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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e00000, enero-diciembre 2024 (Publicado Nov. 22, 2024)
Morphometric variations in the reef crab Plagusia depressa
(Decapoda: Plagusiidae) in the Western tropical Atlantic
Anne K. R. Costa 1*; https://orcid.org/0000-0002-1681-6851
Simone M. A. Lira 1; https://orcid.org/0000-0003-0692-6237
Lucas N. Silva 2; https://orcid.org/0000-0002-0327-0829
Ralf Schwamborn 1; https://orcid.org/0000-0001-9150-8720
1. Oceanography Department, Federal University of Pernambuco, Av. Arquitetura, Cidade Universitária, Recife, PE,
Brazil; annekcosta23@gmail.com (*Correspondence), simonealira@gmail.com, ralf.schwamborn@ufpe.br
2. Fishery Biology Laboratory, Fisheries and Aquaculture Department, Federal Rural University of Pernambuco, Rua
Dom Manoel de Medeiros, Dois Irmãos, Recife, PE, Brazil; lucasns.93@live.com
Received 05-X-2023. Corrected 09-VIII-2024. Accepted 11-XI-2024.
ABSTRACT
Introduction: The reef crab Plagusia depressa is widely distributed in tropical oceans. In the Atlantic Ocean, this
species is distributed in geographically distant regions with different environmental pressures, which may lead
to morphological divergence.
Objectives: To explore morphometric differences in Plagusia depressa populations between coastal reefs and an
oceanic island in the Western tropical Atlantic. Also, to examine the potential link between the species’ pheno-
typic plasticity and environmental and geographic factors.
Methods: A total of 194 crabs were sampled from four Brazilian coastal and oceanic sites (Suape: n= 52,
Tamandaré: n= 53, Barra Grande: n= 44, and Fernando de Noronha Archipelago: n= 45) from 2020 to 2022,
under distinct anthropogenic and environmental influences. Linear and geometric morphometric analysis
employed seven linear measurements and specific landmarks on the carapace, abdomen, and right chelae to
pinpoint significant morphometric differences among these areas.
Results: The westernmost coastal population exhibited striking differences from the other regions. Male crabs in
this population had a pronounced carapace rostrum, while females showed a narrower abdomen, longer telson,
and chelae thinning and elongation. It is possible that the pronounced isolation in this area, along with patterns of
changes in ocean currents, may influence our results. Female crab carapaces from the island area showed lateral
enlargement and pronounced rostrum depressions. Furthermore, being farther from the mainland, this site has
oceanic island environmental features, affecting the population through desiccation and air exposure. For male
crabs, different right chelae shape across areas showed an impact of food capture and interaction with other
organisms on their phenotypic plasticity.
Conclusion: Environmental factors such as tidal exposure and habitat composition might affect the phenotypic
plasticity of tidal crabs. Moreover, a biogeographical barrier in Northeastern Brazil, which was hitherto given
little consideration, holds important implications for the biogeography of the Western tropical Atlantic.
Key words: biogeography; environmental pressures; geometric morphometry; marine ecology; phenotypic
plasticity.
https://doi.org/10.15517/rev.biol.trop..v72i1.56414
INVERTEBRATE BIOLOGY
2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e00000, enero-diciembre 2024 (Publicado Nov. 22, 2024)
INTRODUCTION
Conspecific individuals can differ in sev-
eral specific nuances, ranging from evident dif-
ferences in traits, such as sex, color, and size, to
less conspicuous properties, such as behavior,
genetics, and subtle differences in body shape.
Individual variations in morphology are a
major focus of evolutionary biology since natu-
ral selection acts on them (Afkhami et al., 2016;
Cadrin et al., 2014). Identifying and describ-
ing population variations and biogeographical
barriers is essential to answer fundamental
questions in evolutionary biology, as well as
providing subsidies for the evaluation and man-
agement of fisheries through stock identifica-
tion, habitat utilization, migration patterns and
response to environmental changes (Cadrin et
al., 2014; Hopkins & Thurman, 2010).
Brachyura crab studies have identified
morphological divergences between popula-
tions, which may be influenced over time by
environmental factors (phenotypic plasticity)
due to distinct selective stresses when popula-
tions are geographically isolated (Teschima et
al., 2016; Silva et al., 2010). In the oceans, larval
dispersal promotes marine life and connectiv-
ity within and between populations, leading to
the exchange of individuals among distant or
geographically isolated populations. This con-
nectivity carries significant implications for the
evolution and ecology of the species (Becker et
al., 2007).
Ocean currents significantly influence
marine environments, particularly impacting
the movements and dispersal of plankton-
ic larval species (Chapman et al., 2011). In
the Tropical Western Atlantic (TWA), various
RESUMEN
Variaciones morfométricas en el cangrejo de arrecife Plagusia depressa (Decapoda: Plagusiidae)
en el Atlántico tropical occidental
Introducción: El cangrejo de arrecife Plagusia depressa se distribuye ampliamente en los océanos tropicales. En
el océano Atlántico, esta especie se distribuye en regiones geográficamente distantes con diferentes presiones
ambientales, lo que puede llevar a una divergencia morfológica.
Objetivos: Explorar las diferencias morfométricas en las poblaciones de Plagusia depressa entre arrecifes costeros
y una isla oceánica en el Atlántico tropical occidental. Además, examinar el posible vínculo entre la plasticidad
fenotípica de la especie y los factores ambientales y geográficos.
