; Richardson & Araujo, 2015; Taiti, 2018).

The group encompasses over 4,000 described

species in more than 500 genera within 38 or

39 families, distributed across almost all terres-

trial environments, making it one of the richest

groups within Isopoda (Campos-Filho & Taiti,

2021; Dimitriou et al., 2019; Lins et al., 2017;

Sfenthourakis & Taiti, 2015).

RESUMEN

Diversidad de isópodos supralitorales (Oniscidea) en tres ecorregiones

a lo largo del Caribe colombiano: datos útiles para la gestión ambiental

Introducción: Los isópodos terrestres (Oniscidea) juegan un papel importante en los procesos ecológicos del

suelo en ecosistemas tropicales y han sido empleados como indicadores de impacto ambiental. A pesar de su

importancia, los estudios sobre la ecología de este suborden en el Neotrópico son escasos.

Objetivo: Evaluar los cambios espaciales en la diversidad alfa y beta de Oniscidea en la zona supralitoral en

las ecorregiones Archipiélagos Coralinos (ARCO), Magdalena (MAG) y Morrosquillo (MOR) en el Caribe

colombiano.

Métodos: Realizamos Búsquedas Intuitivas Directas de especímenes y medimos la temperatura y la humedad del

suelo en 19 transectos con troncos, hojarasca, restos de coral y material vegetal en descomposición.

Resultados: Recolectamos un total de 1 970 individuos representando 17 especies, siendo Tylidae, Halophilosciidae

y Ligiidae las familias más abundantes. Los órdenes de diversidad alfa fueron mayores en ARCO, en comparación

con las ecorregiones MAG y MOR. MAG y MOR difirieron en la riqueza observada. La estructura del ensam-

blaje varió en especies dominantes y sus abundancias. En ARCO las especies indicadoras fueron Tylos niveus,

Littorophiloscia denticulata, Halophiloscia trichoniscoides y Ligia baudiniana; en MOR fue Tylos marcuzzii y en

MAG fue Littorophiloscia tropicalis. El NMDS confirmó una alta diversidad beta (> 60%), con diferencias en la

estructura del ensamblaje entre ecorregiones, que separó claramente cada grupo. El ACC reveló una relación

negativa entre la mayoría de las especies con la temperatura y humedad del suelo, observándose una relación

positiva con T. marcuzzii.

Conclusiones: Este es el primer esfuerzo por describir los cambios espaciales en la diversidad de oniscídeos en la

zona supralitoral de la región Neotropical, proporcionando una línea base para futuros estudios. Esta información

podría ser fundamental para identificar áreas prioritarias para los esfuerzos de conservación.

Palabras clave: isópodos terrestres; cochinillas; ecosistemas costeros; ecorregiones del Caribe; diversidad espacial.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58577, enero-diciembre 2024 (Publicado Ago. 22, 2024)

Alongside other members of the edaphic

fauna, the oniscideans play a key role in soil for-

mation and nutrient recycling (Abd El-Wakeil,

2015; Ŝpaldoňová & Frouz, 2014; Zimmer &

Topp, 1999). Many species within this group are

utilized as model organisms in research on ecol-

ogy (Hamaïed & Charfi-Cheikhrouha, 2004;

Sfenthourakis et al., 2005; Sghaïer & Charfi-

Cheikhrouha, 2002), reproduction (Araujo &

Bond-Buckup, 2005), and physiology (Lesěr

et al., 2008), and they are considered valuable

indicators of environmental impact (Longo et

al., 2013; Paoletti & Hassall, 1999; Solomou et

al., 2019). The dynamics of terrestrial isopod

populations and assemblages are significantly

influenced by environmental factors such as

temperature and humidity, impacting their sur-

vival, growth, and reproduction (Leistikow,

2001; Messina et al., 2016; Rushton & Hassall,

1987; Solomou et al., 2019; Zimmer, 2005).

