Profiling abundance, size, and shell utilization patterns of Coenobita clypeatus (Fabricius, 1787) (Decapoda: Anomura: Coenobitidae) in protected and highly frequented beaches in Puerto Rico

Abstract

The coastal Caribbean is a well-known harbor for biodiversity, yet it is mainly valued for its ample resources and services. Economic interests typically supersede conservation efforts, introducing anthropogenic-related factors such as noise, chemical pollution, and geographical disturbances into the littoral zone, where ecological diversity is abundant. Although human activity is known to be detrimental to biodiversity across habitats, the effect of conservation measures that limit anthropogenic activity on coastal populations remains understudied. To measure the benefit of conservation in the littoral environment, we sampled populations of the hermit crab Coenobita clypeatus (Fabricius, 1787) of highly frequented (non-protected) and protected beaches in northern Puerto Rico. We profiled 1,119 individuals by using transects, describing their size and shell utilization patterns during winter and summer. The C. clypeatus population was larger (P < 0.0001 during both seasons) and more abundant (P = 0.0006 during winter, P < 0.0038 during summer) in the protected beach than in the non-protected beach, with no effect of season. Shell utilization patterns were more consistent in the protected beach, likely due to the greater availability of gastropod shells. These results suggest that the conservation measures implemented in the protected beach promote the survival, reproduction, and growth of hermit crabs in the location. Expansion of protected habitats through governmental and civilian efforts should enhance the conservation of the biodiversity of protected areas.

Full text

Journal of Crustacean Biology, 2022, 42, 1–9
hps://doi.org/10.1093/jcbiol/ruac048
Advance access publication 24 September 2022
Research Article
The Crustacean Society
© e Author(s) 2022. Published by Oxford University Press on behalf of e Crustacean Society. All rights reserved. For permissions, please e-mail: journals.permissions@oup.
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Received 24 January 2022; Accepted 2 September 2022
Proling abundance, size, and shell utilization paerns
of Coenobita clypeatus (Fabricius, 1787) (Decapoda:
Anomura: Coenobitidae) in protected and highly
frequented beaches in Puerto Rico
Francisco J.Torre s -To rres , Ana D.González-Colón*, Paola N.Negrón-Moreno*,
Naishka C.Rivera-Rosado, EnriqueCruz-Reyesand María I.De Jesús-Burgos
University of Puerto Rico at Cayey, Cayey, Puerto Rico 00736
*Equal contribution.
Correspondence: F.J. Torres-Torres; e-mail: franciscoj16@gmail.com and M.I. De Jesús-Burgos; e-mail: maria.dejesus2@upr.edu
ABSTRACT
e coastal Caribbean is a well-known harbor for biodiversity, yet it is mainly valued for its ample resources and services. Economic interests typically
supersede conservation eorts, introducing anthropogenic-related factors such as noise, chemical pollution, and geographical disturbances into the
lioral zone, where ecological diversity is abundant. Although human activity is known to be detrimental to biodiversity across habitats, the eect of
conservation measures that limit anthropogenic activity on coastal populations remains understudied. To measure the benet of conservation in the lit-
toral environment, we sampled populations of the hermit crab Coenobita clypeatus (Fabricius, 1787) of highly frequented (non-protected) and protected
beaches in northern Puerto Rico. We proled 1,119 individuals by using transects, describing their size and shell utilization paerns during winter and
summer. e C. clypeatus population was larger (P < 0.0001 during both seasons) and more abundant (P = 0.0006 during winter, P < 0.0038 during
summer) in the protected beach than in the non-protected beach, with no eect of season. Shell utilization paerns were more consistent in the protected
beach, likely due to the greater availability of gastropod shells. ese results suggest that the conservation measures implemented in the protected beach
promote the survival, reproduction, and growth of hermit crabs in the location. Expansion of protected habitats through governmental and civilian
eorts should enhance the conservation of the biodiversity of protected areas.