Métodos: Se muestrearon un total de 194 cangrejos en cuatro sitios costeros y oceánicos brasileños (Suape: n=
52, Tamandaré: n= 53, Barra Grande: n= 44 y Archipiélago Fernando de Noronha: n= 45) desde 2020 hasta 2022,
bajo influencias antropogénicas y ambientales distintas. El análisis morfométrico lineal y geométrico empleó
siete medidas lineales y puntos de referencia específicos en el caparazón, abdomen y quelas derechas para señalar
diferencias morfométricas significativas entre estas áreas.
Resultados: La población costera más occidental mostró diferencias sorprendentes con las otras regiones. Los
cangrejos machos en esta población presentaban un rostro de caparazón pronunciado, mientras que las hembras
mostraban un abdomen más estrecho, telson más largo y adelgazamiento y alargamiento de las quelas. Es posible
que el aislamiento pronunciado en esta área, junto con patrones de cambios en las corrientes oceánicas, puedan
influir en nuestros resultados. Los caparazones de las cangrejas hembra de la zona de la isla mostraron un ensan-
chamiento lateral y depresiones de rostro pronunciadas. Además, al estar más lejos del continente, este sitio tiene
características ambientales de isla oceánica, lo que afecta a la población a través de la desecación y la exposición
al aire. Para los cangrejos machos, diferentes formas de quelas derechas en diferentes áreas indican un impacto de
la captura de alimentos y la interacción con otros organismos en su plasticidad fenotípica.
Conclusión: Factores ambientales como la exposición a las mareas y la composición del hábitat podrían desem-
peñar un papel en la plasticidad fenotípica de los cangrejos de marea. Además, una barrera biogeográfica en el
noreste de Brasil, que hasta ahora se había tenido en poca consideración, tiene importantes implicaciones para la
biogeografía del Atlántico tropical occidental.
Palabras clave: biogeografía; presiones ambientales; morfometría geométrica; ecología marina; plasticidad
fenotípica.
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current systems, including the central branch
of the South Equatorial Current (cSEC), the
Brazil Current (BC), and the North Brazil
Undercurrent (NBUC), play vital functions
(Fig. 1) (Dossa et al., 2021). TWA and the
Brazilian coast areas feature two well-defined
biogeographic barriers: the low-salinity Ama-
zon River plume and the cold-water upwelling
of Cabo Frio (Floeter et al., 2008; Rocha, 2003;
Tosetto et al., 2022). Another potential barrier
that is less evident and unexplored, is the cape
of Ponta do Calcanhar (Fig. 1). Many studies
have shown that this geographical point tends
to substantially restrict gene exchange between
populations to the North and South of this
cape, acting as a biogeographical barrier for
species with planktonic larval stages, probably
due to the lack of any advective transport in a
southerly direction at this cape (e.g. Hampton
et al., 2014; Melo et al., 2020; Shanks, 2009;
Weersing & Toonen, 2009). Studies on the con-
nectivity of brachyuran crabs have reported
patterns of intraspecific morphological varia-
tion between populations to the North and
South of Ponta do Calcanhar, as observed in
populations of the genus Uca (Hampton et
al., 2014; Wieman et al., 2014) and in semi-
terrestrial crab Armases angustipes (Rathbun,
1897) (Marochi et al., 2017), indicating that
such geographical features and environmental
Fig. 1. The study areas in the Western Tropical Atlantic, where Plagusia depressa specimens were captured. Barra Grande
Marine Protected Area, Suape Bay, Port and Industrial Area, Tamandaré Beach Marine Protected Area and Fernando
de Noronha Archipelago Marine Protected Area. Yellow Triangle: Ponta do Calcanhar Cape, a potentially relevant
biogeographic barrier (for details, see text). Ocean currents shown in the map, according to (Dossa et al., 2021): North Brazil
Undercurrent (NBUC), North Brazil Current (NBC), the central branch of the South Equatorial Current (cSEC), South
Equatorial Undercurrent (SEUC).
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pressures may influence phenotypic plasticity
within populations.
A key characteristic of the Tropical West-
ern Atlantic (TWA) off Northeastern Brazil is
the presence of oceanic islands, as Fernando
de Noronha Archipelago. This insular envi-
ronment is separated by kilometers of dis-
tance, and may support species with limited
recruits, necessitating their management as dis-
tinct ecological populations (Palumbi, 2003;
Teschima et al., 2016). The average dispersal
range for fish and invertebrate larvae is 25 to
150 km (Palumbi, 2003), while Brazilian oce-
anic islands are over 300 km from the coast,
leading to reduced gene flow among popula-
tions, implying in the demographic rates and
population dynamics of the species and that
can affect their survival, reproduction, and
overall population health. This isolation has
been shown to result in intraspecific variations
in certain marine invertebrates, including the
sally lightfoot crabs Grapsus grapsus (Linnaeus,
1758) and Grapsus adscensionis (Osbeck, 1765)
(Freire et al., 2021; Teschima et al., 2016) and
the chaetognath Flaccisagitta enflata (Grassi,
1881) (Melo et al., 2020).