While studies on distribution patterns and

spatial changes in terrestrial isopods diversity

have been conducted in the Palearctic region,

particularly in mountainous areas, oases, and

wetlands (e.g., Gabsi et al., 2024; Khemaissia et

al., 2012a, Khemaissia et al., 2016, Khemaissia

et al., 2017; Sfenthourakis, 1993, Sfenthourakis,

1996a, Sfenthourakis, 1996b; Sfenthourakis &

Legakis, 2001; Sfenthourakis & Triantis, 2009;

Sfenthourakis et al., 2008), the research con-

ducted in the Neotropical supralittoral zone has

primarily focused on taxonomy, with no prior

investigations into the spatial patterns of this

group’s assemblage (e.g., López-Orozco et al.,

2022; Paoletti & Stinner, 1989; Schultz, 1972;

Schultz 1984; Schultz & Johnson, 1984; Taiti et

al., 2018). Similarly, there is a limited number

of studies investigating distribution patterns of

species in the different marine ecoregions of

the country within the supralittoral zone. Most

studies conducted in the region have focused

on the slope and continental shelf at depths

ranging from 20 to 1 000 meters and in some

cases, there are no known works on groups

that inhabit the supralittoral zone (e.g., Bena-

vides-Serrato & Borrero-Pérez, 2010; Merchán-

Cepeda et al., 2009; Navas et al., 2010; Navas et

al., 2013; Vides, 2011).

This study aims to evaluate the spatial

changes in alpha and beta diversity within

the terrestrial isopod assemblage across three

marine ecoregions of the Colombian Caribbe-

an. Additionally, it seeks to examine abundance

gradients in relation to soil temperature and

moisture. The obtained information will serve

as a key input for proposing plans dedicated to

the conservation, management, and sustainable

use of this group of organisms, representing

opportunities to provide insights into the com-

position, structure, function, and dynamics of

ecological systems.

MATERIAL AND METHODS

Study area: The Colombian Caribbean

coast spans from 11°50’ N-71°18’ W in Cas-

tilletes to 08°42’ N- 7°19’ W in Cabo Tiburón,

covering an approximate length of 1 600 km

(Fig. 1). IDEAM et al. (2007) assert that the

Colombian Caribbean Sea Province is locat-

ed in the Marine Biogeographic Region of

the Western Tropical Atlantic (Spalding et al.,

2007), encompassing two ecozones (Carib-

bean Continental Shelf and Caribaná Talud).

These represent uniform sectors of the seabed,

characterized by significant geomorphological

features that group distinct biota types. The

marine coast of the Colombian Caribbean is

divided into eight ecoregions, the lowest level

of regionalization for marine systems. Ecore-

gions are delimited based on factors includ-

ing the degree of continental influence, coast

geomorphology, sediment types, water masses

outcrops, wave energy levels, presence of eco-

logical units, biological productivity of the

water column, and type of coastal ecosystems,

and are located in the ecozone Caribbean Con-

tinental Shelf (Fig. 1) (Díaz & Acero, 2003).

This study focuses on three ecoregions in

the central part of the Colombian Caribbean

(Fig. 1): 1. Coral Archipelagos (ARCO), char-

acterized by clear waters, hosting a high species

richness, and feature diverse habitats, including

coral reefs, seaweed beds, bioclastic sand flats,

and mangroves on some islands; 2. Magdalena

(MAG), highly influenced by the discharges of

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e58577, enero-diciembre 2024 (Publicado Ago. 22, 2024)

the Magdalena River, characterized by strong

sediment loads and low salinity levels; and,

3. Gulf of Morrosquillo (MOR), affected by

continental discharges through the Canal del

Dique and the Sinú River, characterized by

fine sediments and mangrove ecosystems (Díaz

& Acero, 2003). Three sampling stations in

each ecoregion were stablished, selected a

priori based on Google Earth and available

basic cartography maps, following three main

criteria: 1. Existence of cliffs, dunes, coastal

remains, rocky, or sandy coastline; 2. Low level

of anthropic intervention; and 3. Ease of access.

Supplementary Information SMT1 and SMF1

present the characteristics and photographs,

respectively, of the different sampling stations,

and Fig. 1 shows their geographical location.

Sampling and taxonomic identification:

Sampling was conducted between September

and November 2022. At each sampling station,

a visit was made, and Direct Intuitive Searches

(DIS) were performed, which involved search-

ing for terrestrial isopods in key sites or micro-

habitats (such as leaf litter, logs, coral remains,

and decomposing plant material) for 10 min-

utes per observer (two observers) (Karasawa,

2022; Taiti & Wynne, 2015). Ten repetitions

were conducted in each microhabitat, spaced

at least 15 meters apart to ensure data indepen-

dence. This resulted in 1.65 hours of searching

per microhabitat per observer at each station.