KEY WORDS: anthropogenic factors, conservation, Crustacea, natural reserves, West Indies
INTRODUCTION
An outstanding characteristic of the coastal regions of the
Caribbean region is its rich biological diversity (Beatley, 1991;
Anadon-Irizarry et al., 2012). In particular, the lioral zone har-
bors several unique animal species, including molluscs, echino-
derms, and crustaceans (Göltenboth et al., 2006). e economic
value of the lioral zone, however, aracts anthropogenic activ-
ity through tourism and urbanization, the eects of which may
threaten the integrity of coastal ecosystems (Chan & Blumstein,
2011; Ke et al., 2011). e destruction of the ecosystem, replace-
ment by structures, and disruption by chemical and noise pol-
lution may disturb the behavior of various animal species in
urbanized coastal regions (Beatley, 1991; Neves & Bemvenuti,
2006; Dauvin, 2008; Pine et al., 2016). Anthropogenic-related
factors increase energy expenditure when searching for food,
shelter (Stillman & Goss-Custard, 2002), and mates (Butler &
Maruska, 2020), impacting tness and decreasing population
density. Increasing the number and area of protected habitats
or natural reserves is a viable strategy to regulate urban develop-
ment and preserve biodiversity (Beatley, 1991; Ke et al., 2011).
More empirical data on the population of coastal organisms
occupying the understudied lioral zone is necessary to beer
understand the eects of urbanization and promote local legisla-
tion for coastal conservation.
e Caribbean hermit crab, Coenobita clypeatus (Fabricius,
1787), is a semi-terrestrial decapod crustacean that inhabits the
supralioral zone of tropical regions, including the Bahamas
(Morrison & Spiller, 2006), Jamaica (Warner, 1969), and Puerto
Rico (Nieves-Rivera & Williams, 2003). A variety of factors
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2 • TORRESTORRES ET. AL .: ABUNDANCE, SIZE, AND SHELL UTILIZATION IN COENOBITA CLYPEATUS
related to human presence, such as chemical contamination and
physical disturbances, adversely alter the population dynamics
of hermit crabs and other animals of the lioral zone (Schlacher
et al., 2016). Previous studies have reported that the marine
hermit crab, Pagurus bernhardus (Linnaeus, 1758) is slower and
more hesitant to change from a suboptimal to an optimal shell
when exposed to reduced sea water pH, indicating the poten-
tial vulnerability of resource assessment and decision-making
to environmental stressors (de la Haye et al., 2011). Another
environmental stressor, sound pollution, was also found to alter
social behavior in P. bernhardus, depending on the size of the shell
occupied (Tidau & Bria, 2019). Ryan et al., (2012) showed that
short bursts of elevated levels of sound had a detrimental eect
on the response of C. clypeatus to predators. Roberts (2021)
characterized chirp events in Coenobita compressus (H. Milne
Edwards, 1837), which occurred during shell ghts and in the
presence of conspecics. Despite these ndings, dierences in
the population dynamics of coastal organisms, such as C. clypea-
tus, in protected and non-protected environments are yet to be
documented.
We used the transect method to compare dierences in the
paerns of abundance, size, and shell utilization by C. clypeatus
in a non-protected, highly frequented beach and in a protected
natural reserve on the northern coast of Puerto Rico. We hypoth-
esized that C. clypeatus is less abundant and smaller in size in the
non-protected beach in comparison to a protected beach. Our
goal is that the presented data will promote local legislation to
preserve the coastal region and increase the size and number of
protected coastal areas. Furthermore, our research may establish
C. clypeatus as a local bioindicator (Holt & Miller, 2010) to study
the eects of regulations in the lioral zone.