The reef crab Plagusia depressa (Fabri-
cius, 1775) (Brachyura: Plagusiidae) is widely
distributed in the tropical oceans and in the
Western Atlantic, P. d e p re s s a occurs on Brazil’s
Northeast coast and oceanic islands Fernando
de Noronha, São Pedro and São Paulo Archi-
pelago, Rocas Atoll, and Trindade and Martin
Vaz Archipelago (Coelho et al., 2008; Melo,
1996; Oliveira-Almeida & Lopes-Carvalho,
2014). This species can be found in crevices of
shallow subtidal rocks and the intertidal zones
of coral reefs (Coelho et al., 2008), in general,
on the reef line furthest from the shore. This
species is commercially exploited and con-
sumed by local populations, particularly in
some Brazilian coastal areas (Freitas & Santos,
2007). Despite its wide distribution, studies on
P. d e p ress a in the Western Atlantic is limited,
focusing mainly on body growth and mortal-
ity (Coelho et al., 2004), population structure
(de Oliveira-Rocha et al., 2019; Freitas & San-
tos, 2007; Oliveira-Rocha & Paiva-Guimarães,
2016), gonadal development (Paiva-Guimarães
et al., 2021), and feeding habits (de Lemos et
al., 2019). Challenges in studying this species
arise from its cryptic nocturnal behavior and
difficulty in capturing within reef crevices, con-
tributing to the lack of greater contributions to
assessments of its ecology and formal quantita-
tive stocking efforts.
Understanding the biological and ecologi-
cal characteristics of this species across its dis-
tribution range -such as population dynamics,
interpopulation connectivity, and the impacts
and pressures on its habitat- is crucial for a
deeper comprehension of these populations and
for the formulation of effective strategies for the
conservation and management of this species.
Thus, the objective of this study was to investi-
gate the potential existence of variation patterns
in the shape and size of P. d e p re s s a populations
at three coastal sites and one oceanic island in
the WTA, each with varying conservation sta-
tuses and environmental characteristics, using
two different morphometric techniques (linear
and geometric). We tested the hypothesis that
P. d e p ress a demonstrates phenotypic plasticity
across populations based on environmental and
geographical factors.
MATERIAL AND METHODS
Sexually mature specimens of P. d e p ress a
(i.e. specimens with carapace widths larger
than 24 mm for males and 27 mm for females,
according to de Oliveira-Rocha et al. (2019)
were collected in three coastal zones and one
oceanic insular ecosystem with different levels
of protection: Barra Grande Marine Protect-
ed Area (BG); Tamandaré beach (TM) with-
in Costa dos Corais Marine Protected Area
(MPA); Suape Beach (SB) with open, unre-
stricted access for tourism and fisheries, and
in the oceanic Fernando de Noronha Archi-
pelago (FN) marine protected area (Table 1,
Fig. 1). Among these areas, the SB port and
industrial area has the lowest level of protec-
tion, and reef crab meat is regularly offered and
sold there (known as “aratú-da pedra”). At BG
and TM marine protected areas, the capture
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of reef crabs is permitted for subsistence, but
there is no regular commercial activity based
on this species. On the oceanic FN island, the
capture of this species is strictly forbidden and
effectively enforced.
Structure measurements and anatomi-
cal landmarks: All individuals were identified,
sexed, weighed, and measured. Body measures
were obtained using precision calipers (near-
est 0.01 mm). The measures were: A: carapace
Table 1
Sampling areas for the reef crabs Plagusia depressa, with area characterization and sampling period.
Sampling area Coordinates Area characterization Sampling period
Fernando de Noronha
Archipelago (FN) 3º15’ S & 36º10’ W
MPA, insular area, crustacean harvest and fishing
activities prohibited by federal laws, and strong tour-
ism activity (Teixeira, 2003)
2020, Nov
Barra Grande (BG) 4°40’04’’ S & 37°24’54’’ W MPA, urban, sustainable crustacean fishing activity
(de Andrade-Meireles et al., 2017) 2022, Jan
Suape Bay (SB) 8º22’ S & 34º56’W
Industrial and port complex, intensive fishing activi-
ties, industrial effluents and domestic sewage (Lima-
Barcellos et al., 2018)
2021, Nov
Tamandaré Beach
(TM) 8º45’ S & 35º08’ W MPA, urban, sustainable fishing and tourism activi-
ties, agriculture activities (Maida & Ferreira, 2003) 2020, Dec
MPA: Marine Protected Area.
Fig. 2. Carapaces of Plagusia depressa specimens from sampled areas photo-documented in TPSDig software (v. 2.31)
with their respective landmarks for geometric morphometric analysis. TM: Tamandare Beach; FN: Fernando de Noronha
Archipelago; SB: Suape Bay; BG: Barra Grande.
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length (CL), B: carapace width (CW), C: abdo-
men length (AL); D: abdominal width (AW); E:
right chelae length (RCL) F: right chelae width
(RCW) (Fig. 2, Fig. 3, Fig. 4, Fig. 5).