The samples were collected manually, and all

search sites were delimited to 1 m2 with a PVC

quadrant. It is important to note that there was

Fig. 1. Sampling stations in each of the ecoregions under study. ARCO, Coralline Archipelagos Ecoregion; MAG, Magdalena

Ecoregion; MOR, Gulf of Morrosquillo Ecoregion. Shapefile from the ecoregions provided by INVEMAR.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58577, enero-diciembre 2024 (Publicado Ago. 22, 2024)

no delimitation of the microhabitats, and the

sites were selected considering the complete-

ness of the microhabitat greater than 90%

within the sampling station. In each microhabi-

tat, soil temperature and moisture data were

recorded using a YAXU N03654 soil thermohy-

drometer, and substrate information was noted.

Moreover, three replicate measurements per

parameter were conducted.

The material was identified using mor-

phological characters using micropreparations

(microscope glass slides) in Hoyer’s medium

(Anderson, 1954), following Carpio-Díaz et al.

(2016), Carpio-Díaz et al. (2023), López-Orozco

et al. (2014), López-Orozco et al. (2022), and

Taiti et al. (2018). The collected material was

deposited in the research laboratories of the

Grupo de Investigación Hidrobiología of the

University of Cartagena, Cartagena, Colombia,

with catalog numbers between CBUDC-CRU

408 and CBUDC-CRU 492.

Data analysis: We analyzed three transects

of logs, three of coral remains, and two of leaf

litter in ARCO; three of logs and two of decom-

posing plant material in MAG; and three of

logs, two of decomposing plant material, and

one of leaf litter in MOR. Richness was treated

as the total number of species per transect, and

abundance as the total number of individuals

captured. We evaluated the completeness of the

sampling by applying the approach of Chao et

al. (2014), using extrapolation-interpolation

curves on the rarefaction and coverage of the

sample. This is based on the first-order diver-

sity according to Hill numbers (q = 0), utilizing

the abundance data, following the propos-

als by Chao et al. (2014) and Colwell et al.

(2012). Alpha diversity was evaluated using the

effective numbers of species (q0, q1, and q2)

for each site, representing the three diversity

orders: q0, the number of species observed; q1,

the exponential of the Shannon index; and q2,

the inverse of the Simpson index. For each q

order, 95 % confidence intervals were obtained

with 500 bootstrap pseudoreplicates, and alpha

diversity profiles were constructed. These anal-

yses were performed using RStudio v4.2.0 with

the “iNEXT” package and the online iNEXT

tool (Chao et al., 2016; Hsieh et al., 2016; R

Core Team, 2020). Additionally, to compare

the patterns of richness, abundance, and uni-

formity between sites, rank/abundance curves

were performed with the abundance data trans-

formed using Log10, following the proposal of

Whittaker (1972).

Following the proposal of Moreno et al.

(2011), the q values were compared based on

the magnitude of their differences (MD) with

the modifications of Cultid-Medina & Escobar

(2016) and Cultid-Medina & Escobar (2019),

taking into account that the values obtained

for the completeness of the sampling in each of

the sites according to the coverage curves (100

% in each case). This method considers that it

is possible to compare diversity estimates (qD

± 95 % CI) under the same sampling cover-

age, allowing the principle of replication to be

respected and to calculate how many times one

assemblage is more or less diverse than another.

This measurement is calculated in percentage

terms using the following equation: % MD =

100 – [(qD sample 2 * 100) / qD sample 1].

In that sense, when sample 1 is more diverse

than sample 2, the MD percentage will be posi-

tive; otherwise, it will be negative. MD varies

between 0 (no change in pairwise diversity)

and ± 100 % (completely different diversity).

The MD values were compared visually, and the

interpretation of the comparisons is comple-

mentary to that of the 95% confidence interval

(Cultid-Medina & Escobar, 2016; Cultid-Medi-

na & Escobar, 2019).

Beta diversity and its components were

evaluated using the proposal of (Baselga, 2010;

Baselga, 2013; Baselga, 2017), implementing

the functions beta.multi.abund and beta.pair.

abund, with the Bray-Curtis index through

the “betapart” package in RStudio (Baselga,

2013; Baselga, 2017; Baselga & Orme, 2012; R

Core Team, 2020). To determine if there were

significant differences in the composition and

abundance of the species assemblage between

the ecoregions, a Permutational Analysis of

Variance (PERMANOVA) of one-way was per-

formed based on the similarities of Bray-Curtis

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e58577, enero-diciembre 2024 (Publicado Ago. 22, 2024)

index with 999 permutations in the software

PAST v4.12 (Anderson, 2001; Hammer et al.,

2001). Additionally, the matrix of abundances

by transects was transformed to the square root

to reduce the weight of the dominant species,

and a similarity matrix was calculated using the

Bray-Curtis index, and an ordination was car-

ried out using a Non-metric Multidimensional

Scaling analysis (NMDS), to explore possible

relationships between transects per ecoregion.