METHODS
Study site
We selected two study sites in the northern coast of the main
island of the Puerto Rican archipelago. Both sites have a similar
topography, vegetation, tidal activity, and weather conditions,
but with dierences in anthropogenic activity (Fig. 1). e ana-
lyzed beaches were Puerto Nuevo in Vega Baja (18.490103º
N, –66.3945295º W), a non-protected and highly frequented
beach, and Hacienda La Esperanza in Manatí (18.4808763º
N, –66.5196964º W), the largest natural reserve of its type in
northern Puerto Rico. e two study sites are approximately
13.52 km apart. Both beaches include subtidal environments
populated by seagrass meadows and aeolianite rock formations.
e beaches also share similar land vegetation (grasses, vines,
Coccoloba uvifera, Calophyllum antillarum). Puerto Nuevo and
La Esperanza beaches, nevertheless, dier in the anthropo-
genic eects along the study sites, where the former is located
near a commercial and residential area, as well as a main road,
whereas the laer is located farther from less densely populated
urban areas. We dened a non-protected beach as an area with
constant anthropogenic activity and minimal regulation medi-
ated by governmental or non-governmental organizations. In
contrast, we dene a protected beach as an area where ecolog-
ical features are preserved, and anthropogenic activity is regu-
lated by governmental or non-governmental organizations. e
implementation of conservation measures in La Esperanza is
managed and monitored by the non-prot organization, Para la
Naturaleza (hps://www.paralanaturaleza.org/).
e eld studies were conducted in cycles and were com-
pleted in the morning over two consecutive days in each beach.
Annual dierences in tide levels, as well as lioral dynamics may
vary per season within the same studied beach. Beach-visitation
paerns were also likely to dier due to seasonal variations in
weather and anthropogenic activity. For these reasons, eld stud-
ies were conducted during January (winter) and July (summer).
Transect sampling
e broadest ecological diversity of the lioral area can be found
in the supralioral zone, which is dened by the onset of coastal
vegetation on the shore inward (Peters & Lodge, 2009). We used
the transect and quadrats method (see Bertness, 1981) to assess
hermit crab abundance, size, and shell utilization paerns, in the
supralioral zones of the studied beaches. Five transects, each 5
m long, were laid parallel to each other and 5 m apart from each
other. Each transect was composed of ve 1 m2 × 1 m2 quadrats.
Transects were positioned perpendicular to the shoreline and
began within the supralioral zone. Hermit crabs were counted
and analyzed from odd quadrats at 8:00, 9:00, 10:00, 11:00, and
12:00 noon. Hermit crab individuals were retained aer each
period of quadrat sampling until all transects were completed to
avoid recounting individuals. Crabs were relocated and distrib-
uted within the studied site following data collection.
Measurements of crab size and percentage of shell
occupation
e major chela of hermit crab individuals was measured in the
eld as a morphological character to estimate size with minimal
disturbance (see Colón-Piñeiro et al., 2021; Morrison & Spiller,
2006). We measured the length of the major chela with calipers ±
0.01mm. To evaluate shell utilization paerns, we photographed
the occupied gastropod shell to identify the species. e hermit
crab’s dry body weight was estimated from a linear regression
correlating dry body weight and chela length: Y= 0.231+2.995
* x, where Y = dry body weight and x = measured chela length in
mm (Morrison & Spiller, 2006). e percentage of shell occupa-
tion per season was calculated by dividing the number of hermit
crabs that occupied the shell of a particular species of gastropod,
over the total number of hermit crabs proled in both the highly
frequented and protected beach, during winter or summer.
Statistical analysis
A two-way repeated measures ANOVA was used to compare
crab abundance dierences in the non-protected and protected
beaches (Fig. 2). A mixed-eects two-way ANOVA was used to
compare dierences between chela length and dry body weight
measurements in the non-protected and protected beaches (Fig.
3). Post-hoc Šídák’s tests were used when there was a main eect
of beach type or an interaction between beach type and season
(Figs. 2, 3).
We performed linear regressions to visualize slopes between
beach types and seasons, as well as to make an initial probe of
the relationship between chela length (mm) and shell aper-
ture length (mm). Because chela length (mm) has a positive
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TORRESTORRES ET. AL .: ABUNDANCE, SIZE, AND SHELL UTILIZATION IN COENOBITA CLYPEATUS • 3
relationship with dry body weight (g) and serves as a proxy for
crab size, we explored whether chela length would also correlate
positively with shell aperture length. Linear regression analyses
were used (Fig. 4, Table 1).