Morphological variation in body shapes
was assessed using geometric morphometric
methods (Teschima et al., 2016; Thurman et al.,
2021; Zelditch et al., 2012). Images were taken
with the aid of a tripod attached to a camera
(Canon EOS Model T3i) that was maintained
parallel to the plane, for standardization. To
each crab from the sampled locations, three
pictures were photo-documented: dorsal, ven-
tral, and right chelae (Fig. 2, Fig. 3, Fig. 4)
Landmarks were distributed to better obtain
the shape of the animal using the TPSDig
software (version 2.31, Rohlf, 2010) based on
previous studies using other brachyuran crabs
(e.g. Marochi et al., 2017; Teschima et al., 2016;
Thurman et al., 2021; Silva et al., 2010). For
the carapace, 15 anatomical landmarks were
distributed: being 11 landmarks for female
abdomens, 10 landmarks for male abdomens,
and six landmarks for right chelae (Fig. 5).
Morphometric Analysis: The degree of
morphologic divergence among the studied
populations of P. d e pre ss a was assessed using two
complementary methods: linear and geomet-
ric morphometric analyses (LMA and GMA,
respectively). First, we analyzed the influence
of linear measurements on the morphometric
variation of the different sampling areas. For
this purpose, a Principal Component Analysis
(PCA) was conducted to describe, graphically,
which body structures most influenced the
separation between the sampling areas. Next,
to identify possible morphological divergences
through the shape of the body structures in
the studied populations, a geometric mor-
phometric analysis (GMA) was adopted. For
this, a Generalized Procrustes Analysis (GPA)
was conducted with raw landmark coordinates
within superimposed configurations, based on
the centroid (i.e. mass center of the configura-
tion). GPA overlapping removed the effect of
position, orientation, and size of landmark con-
figuration, in such a way that the aligned con-
figurations corresponded exclusively to shape
changes (Adams et al., 2004).
Fig. 3. Chelae of Plagusia depressa specimens from sampled areas photo-documented in TPSDig software (v. 2.31) with their
respective landmarks for geometric morphometric analysis. TM: Tamandare Beach; FN: Fernando de Noronha Archipelago;
SB: Suape Bay; BG: Barra Grande.
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Fig. 4. Abdomen of Plagusia depressa male and female specimens from sampled areas photo-documented in TPSDig software
(v. 2.31) with their respective landmarks for geometric morphometric analysis. TM: Tamandare Beach; FN: Fernando de
Noronha Archipelago; SB: Suape Bay; BG: Barra Grande.
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Similarly to LMA, a Principal Compo-
nent Analysis (PCA) was conducted to identify
the main characteristics of the shapes. Then,
Canonical Variance Analysis (CVA) was per-
formed, with 10 000 permutations, to find the
shape characteristics that best distinguish and
separate the sampling areas, using Procrustes’
Distance (Proc. Dist.). Differences between
the forms were tested by applying the Hotel-
ling test (T²) with Bonferroni correction in
Discriminant Analysis (DA). Thin-plate spline
functions (Klingenberg, 2011) were generated
between the groups that presented significant
differences in DA using the MorphoJ 2.0 soft-
ware. In all instances, the level of statistical
significance was set at p ≤ 0.05 for rejecting the
null hypothesis.
A multivariate regression analysis was car-
ried out to determine the influence of size on
shape (allometry) in the dataset using centroid
size (size variable) as an independent variable
and shape (Procrustes coordinates) as a depen-
dent variable (Klingenberg, 2016) with p-values
estimated by permutation tests (10 000 inter-
actions). This test simulates the null hypoth-
esis of complete independence between size
Fig. 5. Structure measurements and anatomic landmarks for Plagusia depressa specimens used for linear and geometric
morphometric analysis. A. Carapace: 1 and 2: posterior margins; 3 and 13: concavity limits of the fifth pereiopods; 4 and 12:
convex points of the posterior lateral region; 5 and 11: spines of maximum carapace width; 6 and 10: anterolateral spine tips;
7, 8 and 9: rostrum dent depressions; 14 and 15: distal points of the cardiac line structure; dotted lines: I: carapace length; II:
carapace width. B. Male abdomen: 1 and 9: abdomen anterior margin; 2 and 8: third abdominal somite posterolateral margins;
3 and 7: fourth abdominal somite lateral margins; 4 and 6: fifth abdominal somite anterolateral margins; 5: top of the telson;
10: midpoint of the third abdominal somite; dotted lines: III: abdomen length; IV: abdomen width. C. Female abdomen: 1
and 11: abdomen anterior margin; 2 and 10: third abdominal somite posterolateral margin; 3 and 9: fourth abdominal somite
lateral margin; 4 and 8: fifth abdominal somite anterolateral margin; 5 and 7: sixth abdominal somite anterolateral margin; 6:
telson tip. D. Right chelae: 1 and 7: lower and upper attachment point of carpus with manus; 2: maximum concave point of
the lower manus region; 3: polex tip; 4: lower point of dactylar joint with manus; 5: upper point of dactylar joint with manus;
6: maximum convex point of the upper manus region; dotted lines: V: chelae length; VI: chelae width.
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and shape by randomly reassigning the sizes
and shapes to each other, indicating percent
allometry (%) between shape and size in the
population studied.
RESULTS
A total of 194 P. d e pre s s a specimens (87
females and 107 males) were collected: 44 at
Barra Grande (BG), 52 in Suape Bay (SB), 53 at
Tamandaré Beach (TM), and 45 at Fernando de
Noronha Archipelago (FN). Adult crabs varied
considerably in carapace width for both females
and males (Table 2).
In the Principal Component Analysis
(PCA) conducted within the linear morpho-
metric analysis for males (PCA, Fig. 6), the
variable RCL contributed the most to differ-
ences between Tamandaré (TM) and Suape Bay
(SB) (Fig. 7). These PCA results explained 92 %
of the variation in the first two components.