This analysis was performed using RStudio

v4.2.0 with the package “vegan” (Oksanen et

al., 2014; R Core Team, 2020). Graphics of

alpha and beta diversity were performed in

RStudio v4.2.0 using the “ggplot2” package

(Wickham, 2016).

Characteristic or indicator species of the

ecoregions were identified using the indica-

tor species analysis (IndVal %). This method

consists of determining the species’ affinity for

a specific environment, site, or habitat. The

measure is based on fidelity (relative frequency)

and specificity (relative abundance) and obtains

its maximum value (100 %) when a species is

found only at one site and in all its samples

(Dufrêne & Legendre, 1997). Species with Ind-

Val ≥ 50 % and with statistical significance (P

< 0.05) were considered as indicators. These

analyses were performed in the software PAST

v4.12 (Hammer et al., 2001).

A non-parametric Kruskall-Wallis test was

performed (after confirmation of normality

using the Shapiro-Wilk test and homogeneity

of variances using the Levene test), to iden-

tify possible differences between the ecore-

gions regarding soil temperature and moisture

(P < 0.05). Subsequently, to identify between

which pairs of ecoregions the differences exist-

ed, a Wilcoxon post-hoc test was applied (P

< 0.05). This analysis was performed in RStu-

dio v4.2.0 (R Core Team, 2020). Canonical

Correspondence Analysis (CCA) was used to

detect possible relationships between species

and environmental variables (soil moisture and

temperature), following the procedures of Leg-

endre & Legendre (1998) in the software PAST

v4.12, using type 2 scaling, which emphasizes

the relationship between species and variables.

The P-values for each eigenvalue were obtained

using 999 permutations (Braak & Verdon-

schot, 1995; Hammer et al., 2001; Legendre &

Legendre, 1998). Species with an abundance of

fewer than 20 individuals were excluded from

this analysis.

RESULTS

We collected 1 970 individuals, distributed

across three ecoregions: ARCO (1 166), MOR

(533), and MAG (271), representing nine fami-

lies and 17 species, two of which are classified

as Incertae sedis (Table 1). The families with

the greatest richness were Tylidae (N = 1 109,

56.3 %), Halophilosciidae (N = 598, 30.3 %),

and Detonidae (N = 43, 2.2 %), each with three

species. The genera Tylos Audouin, 1826 and

Armadilloniscus Uljanin, 1875 presented the

highest number of species, each with three.

However, Tylos contributed 56.3 %, and Arma-

dilloniscus 2.2 % in terms of abundance.

Sampling coverage was 100 % in each

ecoregion, indicating a high efficiency of the

implemented methodology in capturing ter-

restrial isopods (Fig. 2A). Rarefaction and

extrapolation curves, based on the number of

individuals, revealed that doubling the sample

size would yield the same sampling complete-

ness in MAG and MOR ecoregions. However,

for the ARCO ecoregion, there would possibly

be one more species (16.2 estimated) with a 95

% confidence interval. Additionally, richness

exhibited consistent behavior across ecoregions

(Fig. 2B).

In terms of species richness, ARCO

revealed 10 additional species compared to

MOR and eight more than MAG. Moreover,

ARCO boasts 2.8 and 3.5 more effective species

than MAG and MOR, respectively. Regarding

dominant effective species, ARCO outpaced

MAG by 1.8 and MOR by 2.2. Consequently,

ARCO demonstrated superior richness, diversi-

ty, and dominance. Additionally, MAG yielded

two more species than MOR, with comparable

values in terms of effective and dominant spe-

cies (Fig. 2C). Pairwise differences were con-

sistently positive for ARCO across all diversity

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58577, enero-diciembre 2024 (Publicado Ago. 22, 2024)

orders, being greater between ARCO and MOR

(q0 = 66.7 %, q1 = 63.1 %, q2 = 59.9 %), than

between ARCO and MAG (q0 = 53.3 %, q1 =

49.6 %, q2 = 49.2 %). Between MAG and MOR,

the greatest difference was observed in terms of

richness (q0 = 28.6 %), with no clear differences

in terms of Shannon’s exponential (q1 = 26.7 %)

and inverse of Simpson’s (q2 = 21.2 %).