To evaluate the relationship of shell aperture length with
chela length, beach type, and season, we performed a general-
ized linear model (GLM). To establish which predictive variable
had the higher correlation, we calculated the percent of variation
Figure 1. Study site topography is similar between Puerto Nuevo (18.490103º; -66.3945295º W; Google Earth,
hps://earth.google.com/web/search/Hacienda+La+Esperanza+Para+la+Naturaleza,+Calle+La+Esperanza,+
Manat%C3%AD,+Puerto+Rico/@18.47520438,-66.52260072,16.00127533a,3274.35212106d,35y,-0h,0t,0r/
data=CigiJgokCZ4W3asvgDJAEU6lvKmgfDJAGbRsMeqnmFDAISgze6pNmlDA) (A) and La Esperanza (18.4808763º N, –66.5196964º
W; Google Earth, hps://earth.google.com/web/@18.4937774,-66.39811953,6.56378605a,2444.42792695d,35y,-0h,0t,0r) (B). Google ©
Maxar Technologies Data SIO, NOAA, U.S. Navy, NGA, GEBCO TerraMetric.
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4 • TORRESTORRES ET. AL .: ABUNDANCE, SIZE, AND SHELL UTILIZATION IN COENOBITA CLYPEATUS
explained by each variable included in the model, dividing the
regression sum of squares for each predictive variable by the total
sum of squares (Acevedo-Charry & Aide, 2019; Colón-Piñeiro
et al., 2021). GLM analysis summary is included in Table 2.
To verify whether the number of gastropod-shell types var-
ied signicantly between the studied beaches, we performed a
Chi-square test of independence comparing the frequency of the
most occupied shells during both winter and summer seasons.
Dierences were considered statistically signicant when proba-
bility values were  0.05.
R E S U LT S
A two-way ANOVA revealed a signicant eect of beach type on
the number of crabs collected in each transect (F(1,18) = 26.42, P
< 0.0001). We found no eect of season nor interaction between
season and beach type on the number of crabs collected in each
transect (F(1,18) = 0.003039, P = 0.9566, F(1,18) = 0.2015, P =
0.659, respectively). Šídák’s multiple comparisons test revealed
that more crabs were collected on average in each transect at
the protected beach compared to the non-protected, highly fre-
quented beach for both the winter and summer seasons (t(36) =
3.983, P = 0.0006, t(36) = 3.354, P < 0.0038, respectively) (Fig. 2).
e total number of crabs identied during winter and summer
was 101 and 126 in the non-protected beach, 462 and 430 in the
protected beach, respectively.
A mixed-eects two-way ANOVA revealed a signicant
eect of beach type (F(1,1115) = 338.1, P < 0.0001) on chela
length in the two types of beaches analyzed. No eect of season
(F(1,1115) = 0.4026, P = 0.5259) or season versus beach (F(1,1115) =
1.780, P = 0.1824) was detected. Šídák’s multiple comparisons
test revealed that crabs collected from the protected beach are
larger, as measured by chela length, compared to those from the
non-protected beach for both the winter and summer seasons
(t(1115) = 11.41, P < 0.0001, t(1115) = 14.34, P < 0.0001, respec-
tively) (Fig. 3A). Since dry body weights were not measured in
the eld, we used the formula (Y = 0.231+2.995 * x) (Morrison
& Spiller, 2006) to estimate the crabs’ dry body weight. Similarly,
mixed-eects two-way ANOVA revealed a signicant eect of
beach type (F(1,1115) = 338.1, P < 0.0001). No eect of season
(F(1,1115) = 0.4026, P = 0.5259) or season versus beach (F(1,1115)
= 1.780, P = 0.1824) was detected. Šídák’s multiple compar-
isons test also revealed that crabs collected from the protected
beach have a higher dry body weight compared to those from the
non-protected beach for both seasons (t(1115) = 11.41, P < 0.0001,
t(1115) = 14.34, P < 0.0001, respectively) (Fig. 3B). Since dry body
weight estimates were calculated using the formula of Morrison
& Spiller (2006), which uses chela length as the explanatory
variable, the statistics obtained from the mixed-eects two-way
ANOVA and Šídák’s multiple comparisons test are the same.