PC1 explained 87.4 %, with a strong influence
of right chelae length (RCL).
In females, PCA, showed that there were
strong influences of the right chelae width
(RCW), abdomen width (AW), and carapace
height (CH) on the separation between areas
(Fig. 7). These structures indicated that these
variables were important in the separation of
females of the Fernando de Noronha Archi-
pelago (FN) population from the other areas.
The first two components explained 86.7 % of
the variability, being 74.2 % explained by PC1
and 12.5 % by PC2.
According to the results of the geometric
morphometric analysis (GMA), the vectors
Table 2
Populations of reef crab Plagusia depressa used for
morphometric analyses.
Sampling
Area Sex N CW Mean (St. Dev.)
CW
BG F 17 31-54 mm 36 mm (± 8.2)
M 27 24-57 mm 46 mm (± 10.9)
SB F 25 32-51.5 mm 39 mm (± 4.1)
M 27 32.5-44 mm 38 mm (± 3.0)
TM F 26 33.5-52 mm 42.5 mm (± 5.1)
M 27 33.5-52 mm 44 mm (± 5.5)
FN F 19 27-49.5 mm 34 mm (± 5.3)
M 26 26.5-54 mm 36 mm (± 7.0)
Sample size (N), Carapace width (CW), with their respective
mean and standard deviation (St. Dev). Sampling areas:
Barra Grande (BG), Suape Bay (SB), Tamandaré Beach
(TM), Fernando de Noronha Archipelago (FN).
Fig. 6. Principal Component Analysis (PCA) of male Plagusia depressa populations of the variables studied in the areas
studied. Carapace width (CW); carapace length (CL) carapace height (CH); abdomen width (AW); abdomen length (AL);
right chelae width (RCW); right chelae length (RCL).
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below can be interpreted and visualized as a
shape change per unit of size change. Females
and males of P. d e p ress a showed low allometric
percentages with values less than 12 % in all
multivariate regressions analyzed, indicating
that the effect of structure sizes has little influ-
ence on the morphological variation in reef crab
population in studied areas. The carapace and
abdomen of females showed 6.41 % and 11.16
% of allometric percentage, respectively, with
highly significant permutation values (Multi-
variate regression; p < 0.0001). For chelae, the
allometric value was about 1 % and there was
no significant difference between shape and
centroid size in females (p = 0.57, Fig. 8).
Conversely, male crabs exhibited values of
11.1 % of allometric percentage in carapace and
chelae multivariate regression and 3.5 % for
male abdomen, with significant permutation
values in all sampled reef environments (Multi-
variate regression, p < 0.0001).
Carapace shapes: P. d e p r e s s a populations
exhibited significant differences in carapace
shapes between populations. Procrustes dis-
tance values of males were different between
Tamandaré (TM) and Barra Grande (BG)
populations (CVA; p < 0.05, Table 3). The CVA
results explained 86 % of the morphological
variations between the studied areas (Fig. 9A).
Males from TM presented a more concave
fourth pereiopod region (3 and 13 points) than
the male population from BG and a narrowing
of the cardiac lines (14 and 15 points). On the
other hand, the BG population presented the
region corresponding to the rostrum more pro-
nounced than TM. According to the discrimi-
nant analysis (DA) through cross-validation
between the groups analyzed, the percentage of
correct allocation of the BG-TM male popula-
tions was 85 and 73 %, respectively (p < 0.0001)
(Fig. 6B).
In the same way as the linear results, the
shape data of the female crabs of P. de pre s s a
for the FN population were different from
the other areas (CVA, p < 0.05, Table 3) with
CVA results explaining 88 % of the first two
variables (Fig. 6C). The FN female population
showed enlargement in the posterior lateral
region (4 and 12 points) and more pronounced
rostrum depressions (7 and 9 points) in relation
to the coastal areas studied. According to the
discriminant analysis through cross-validation
between the analyzed groups, it was possible to
Fig. 7. Principal Component Analysis (PCA) of female Plagusia depressa populations of the variables studied in the areas
studied. Carapace width (CW); carapace length (CL) carapace height (CH); abdomen width (AW); abdomen length (AL);
right chelae width (RCW); right chelae length (RCL).
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observe that the percentage of correct alloca-
tion of females in the Fernando de Noronha
Archipelago was higher than 61 % in relation
to the other areas (Fig. 9D).
Abdomen shapes: Abdomen shapes also
showed distinct variations in patterns in both
male and female P. d e p re s s a populations from
the WTA. Male crab populations showed sig-
nificant differences between all areas (p < 0.05,
Table 3) except between FN and TM (p = 0.123,
Table 3). In general, males from SB showed a
narrowing of the posterior lateral region at the
margin of the third abdominal somite (2 and
Fig. 8. Multivariate regression of influence of size on shape (allometry) in Plagusia depressa populations. Centroid size
(independent variable) and regression score-Procrustes distance (dependent variable). Barra Grande-BG. Suape Bay-SB.
Tamandaré Beach-TM and Fernando de Noronha Archipelago-FN. % prediction: allometric percentage with corresponding
p-values corrected from permutation tests (10 000 permutation rounds).