The assemblage in ARCO has four domi-

nant species, differing from MAG and MOR,

where one species had the greatest number

of individuals. The species with the highest

abundances were Tylos niveus, Littorophilos-

cia tropicalis, Halophiloscia trichoniscoides, and

Ligia baudiniana in ARCO ecoregion; Tylos

marcuzzii in MOR; and L. tropicalis in MAG

(Fig. 2D). The abundance of these species rep-

resents 84.4 % of the total.

We found that total beta diversity between

ecoregions (βBC = 82.7 %), was modulated to

Table 1

Composition and abundance of terrestrial isopod assemblages in the Coralline Archipelagos (ARCO), Magdalena (MAG),

and Gulf of Morrosquillo (MOR) ecoregions.

Family/Species ARCO-

ARCO-

MOR-

MAG-

Ligiidae

Ligia baudiniana Milne-Edwards, 1840 31 60 24 _ 10 _ 20 5 _

Tylidae

Tylos marcuzzii Giordani Soika, 1954 _ _ 11 389 1 40 _ 4 _

Tylos negroi López-Orozco,

Carpio-Díaz & Campos-Filho, 2022 4 31 20 18 23 _ 20 7 _

Tylos niveus Budde-Lund, 1885 438 26 77 _ _ _ _ _ _

Stenoniscidae

Stenoniscus nestori López-Orozco,

Taiti & Campos-Filho, 2022 1________

Detonidae

Armadilloniscus luisi Carpio-Díaz,

Taiti & Campos-Filho, 2022 _ 5 3 _ _ _ _ _ _

Armadilloniscus ninae Schultz, 1984 _ 2 3 _ _ _ _ _ _

Armadilloniscus caraibicus Paoletti & Stinner, 1989 1 _ 29 _ _ _ _ _ _

Halophilosciidae

Halophiloscia trichoniscoides (Vandel, 1973) 41 _ 91 _ _ _ _ _ _

Littorophiloscia denticulata (Ferrara & Taiti, 1982) 13 35 17 _ _ _ 7 _ _

Littorophiloscia tropicalis Taiti & Ferrara, 1986 36 91 49 17 3 5 121 36 36

Platyarthridae

Trichorhina bermudezae Carpio-Díaz,

López-Orozco & Campos-Filho, 2018 21________

Trichorhina heterophthalma Lemos de Castro, 1964 1________

Porcellionidae

Porcellionides pruinosus (Brandt, 1833) 3________

Armadillidae

Ctenorillo tuberosus (Budde-Lund, 1904) _ _ _ _ 27 _ 3 _ _

Incertae sedis

Buchnerillo neotropicalis Taiti,

Montesanto & Vargas, 2018 _ _ _ _ _ _ 10 _ 2

Buchnerillo sp. _ 1 1 _ _ _ _ _ _

Abundance 590 251 325 424 64 45 181 52 38

Richness 11 8 11 3 5 2 6 4 2

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a greater extent by the balanced variation in

abundance (βBC:BAL = 67.6 %) than the abun-

dance gradient (βBC:GRA = 15.1 %). Beta diver-

sity among ecoregions exceeded 60 %, with the

greatest dissimilarity observed between ARCO

and MOR (βbc = 0.89), primarily determined

by balance. Similarly, between MAG and MOR

(βbc = 0.83), dissimilarity was modulated by

balance, and between ARCO and MAG (βbc

= 0.65), it was determined by the gradient

(Fig. 3A). Assemblage structure differed signifi-

cantly between ecoregions (FPermanova = 3.706; P

= 0.001), with significant differences observed

between ARCO and MAG (FPermanova = 3.923;

P < 0.01), ARCO and MOR (FPermanova = 4.305;

P < 0.001), and MAG and MOR (FPermanova =

2.761; P < 0.05). The NMDS confirmed the

PERMANOVA results, clearly separating the

structure of the assemblages between the ecore-

gions (Fig. 3B).

Six indicator species were identified (IndVal

≥ 50 %, P < 0.05). L. denticulata, L. baudiniana, T.

niveus, and H. trichoniscoides are indicator spe-

cies for ARCO ecoregion; L. tropicalis for MAG;

and T. marcuzzii for MOR (Fig. 4).