Overall, these ndings suggest that both dry body weight and
major chela length are accurate estimates of crab size.
Linear regression analyses of the relationship between chela
length and shell-aperture length revealed that in both the pro-
tected and non-protected beach, regardless of season, there
is a signicant and positive relationship between the two vari-
ables (Table 1). We used a generalized linear model (GLM) to
assess the statistical signicance of major chela length, location,
and season as predictors for shell aperture length. e GLM
test revealed that chela length is the most important predictive
variable in the model, predicting most of the variance (76%) in
shell-aperture length (Table 2).
To assess shell-occupation patterns in the field, each shell
was photographed, and the gastropod identified. During
winter, hermit crabs in the non-protected beach utilized
24 genera of gastropod shells, of which 11 were unique to
Puerto Nuevo. In the protected beach, hermit crabs occu-
pied 36 different genera of gastropods, and of these, 24 were
only found in La Esperanza. During summer, hermit crabs
of the non-protected beach utilized 23 genera of gastropods,
where only three were unique to Puerto Nuevo. In the pro-
tected beach, 39 different gastropod genera were occupied
by crabs, and 19 of these shells were only documented in La
Esperanza. Shell occupation was measured in percentage of
occupation of each identified gastropod shell observed per
season (Supplementary material Tables S1, S2), for winter
and summer, respectively. Measuring the frequency of shell
use by beach type, the most used shells in the non-protected
beach during winter were the land snail Bulimulus guadalupen-
sis (Bruguière, 1789) (18.8%), the tessellated nerite Nerita
tessellata (Gmelin, 1791) (11.9%), and the green star shell
Astraea tuber (Linnaeus, 1767) (9.9%). During summer, the
most used shells in the non-protected beach were the glossy
dove shell Nitidella nitida (Lamarck, 1822) (34.1%), N. tes-
sellata (9.5%), and A. tuber (6.4%). The most used shells in
the protected beach during winter were A. tuber (34.9 %),
N. tessellata (11.5 %), and the beaded periwinkle Tect ar iu s
muricatus (Linnaeus, 1758) (7.6 %), and following the same
Figure 2. e abundance of Coenobita clypeatus according to the
beach type and season.
Figure 3. Major chela size (A) and body weight (B) of Coenobita
clypeatus by beach type and season.
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TORRESTORRES ET. AL .: ABUNDANCE, SIZE, AND SHELL UTILIZATION IN COENOBITA CLYPEATUS • 5
Figure 4. Linear relationship between chela length (mm) and shell aperture length (mm) of Coenobita clypeatus by beach and season.
Table 1. Linear regression analyses of the relationship between the chela length and aperture length of occupied gastropod shells by the C.
clypeatus population of conserved and non-conserved beaches.
Beach type Season DFn, DFd Intercept Slope R2 P
Highly Frequented Winter 1, 99 1.574 1.025 0.9283 < 0.001
Highly Frequented Summer 1, 124 0.4785 0.9254 0.9115 < 0.001
Protected Winter 1, 460 2.736 0.8010 0.5814 < 0.001
Protected Summer 1, 428 1.881 0.8300 0.7250 < 0.001
Table 2. Generalized linear-model analysis of the eects of chela length, beach type, season, and the interaction between beach type and season
on the aperture length of shells occupied by C. clypeatus populations in non-conserved and conserved beaches.
Estimate + SE Pr(> |t|) % Variance explained
Intercept 1.64955±0.15351 < 0.001 NA
Chela 0.85848±0.01619 < 0.001 76.31%
Beach 0.91986±0.17997 < 0.001 0.004%
Season 0.64446±0.10962 < 0.001 1.35%
Beach * Season 0.85175±0.24411 < 0.001 0.23%
Residuals 21.72%
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6 • TORRESTORRES ET. AL .: ABUNDANCE, SIZE, AND SHELL UTILIZATION IN COENOBITA CLYPEATUS
pattern, A. tuber (28.8%), N. tessellata (12.1%), and T. muri -
catus (7.7%) during summer.