Table 3
Procrustes distance and corresponding “p”-values referring to the pairwise structure shapes differences between the male and
female of Plagusia depressa populations.
BG x SB Procrustes Distance/ P-values
BG x TM BG x FN SB x TM SB x FN FN x TM
MALE Carapace 0.015/p = 0.326 0.023/p = 0.008 0.022/p = 0 .083 0.016/p = 0.053 0.017/p = 0.157 0.018/p = 0.194
Abdomen 0.026/p < 0.001 0.083/p < 0.001 0.020/p = 0.021 0.035/p < 0.001 0.031/p < 0.001 0.013/p = 0.123
Chelae 0.082/ p < 0.001 0.050/p < 0.001 0.046/p = 0.003 0.046/p < 0.001 0.055/p < 0.001 0.037/p = 0.034
FEMALE Carapace 0.015/p = 0.464 0.023/p = 0.061 0.003/p = 0.001 0.016/p = 0.464 0.026/p < 0.001 0.027/p < 0.001
Abdomen 0.033/p = 0.017 0.036/p < 0.001 0,031/p = 0.057 0.015/p = 0.145 0.015/p = 0.170 0.015/p = 0.128
Chelae 0.054/p = 0.014 0.042/p = 0.173 0.057/p = 0.012 0.033/p = 0.136 0.019/p = 0.730 0.038/p = 0.077
Barra Grande-BG. Suape Bay-SB. Tamandaré Beach-TM and Fernando de Noronha Archipelago-FN. The P-values were
corrected from permutation tests (10 000 permutation rounds) for Procrustes distances among groups.
12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e00000, enero-diciembre 2024 (Publicado Nov. 22, 2024)
8 points), elongation of the anterior margin (1
and 9 points), and an elevation of the midpoint
of the third somite (Fig. 10A, Fig. 10B).
Abdomen morphological variations in
females were observed between BG and SB
and, BG and TM populations (p < 0.05). These
variables explained 87 % of the observed areas
(CVA p < 0.05). In BG females, a narrowing of
the anterior and lateral margins of the abdomi-
nal somites occurred, and a prolongation of the
top of the telson (Fig. 10C, Fig. 10D). Between
groups, the percentages of correct allocation
were higher than 65 % in discriminant analysis
(DA) (p < 0.05).
Right chelae shape: Right chelae shapes of
male crab populations were different between
all areas, according to the procrustes distance
values (p < 0.05, Table 3). Variations in the SB
population were due to a shortening of lower
and upper attachment points of carpus with
manus (1and 7 points) and a thickening of the
convex point of the upper manus region (6
point), when compared to the other sampling
Fig. 9. Carapace morphologic variations based on canonical variable analysis (CVA). A.-C. Thin-plate Splines of
morphological variation based on discriminant analysis (D. A). B.-D. Of male and female Plagusia depressa respectively in
the areas studied. Barra Grande-BG. Suape Bay-SB. Tamandaré Beach-TM and Fernando de Noronha Archipelago-FN. 95 %
confidence ellipses.
13
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e00000, enero-diciembre 2024 (Publicado Nov. 22, 2024)
areas (CVA, p < 0.05). BG population presented
lower manus concavity (2 point) and the polex
tip was more pronounced (3 point) than in the
other sampling areas. Besides, the BG popula-
tion presented an elongation of the lower and
upper carpal attachment points with the manus
(points 1and 7) (Fig. 11A, Fig. 11B).
Overall, female populations showed simi-
lar patterns to males, regarding morphological
differentiation between BG and SB, and BG
and FN populations (p < 0.05, Table 3). In this
case, BG also showed an increase in the lower
concavity of the manus (point 2) and the tip of
the polex more pronounced (3 point) than the
other study areas (Fig. 11C, Fig. 11D).
DISCUSSION
The present study provides important and
new insights into the morphological variability
in the reef crab P. d e pre s s a , a cryptic species
that is not well studied. The sampling areas had
different levels of protection and environmen-
tal conditions, and distinct biogeographical
Fig. 10. Abdomen morphologic variations based on canonical variable analysis (CVA). A.-C. Thin-plate Splines of
morphological variation based on discriminant analysis (D. A). B.-D. of male and female Plagusia depressa respectively in
the areas studied. Barra Grande-BG. Suape Bay-SB. Tamandaré Beach-TM and Fernando de Noronha Archipelago-FN. 95%
confidence ellipses.
14 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e00000, enero-diciembre 2024 (Publicado Nov. 22, 2024)
barriers for adult and larval dispersal of this
species. Overall, male crabs were morphologi-
cally different, regarding several key morpho-
metric parameters, in the westernmost area, the
Barra Grande Marine Protected Area, from all
the other sampling areas. On the other hand, the
carapace shape of females was different among
the offshore oceanic Fernando de Noronha
Marine Protect Area and the coastal areas.
Factors, processes, and biogeographic
barriers affecting reef crab populations in
the Barra Grande Marine Protected Area:
Our results showed significant morphological
differentiation patterns for male crabs in the
Barra Grande Marine Protection Area (BG)
for almost all the anatomical structures used
in geometric morphometric analysis in relation
to most of the studied areas. The most distinct
morphological variations observed in crabs
from BG were chelae shape, which had a more
pronounced polex tip and an elongated manus
in this region than in the other areas. Some
studies related to brachyuran morphometry
have shown that chelae are amongst the most
conspicuous anatomical features of decapod
crustaceans and are directly related to feeding
behavior and manipulation of the food items
(Marochi et al., 2017; Miyajima et al., 2012;
Silva & Paula, 2008; Teschima et al., 2016).