The highest average soil temperatures were

found in MAG (29.7 ± 0.3), while the lowest

were in ARCO (28.3 ± 0.1). Concerning soil

moisture, the highest values were observed in

MOR (75.4 ± 2), and the lowest in MAG (64.2

± 1.9). These two variables differ significantly

between ecoregions (temperature: H = 17.725;

P < 0.001; moisture: H = 17.573; P < 0.001).

Soil temperature differences were observed

among all ecoregions, whereas soil moisture

showed significant differences between ARCO

and MAG, without differences between ARCO

and MOR (Fig. 5).

Canonical Correspondence Analysis

revealed a positive relationship between the two

Fig. 2. A. Coverage-based rarefaction and extrapolation sampling curves of the assemblage of terrestrial isopods for

ecoregion. B. Species interpolation/extrapolation rarefaction curves based on number of individuals and richness (q0) for

ecoregion. C. Diversity profiles for each ecoregion, with CI 95% for each q order. D. Rank abundance (Whittaker curves) of

the assemblage of terrestrial isopods for ecoregion. ARCO, Coralline Archipelagos Ecoregion; MAG, Magdalena Ecoregion;

MOR, Gulf of Morrosquillo Ecoregion.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58577, enero-diciembre 2024 (Publicado Ago. 22, 2024)

Fig. 3. A. Beta diversity partitioning values calculated with the Bray-Curtis index between the ecoregions studied in the

Colombian Caribbean. βbc.bal: balanced variation component of Bray-Curtis dissimilarity; βbc.gra: abundance gradient

component of Bray-Curtis dissimilarity. B. Non-metric Multidimensional Scaling (NMDS) ordination analysis based on

Bray-Curtis index of similarities of the terrestrial isopods assemblage between ecoregions. ARCO, Coralline Archipelagos

Ecoregion; MAG, Magdalena Ecoregion; MOR, Gulf of Morrosquillo Ecoregion.

Fig. 4. Indicator species analysis (IndVal%) of the terrestrial isopod assemblage in the three ecoregions. Gray boxes denote

species with significances (P < 0.05) of IndVal. ARCO, Coralline Archipelagos Ecoregion; MAG, Magdalena Ecoregion;

MOR, Gulf of Morrosquillo Ecoregion. Species: L.b, Ligia baudiniana; T.m, Tylos marcuzzii; T.ne, T. negroi; T.n, T. niveus;

A.c, Armadilloniscus caraibicus; A.n, A. ninae; A.l, A. luisi; H.t, Halophiloscia trichoniscoides; L.d, Littorophiloscia denticulata;

L.t, Littorophiloscia tropicalis; T.b, Trichorhina bermudezae; T.h, T. heterophthalma; C.t, Ctenorillo tuberosus; B.n, Buchnerillo

neotropicalis; B.sp., Buchnerillo sp.; S.n, Stenoniscus nestori; P.p, Porcellionides pruinosus.

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e58577, enero-diciembre 2024 (Publicado Ago. 22, 2024)

variables and the first axis, explaining 100 % of

the variation (P < 0.05). This axis was positively

associated with the abundance of T. marcuzzii,

displaying a marked distribution towards the

MOR transects, indicating that this species is

linked to high values of soil temperature and

moisture. The other species included in the

analysis exhibited negative relationships with

the two variables (L. baudiniana, T. negroi,

T. niveus, A. caraibicus, H. trichoniscoides, L.

denticulata, L. tropicalis, T. bermudezae, and C.

tuberosus) (Fig. 6).

Fig. 5. Box-plot of soil temperature (A) and soil moisture (B) in the study area. Different letters indicate statistically

significant differences (P < 0.05). ARCO, Coralline Archipelagos Ecoregion; MAG, Magdalena Ecoregion; MOR, Gulf of

Morrosquillo Ecoregion.

Fig. 6. Ordination diagram of Canonical Correspondence Analysis (CCA) showing distribution of abundance data for taxa,

transects and environmental variables (red arrows). S_M, soil moisture; S_T, soil temperature. Squares, transects of Gulf of

Morrosquillo Ecoregion; triangles, transects of Magdalena Ecoregion; circles, transects of Coralline Archipelagos Ecoregion.