e Chi-square test of independence indicated signicant dif-
ferences in the frequency of identied shells between the pro-
tected and non-protected beaches during winter (P > 0.0001)
and summer (P > 0.0001). During winter, shells of A. tuber and
N. tessellata were less abundant than expected in the non-pro-
tected beach, and fewer shells of A. tuber and more of B. guadalu-
pensis than expected were identied in the non-protected beach
during summer. More shells of B. guadalupensis than expected
were also identied in the non-protected beach but less abun-
dant than expected in the protected beach during summer. e
expected frequencies of shell occupancy were based on the
residuals (< –5 and > 5) from the Chi-square test. e most
frequently occupied shells during winter (Fig. 5A) and summer
(Fig. 5B) are also shown.
DISCUSSION
ere is global concern over the eects that the increase in urban-
ization and other anthropogenic-related factors have on biodi-
versity (Roy et al., 2003; Worm et al., 2006; Alonso et al., 2008;
McDonald et al., 2008; Morris, 2010). To promote thoughtful
and eective legislation that protects biodiversity, empirical
data that evidence the negative consequences of anthropogenic
activity on animal abundance in the lioral zone are particularly
required in the Caribbean. We used C. clypeatus as a bioindica-
tor to assess dierences in populations in relation to the conser-
vation status of particular areas because of the ubiquity of the
species across the coasts of Puerto Rico and its susceptibility to
disturbed-environment cues (Nieves-Rivera & Williams, 2003;
Ryan et al., 2012). Although Puerto Nuevo has been recog-
nized as a Blue Flag beach (hps://blueag.us/), a certication
reserved for beaches that meet environmental safety and quality
standards, our results show that there are signicantly fewer and
smaller hermit crabs with more varied shell use between seasons
in this highly frequented beach when compared to the protected
beach. ese results may be due to the dierences in regulatory
systems that control anthropogenic activity in the beaches, sug-
gesting that conservation measures have a positive impact on the
population dynamics of animals in the lioral zone.
Coenobita clypeatus was more than twice as abundant in the
protected beach than in the highly frequented, non-protected
beach during both seasons (Fig. 2). Dierences in its abun-
dance may reect migration to other lioral regions induced
by the species’ inability to properly adapt to anthropogenic
disturbances. e status of Puerto Nuevo as a Blue Flag beach
(hps://www.vegabaja.gov.pr/) marks it as a popular tourist
araction, with up to 15,000 beachgoers a month visiting during
the tourist season. Studies have shown that marine and non-
aquatic vertebrates, such as the harbor porpoise, Phocoena phoc-
oena (Linnaeus, 1758) and the northern saw-whet owl, Aegolius
acadicus (Gmelin, 1788) change routes and location due to
acoustic pollutants (Kastelein et al., 2013; Dyndo et al., 2015;
Mason et al., 2016; Mamo et al., 2018). Decapod crustaceans are
not exempt from the eect of acoustic disturbance. Wale et al.,
(2013) showed that the ability of the brachyuran crab, Carcinus
maenas (Linnaeus, 1758) to evade predators is disrupted by boat
noise. Another study showed that the withdrawal response of C.
clypeatus, a defensive anti-predator behavior, is sensitive to pro-
longed innocuous sound exposure (Stahlman et al., 2011). is
eect was referred to by Chan et al. (2010) as the distracted prey
hypothesis, which states that the limited aentional resources an
animal possesses are occupied by anthropogenic noise, increas-
ing predation risk. e distracted prey hypothesis, as well as
migration towards unaected regions, could apply to local C.
clypeatus and other lioral animals, and may partially explain the
reduced number of hermit crabs in the non-protected beach.
Figure 5. Ten most utilized gastropod shells by Coenobita clypeatus by season and beach type.