The elongated and robust chelae of males and
females of P. d e p re s s a in BG may be associated
Fig. 11. Right chelae morphologic variations based on canonical variable analysis (CVA). A.-C. Thin-plate Splines of
morphological variation based on discriminant analysis (D. A). B.-D. Of male and female Plagusia depressa respectively in
the areas studied. Barra Grande-BG. Suape Bay-SB. Tamandaré Beach-TM and Fernando de Noronha Archipelago-FN. 95
% confidence ellipses.
15
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e00000, enero-diciembre 2024 (Publicado Nov. 22, 2024)
with the aid in capturing food, the ability to
reach and scrape the substrate, when it presents
many irregularities, as observed for this area,
since this species has preferentially herbivo-
rous feeding habits (de Lemos et al., 2019). In
addition, the BG sampling area is constituted
by environments of abrasion platform types
caused by the erosion of coastal cliffs that are
common along this coastal area (Silva et al.,
2010). Thus, BG presents protuberant areas
with elevated structures, which may contribute
to the need to settle and move around in the
environment.
For brachyurans, several authors hypoth-
esized that chelae size and shape are strongly
influenced by sexual selection (especially in
males), due to cohort behavior and disputes
with other males in the population (Callander
et al., 2013) as observed by Teschima et al.
(2016) for G. grapsus populations in Brazilian
oceanic islands. Another hypothesis regarding
chelae shape is related to prey type, food qual-
ity and availability (Smith & Palmer, 1994).
Both hypotheses may affect chelae shape in a
short period, reflecting a divergent morpho-
logical intraspecific variation when compared
to other anatomical structures (Grinang et al.,
2019; Marochi et al., 2017), which supports our
results that right chelae correspond to the high-
est phenotypic divergence among populations
found even in geometric and linear morpho-
metric analysis, in that it was observed through
PCA that the width (RCW) and length (RCL)
of the chelae influenced the separation of the
study areas.
Another important point is that Barra
Grande, the westernmost sampling area, is
located about 550-600 km from the other areas,
potentially preventing the exchange of indi-
viduals with adjacent populations since the
average larval dispersal distances for marine
fish and invertebrate species is about 125 km
(Palumbi, 2003). The observed differences may
therefore be directly due to the existence of
geographic barriers. One important geographic
barrier in the study area is Ponta do Calcanhar,
where oceanic currents impede the dispersal of
planktonic larvae from Northwest to Southeast,
across this border (Thurman et al., 2013). The
division of the major oceanic currents and the
geomorphology at the Ponta do Calcanhar, may
significantly control gene exchange between the
Northern and Southern populations of indi-
vidual reef crab species, as already reported for
other marine invertebrate species, such as for
estuarine crabs Neohelice granulate (Ituarte et
al., 2012), fiddle crabs of genus Uca (Hampton
et al., 2014; Rosenberg, 2001; Thurman et al.,
2013) and the chaetognath F. enflata (Melo et
al., 2020). Our study contributes to the ongoing
discussion regarding the relevance of Ponta do
Calcanhar as a key biogeographic barrier for
planktonic dispersal in this region (Melo et al.,
2020; Thurman et al., 2013). Further studies are
necessary to understand if patterns of differen-
tiation observed in our results have a genetic
basis, or if they are merely phenotypic, based
on real-time local forcings (i.e., if such differ-
ences are due to barriers in gene flux). Further-
more, in some cases, trophic morphology is
considered to be under strong genetic control
(Teschima et al., 2016; Thurman et al., 2021),
while in other instances trophic variation may
result from diet-induced phenotypic plasticity
(Marochi et al., 2017; Smith, 2004).
Factors affecting the morphological vari-
ation of P. depressa in the offshore Fernando
de Noronha Archipelago Marine Protected
Area: Our results also indicated a pattern of
variation in carapace shape and size for females
in the oceanic offshore Fernando de Noronha
Archipelago Marine Protected Area (FN), pre-
senting the widest carapace and more accentu-
ated depressions of the rostrum than in coastal
populations. Many authors argued that female
brachyurans having a wider carapace shape
stem from a reproductive advantage, as they use
this structure for energy reserves for the repro-
ductive period and these differences may also
reflect an adaptation for internal growth (e.g.,
gonad and muscle) (de Lira & Calado, 2013;
Ferrari et al., 2011; López-Greco et al., 2004).
The morphological variation between pop-
ulations may be related to phenotypic plasticity
driven by environmental differences between
16 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e00000, enero-diciembre 2024 (Publicado Nov. 22, 2024)
sites (Hampton et al., 2014; Sanford & Kelly,
2011). Physical (e.g., tidal regimes and wave
energy), chemical (e.g. salinity, temperature)
and ecological (intra- and interspecific interac-
tions, food availability) conditions of habitats
may be responsible for morphological diver-
gence of carapaces and phenotypic plasticity
or even by epigenetic regulation (Sotka, 2012).
Crabs are ectothermic organisms that
depend on environmental temperature to regu-
late their temperature and metabolic rates, and
when they occupy semi-terrestrial habits, they
suffer directly from water loss and desiccation
stress (Allen et al., 2012; de Lira et al., 2015).