Species: L.b, Ligia baudiniana; T.m, Tylos marcuzzii; T.ne, Tylos negroi; T.n, Tylos niveus; A.c, Armadilloniscus caraibicus; H.t,

Halophiloscia trichoniscoides; L.d, Littorophiloscia denticulata; L.t, Littorophiloscia tropicalis; T.b, Trichorhina bermudezae; C.t,

Ctenorillo tuberosus.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58577, enero-diciembre 2024 (Publicado Ago. 22, 2024)

DISCUSSION

In our study, we identified 17 species of

terrestrial isopods in the supralittoral zone

across the three evaluated ecoregions. Cur-

rently, Colombia boasts the highest number of

species recorded from the coastal environment

in the Neotropical region (Carpio-Díaz et al.,

2016; López-Orozco et al., 2022). Furthermore,

additional surveys in coastal areas outside the

supralittoral zone in the ARCO, MOR, and

MAG ecoregions have unveiled the presence

of species not previously documented from

Colombia, including Rhyscotus sphaerocepha-

lus Budde-Lund, 1893, Littorophiloscia culebrae

Moore, 1901, and Alloniscus buckupi Campos-

Filho & Cardoso, 2018.

The taxonomic composition and abun-

dance observed in the assessed ecoregions

closely resemble findings in other tropical

countries (Mexico, Cuba, Belize, Costa Rica,

Venezuela, and Brazil), featuring common spe-

cies of the genera Ligia Fabricius, 1798, Tylos,

Armadilloniscus, Littorophiloscia Hatch, 1947,

and Stenoniscus Aubert & Dollfus, 1890 being

common (Boone, 1934; López-Orozco et al.,

2022; Paoletti & Stinner, 1989; Schultz, 1972;

Schultz, 1984; Schultz & Johnson, 1984; Taiti &

Ferrara, 1986; Taiti et al., 2018). Schultz (1972),

Schultz (1984), Schultz & Johnson (1984), and

Taiti et al. (2018) documented up to 13 species

in the supralittoral zone of Caribbean coun-

tries. In contrast, López-Orozco et al. (2022)

reported 17 terrestrial isopod species on Isla

Grande (Colombian Caribbean), with 16 in the

coastal environment.

The results for richness and abundance

analysis in the supralittoral zone of the three

evaluated ecoregions were highest in ARCO.

This pattern is likely attributed to the avail-

ability and quality of microhabitats in this

ecoregion. Conversely, the lower availability of

microhabitats, coupled with the influence of

discharges from the Magdalena and Sinú rivers

in the MAG and MOR ecoregions, could be

influencing the establishment of certain spe-

cies with more stringent physiological require-

ments. López-Victoria et al. (2004) mentioned

that the specific composition in the rocky coast-

lines of the Colombian Caribbean is primarily

determined by substrate type, waves, and slope.

While the latter two variables were similar

across all stations, differences in microhabitat

availability (substrates) were noted. Therefore,

the species richness of terrestrial isopods in the

supralittoral zone of the Colombian Caribbean

is related to the availability of microhabitats.

The structure and composition of the ter-

restrial isopod assemblage vary among the

evaluated ecoregions, with high beta diversity

values. Faunistic assemblages respond to abiotic

environmental variables (Messina et al., 2016;

Navas et al., 2010), and their distribution is

determined by the environmental conditions

and the organisms’ capacity to adapt. The dis-

tribution patterns of terrestrial isopods in the

supralittoral zone of the Colombian Caribbean

align with the zoning of marine ecoregions,

each presenting unique characteristics such as

geomorphology, the influence of continental

discharges, and ecosystems, among others. In

general, there is a scarcity of published works on

the structure and composition of species in the

supralittoral zone of the Colombian Caribbean.

Ligia baudiniana, T. niveus, H. trichonis-

coides, and L. denticulata were recognized as

indicator species for the ARCO ecoregion, with

T. marcuzzii in the MOR ecoregion, and L. trop-

icalis in MAG. Ligia baudiniana, known for its

‘runner’ habit, is distributed along all coasts of

America and has been found in river transport

boats, potentially contributing to its expanded

distribution (Com. Per. C.M. López-Orozco).

Tylos niveus, a species with limited mobility,

benefits from local community transportation

of coastal materials favoring its local distribu-

tion in ARCO. Halophiloscia trichoniscoides is

an endemic species in the Caribbean region

(López-Orozco et al., 2022; Vandel, 1973), and

was found in all ARCO stations. Littorophi-

loscia denticulata and L. tropicalis are circum-

tropical species (Leistikow, 2000; López-Orozco

et al., 2022; Taiti & Ferrara, 1986). Accord-

ing to our results, L. tropicalis is distributed

along the marine coasts of the ARCO, MOR

and MAG ecoregions.