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TORRESTORRES ET. AL .: ABUNDANCE, SIZE, AND SHELL UTILIZATION IN COENOBITA CLYPEATUS • 7
Another potential factor inuencing the abundance and size
of C. clypeatus is a reduced availability of gastropod shells in the
lioral zone. Shells play a pivotal role in the survival and social
and reproductive behaviors of hermit crabs. e abdominal
region lacks the protective exoskeleton of the cephalothorax,
and shells protect the vulnerable abdominal region from desic-
cation, predation, and abrasion (i.e., Szabó, 2012). Molting and
subsequent growth are chiey dependent on the internal volume
of the shell, which crabs obtain via scavenging or shell exchange
(Elwood, 2022). e clutch size of a female hermit crab is also
dependent on the size of the occupied shell (Conover, 1978;
Bertness, 1981; Hazle, 1981). Due to the value of this resource,
hermit crabs have evolved to thoroughly examine each shell
encountered, selecting a shell that corresponds to their general
size in order to maximize their individual tness (Hazle, 1981;
Szabó, 2012).
Shell selection is an example of a decision-making process
that is aected by external factors (Reese, 1963; Conover, 1978;
Bertness, 1981; Hazle, 1981; McClintock, 1985; Lewis &
Rotjan, 2009; Rotjan et al., 2010). e shell utilization data indi-
cates that the type of shells used by C. clypeatus in the protected
beach does not vary substantially between seasons, favoring the
green star shell (A. tuber), a preference that was also observed
in Puerto Rico by Colón-Piñeiro et al. (2021). Hermit crabs of
the highly frequented beach, conversely, showed greater varia-
tion in the type of shell used in both seasons sampled. Although
natural dierences in the abundance and species of gastropods
in the studied beaches may impact shell occupation in C. clypea-
tus (Colón-Piñeiro et al., 2021), the studied beaches are similar
environments, containing aeolianite rock formations and sea-
grass meadows, as well as comparable tidal activity and land veg-
etation. e observed dierences in shell utilization paerns are
thus less likely to be due to natural variation in distribution of
gastropod species in each area. Given these observations, along
with those of other studies (Lange et al., 2013; Bloch & Klingbeil,
2016), it is instead probable that gastropod populations and
shell availability are impacted by human activity, inuencing
shell utilization, and subsequently, the potential abundance and
size of C. clypeatus.
Analysis of major chela length as a general indicator of size
(Morrison & Spiller, 2006; Colón-Piñeiro et al., 2021) demon-
strated that hermit crabs at the non-protected and highly fre-
quented beach are signicantly smaller than those in the protected
beach. e proportions of the shells occupied by C. clypeatus as
measured by the shell aperture length (mm) scaled positively
with hermit crab size, as measured by chela length (mm). ese
results are supported by Colón-Piñeiro et al. (2021) showing a
positive relationship between shell proportions and crab size.
is is not surprising considering that shell aperture length is
a quality assessed by C. clypeatus to appropriately select a shell
that meets the necessary dimensions to protect from desiccation
and predation (Szabó, 2012). As hermit crabs have evolved to be
entirely dependent on the shells available, this trait has the draw-
back of needing a constant supply of shells of increasing size,
which crabs must continually scavenge and evaluate (Morrison
& Spiller, 2006). Fewer larger shells available per beach are there-
fore a limiting growth factor for animals inhabiting both sampled
beaches. Gastropods and their shells are frequently collected for
their gastronomic and aesthetic value, limiting their availability
in the beach (Roy et al., 2003). Gastropods such as Ciarium
pica, Astraea tuber, and Nerita tessellata grow to medium and
large sizes and are oen collected for consumption, a practice
that goes unregulated in the non-protected beach. is indirect
anthropogenic interaction should be evaluated in future studies,
as these may contribute to the reduced size and abundance of
hermit crabs from highly frequented beaches when compared to
those of the protected beaches.
e impact of anthropogenic factors on coastal areas, and
the interactions between humans and the lioral zone, are com-
plex and far-reaching. Although hermit crabs and humans have
been shown to be capable of forming mutualistic relationships
(Barnes, 2001), the potential benet of increased anthropogenic
activity in the non-protected lioral zone is not reected by our
ndings. e C. clypeatus prole generated herein suggests that
the protected beach harbors more optimal conditions for the
hermit crab population than the highly frequented beach. is
may be due to the variety of factors and anthropogenic activi-
ties that threaten the ecological integrity of the coastal region,
which is minimized in protected beaches (Ke et al., 2011).