In Fernando de Noronha, the specimens were
collected on a beach in a mesolittoral zone on
a rock formation that is exposed during entire
low tide periods (spring and neap low tides),
causing stressful conditions of desiccation to
resident populations. The coastal reef areas
of Tamandaré Bay, Suape Beach, and Barra
Grande present considerably different habi-
tat conditions than those reported from FN.
These continental reefs are farther from the
beachline, and it emerge only during low spring
tides, reducing the time of exposure to high
temperatures and desiccation of individuals in
these areas, may explain the fact that the female
carapaces do not show significant divergence
between coastal areas.
Hampton et al. (2014), showed that intra-
specific morphological variation found in eight
species of fiddler crabs might be related to
variation in humidity with water conservation
in the gill chambers of female fiddler crabs
Minuca burgersi (Holthuis, 1967). The authors
infer that differences in humidity may influence
gene expression and morphological variation.
A similar pattern (with local pressures and fac-
tors affecting morphology) was also observed
by Marochi et al. (2017), for populations of
the mangrove crab A. angustipes (Dana, 1852)
along the Brazilian coast. They based their
study on differentiation in carapace and chelae
morphological structures and genetic differen-
tiation using DNA sequencing. Similarly to our
study, they also found statistically significant
morphological differentiation and geographic
structuring between areas, despite low genetic
variability and lack of phylogeographic struc-
ture. They related the observed differences to
habitat selective pressure, such as differences in
desiccation stress between areas. In contrast to
our study, their results indicated no clear cor-
relation of morphological (or genetic) variation
with ocean currents or geographic distance.
Possibly, the larval dispersal of P. d e p r e ss a may
be less effective than for A. angustipes. This
highlights the urgent need for further studies
to investigate the reproductive biology and lar-
val dispersal patterns in these key crab species
and other relevant decapods in tropical oceans,
especially considering the challenges produced
by climate change (Anger, 2001; Clarke et al.,
2020; Rebolledo & Wehrtmann, 2016; de San-
tana et al., 2018).
The same pattern could also be true for P.
depressa in the present study. Stress from desic-
cation due to high temperatures, together with
the behavior of carapace enlargement in prepa-
ration for the reproductive period, may explain
the results found in this area.
Another important point for understand-
ing species distributions in marine environ-
ments is the exchange of individuals between
populations, defined by the sum of local popu-
lations that are connected, generally by the
dispersion of planktonic larvae (Marshall et al.,
2010). If larval dispersal is interrupted by a geo-
graphic barrier, or if local populations respond
plastically to environmental factors or are sub-
ject to different selection pressures, geographic
variation may occur (Hopkins & Thurman,
2010) that can affect their survival, reproduc-
tion, and overall population health (Cadrin et
al., 2014). Teschima et al. (2016), were able to
observe the morphological and genetic struc-
turing of G. grapsus populations among Brazil-
ian oceanic islands through a combination of
morphometric and genetic techniques. They
explained this differentiation mainly by the
distance between the islands and the capacity
for larval dispersion through ocean currents.
Fernando de Noronha archipelago is about 345
km from the coast, which makes it virtually
impossible for local reef crabs to exchange with
17
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e00000, enero-diciembre 2024 (Publicado Nov. 22, 2024)
coastal populations, probably causing the mor-
phological differences observed herein.
The results obtained in this study provided
new information on several biological and
ecological aspects of populations of the reef
crab P. d e p re s s a in the WTA. Furthermore, this
study brought, for the first time, information on
this species in an oceanic insular environment.
Intraspecific morphological structuring was
identified in coastal and insular environments
with different levels of anthropogenic and envi-
ronmental stresses, where factors such as habi-
tat composition and structure, and exposure
time related to tidal patterns were identified as
potential causes for the phenotypic plasticity of
the reef crabs. Other factors such as geographic
isolation, biogeographic barriers and ocean
current patterns also appear to be relevant
factors in the morphological differentiation
between the populations studied which can
directly affect demographic rates, population
structure and dynamics, such as migration/
recruitment patterns, and responses to envi-
ronmental changes. However, studies related to
genetic connectivity are still needed to better
clarify if the phenotypic differences found in
this study extend to issues related to gene flow
within this species in the WTA. Our study and
such further studies are paramount to support
efforts for the conservation and management
of this cryptic species and for maintaining
the sustainability of marine resources in the
face of changing environmental conditions and
human pressures.
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.
ACKNOWLEDGMENTS
The authors thank the Federal University
of Pernambuco and the INCT AmbTropic proj-
ect (funded by CNPq, FAPESB, and CAPES)
for logistical support. We thank the CAPES-
Brazilian Ministry of Education for the Ph.D.
scholarships to AKRC. Thanks to the Bra-
zilian Ministry of the Environment (MMA)
for the SISBIO permit no. 71220. We thank
the Brazilian federal environmental protection
agency “Instituto Chico Mendes de Conserva-
ção da Biodiversidade-ICMBio” at Fernando
de Noronha for logistic support in the Archi-
pelago. We thank all people involved in the
fieldwork and laboratory analyses, especially
the fishermen and boat drivers in the study
areas, and all students and colleagues at the
Zooplankton Laboratory at UFPE’s Oceanogra-
phy Department, for their kind support.
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