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e58577, enero-diciembre 2024 (Publicado Ago. 22, 2024)

High values of soil temperature and mois-

ture correlated with low abundance of the

terrestrial isopod assemblage. In contrast, T.

marcuzzii exhibited high abundance and fre-

quency, with increasing values of these two vari-

ables. Generally, terrestrial isopod populations

are associated with increasing values of these

two variables (Solomou et al., 2019; Zimmer,

2005). Rushton & Hassall (1987) highlighted

that temperature and humidity influence the

growth, survival, and reproduction of these

organisms leading to population peaks under

optimal conditions (Fingini, 2008). However,

Preciado & Martínez (2014) found no relation-

ship between factors such as soil temperature,

ambient temperature, and relative humidity

with the abundance of the evaluated species,

suggesting that soil characteristics may be more

influential in determining the abundance of

terrestrial isopod species in a given habitat.

Considering this, evaluating the response of

terrestrial isopod populations in the supralit-

toral zone of the Colombian Caribbean to these

variables, along with other potential determi-

nants, is essential. In addition, it is necessary to

include other variables in order to determine

their influence, which, in some cases, might

be decisive (Gabsi et al., 2024; Hamaïed-Melki

et al., 2010; Khemaissia et al., 2012a; Khe-

maissia et al., 2012b; Khemaissia et al. 2016;

Zimmer, 2005).

Terrestrial isopods have been employed

in the evaluation and monitoring of environ-

mental impacts stemming from heavy met-

als, urbanization, and agricultural processes,

among other factors (Longo et al., 2013; Paoletti

& Hassall, 1999; Solomou et al., 2019; Szlavecz

et al., 2018). The observed differences in assem-

blage structure among the evaluated ecore-

gions underscore the potential utility of these

organisms in devising strategies for the con-

servation, management, and sustainable uti-

lization of resources within the supralittoral

zone of the Neotropical region. Furthermore,

the taxonomic composition discovered exhib-

its unique characteristics that distinguish the

evaluated areas, featuring indicator species with

specific requirements.

Our results provide evidence for the high

species richness of Oniscidea in the supralitto-

ral zone of the Colombian Caribbean. However,

given the diverse orographic and physiographic

conditions of the coastal zone and the lack of

exploration in other ecoregions (Darién, Tay-

rona, Palomino, and Guajira), knowledge on

the taxonomic composition of the terrestrial

isopods in the coastal area remains incomplete.

Collaborative efforts are needed to understand

the biology of species with specific adaptations

and low abundance. Moreover, considering the

threats to the supralittoral zone, such as ero-

sion, environmental and climate change, and

human intervention, species in this area are at

risk of disappearing. This scenario is alarming

for the group, because their ecosystem roles

are not yet known, which may have long-term

repercussions on conservation strategies.

Finally, similar challenges are observed in

other countries, where knowledge of coastal

terrestrial isopod species is nearly nonexistent.

Therefore, investing in personnel training and

interdisciplinary projects is crucial for a better

understanding of the diversity, ecology, and

biology of Oniscidea in the coastal areas of the

Caribbean region.

Ethical statement: the authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict 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 acknowledgments sec-

tion. A signed document has been filed in the

journal archives.

See supplementary material a43v72n1-MS1

ACKNOWLEDGMENTS

The present work was financially sup-

ported by Vicerrectoría de Investigaciones and

Grupo de Investigación en Biología Descriptiva

y Aplicada (Acta de Compromiso N° 053-2022);

to project entitled “Biodiversity of terrestrial

isopods (Crustacea, Isopoda, Oniscidea) from

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e58577, enero-diciembre 2024 (Publicado Ago. 22, 2024)

Cyprus in the light of integrative taxonomy”, for

the postdoctoral fellowship granted to ISC-F,

“ONISILOS Research Program-2018”, funded

by the University of Cyprus. To INVEMAR for

providing the cartography of the marine ecore-

gions from the Colombian Caribbean. To Car-

los Sierra for his help in collecting material. We

appreciate the contributions and suggestions

of the anonymous reviewers, which helped

improve the manuscript.

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