Determining the specic anthropogenic factors inducing the
observed dierences in the C. clypeatus population, was beyond
the scope of our study. Potential anthropogenic-related factors
may include but are not limited to pollution, overexploitation of
resources, introduction of invasive species, governmental man-
agement issues, and even human perception of coastal ecosys-
tems (Beatley, 1991; Suchanek, 1994; Lande, 1998; Reid et al.,
2005; Forster et al., 2011). Although any of these factors could
adversely alter the population dynamics of animals in the lioral
zone, pollution is known to be a signicant contributor to bio-
diversity loss, specically in coastal regions (Wafar et al., 2011).
Exposure to common coastal contaminants, such as heavy met-
als, adversely aects the social behavior and reproduction of
hermit crabs, which in turn impacts abundance (Aghabozorgi
Nafchi & Chamani, 2019). e eects of copper exposure in
the ghting behavior of P. bernhardus (White et al., 2013), and
the cardiac and respiratory function of the brachyuran crab,
Carcinus maenas have been described (Mh, 1984). Tributyltin,
a historically common antifouling agent, provokes morphologi-
cal disruption of the ovaries in female Clibanarius viatus (Bosc,
1801) (Sant’Anna et al., 2012). e negative ecological impact
that anthropogenic factors impose on the behavior of coastal
organisms, not only threatens biodiversity, but also impacts their
sustainability and capability to meet human resource demands
(Worm et al., 2006). Immediate action, in the form of increased
conservation measures, must be taken to limit the noxious con-
sequences of anthropogenic activities in the lioral zone and
prevent further biodiversity loss (Alonso et al., 2008).
Anadon-Irizarry et al., (2012) identied key biodiversity
areas along Caribbean coastlines, including the coastal regions
of Puerto Rico. Expansion of protected areas, such as natural
reserves, can help to protect biodiversity and benet the local
population via the sustainable use of natural resources (Burgess
et al., 2017; van Schalkwyk et al., 2019). Proper conservation
methods also require a robust catalog of the local ora and fauna.
ese eorts typically focus on vertebrate and plant species
so a broader number of taxa must be considered to eectively
preserve biodiversity. Conservation measures, such as those
implemented in the Hacienda La Esperanza, provide optimal
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8 • TORRESTORRES ET. AL .: ABUNDANCE, SIZE, AND SHELL UTILIZATION IN COENOBITA CLYPEATUS
conditions to hermit crab populations. Our study has shown that
C. clypeatus can serve as a useful model organism to study the
benets of conservation measures in lioral organisms. ese
ndings, along with further research, should encourage legis-
lative measures to expand the area and number of lioral pro-
tected areas to mitigate the impact of anthropogenic activity for
the protection of coastal biodiversity.
SUPPLEMENTARY MATERIAL
Supplementary material is available at Journal of Crustacean
Biology online.
Table S1. Gastropod shells utilized by Coenobita clypeatus
in the protected (La Esperanza) and highly frequented beach
(Puerto Nuevo) during late winter.
Table S2. Gastropod shells utilized by Coenobita clypeatus
in the protected (La Esperanza) and highly frequented beach
(Puerto Nuevo) during summer
ACKNOWLEDGEMENTS
We thank the Centers for Research Excellence in Science and
Technology (CREST) Puerto Rico Center for Environmental
Neuroscience (PRCEN) for supporting the research (grant:
National Sciences Foundation (NSF) Human Resource
Development (HRD) 1736019). Special thanks to Dr. Vivian
Mestey, who mentored the authors in shell identication. We
also extend our gratitude to the Institute of Interdisciplinary
Research of the University of Puerto Rico at Cayey, and the
anonymous reviewers for their valuable contributions. We thank
the undergraduate students who contributed to the project:
Wilfredo Torres-Rivera, Aidimar Rodríguez-Fuentes, Emanuel
Zayas-Díaz, Victoria Blaioa-Vázquez, Ariana Figueroa-
González, Natalia Rivera-Rolón, Krystal M. Santiago-Colón,
Gabriel J. Cruz-Rodríguez, and María I. González-De Jesús.
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