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Taxonomic Diversity of Decapod and Stomatopod Crustaceans Associated with

Pocilloporid Corals in the Central Mexican Pacific

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DOI: 10.3390/d14020072

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 diversity
Article
Taxonomic Diversity of Decapod and Stomatopod Crustaceans
Associated with Pocilloporid Corals in the Central
Mexican Pacific
Arizbeth Alonso-Domínguez 1 , Manuel Ayón-Parente 2 , Michel E. Hendrickx 3 , Eduardo Ríos-Jara 2 ,
Ofelia Vargas-Ponce 4 , María del Carmen Esqueda-González 2 and Fabián Alejandro Rodríguez-Zaragoza 2, *

1 Programa de Doctorado en Ciencias en Biosistemática, Ecología y Manejo de Recursos Naturales y

Agrícolas (BEMARENA), Centro Universitario de Ciencias Biológicas y Agropecuarias,
Universidad de Guadalajara, Camino Ramón Padilla Sánchez No. 2100, Nextipac,
Zapopan C.P. 45200, Mexico; [email protected]
2 Laboratorio de Ecología Molecular, Microbiología y Taxonomía, Departamento de Ecología,
Centro Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara, Camino Ramón
Padilla Sánchez No. 2100, Nextipac, Zapopan C.P. 45200, Mexico; [email protected] (M.A.-P.);
[email protected] (E.R.-J.); [email protected] (M.d.C.E.-G.)
3 Laboratorio de Invertebrados Bentónicos, Unidad Académica Mazatlán, Instituto de Ciencias del Mar y
Limnología, Unidad Mazatlán, Universidad Nacional Autónoma de México, Avenida Joel Montes Camarena
S/N Apartado Postal 811, Mazatl C.P. 82040, Mexico; [email protected]
4 Departamento de Botánica y Zoología, Centro Universitario de Ciencias Biológicas y Agropecuarias,
Universidad de Guadalajara, Camino Ramón Padilla Sánchez No. 2100, Nextipac,



Zapopan C.P. 45200, Mexico; [email protected]


* Correspondence: [email protected]
Citation: Alonso-Domínguez, A.;
Ayón-Parente, M.; Hendrickx, M.E.;
Abstract: Many crustacean species are obligate associates of pocilloporid corals, where they feed,
Ríos-Jara, E.; Vargas-Ponce, O.;
reproduce, and find shelter. However, these coral-associated crustaceans have been poorly studied in
Esqueda-González, M.d.C.;
the eastern tropical Pacific. Determining the crustacean richness and taxonomic distinctness could
Rodríguez-Zaragoza, F.A. Taxonomic
Diversity of Decapod and
help in comparing different coral reefs and the potential effects of degradation. This study evalu-
Stomatopod Crustaceans Associated ated the spatio–temporal variation of the taxonomic diversity and distinctness of coral-associated
with Pocilloporid Corals in the crustaceans in four ecosystems of the Central Mexican Pacific (CMP) with different conditions and
Central Mexican Pacific. Diversity coral cover. In all ecosystems, 48 quadrants were sampled during the summer and winter for two
2022, 14, 72. https://doi.org/ years. A total of 12,647 individuals belonging to 88 species, 43 genera, and 21 families were recorded.
10.3390/d14020072 The sampling effort yielded 79.6% of the expected species richness in the study area. Species rarity
Academic Editors: Michael Wink and
had 19% singletons, 4% doubletons, 22% unique, and 9% duplicate species; two species represented
Simone Montano new records for the Mexican Pacific, and six were new to the CMP. This study recorded most of the
symbiotic crustacean species in pocilloporid corals previously reported in the CMP. The taxonomic
Received: 15 December 2021
diversity and distinctness differed significantly between coral ecosystems and seasons, which was
Accepted: 18 January 2022
also visualized by nMDS ordination, showing an evident spatio–temporal variation in the taxonomic
Published: 21 January 2022
beta diversity.
Publisher’s Note: MDPI stays neutral
with regard to jurisdictional claims in Keywords: crustacean; coral-associated; western Mexico; Pocillopora; diversity
published maps and institutional affil-
iations.

1. Introduction
Copyright: © 2022 by the authors.
Invertebrates are frequently associated with scleractinian corals of the genus Pocil-
Licensee MDPI, Basel, Switzerland. lopora [1]. Macrocrustaceans are the most representative coral-associated fauna. Among
This article is an open access article these, diverse assemblages find shelter among the Pocillopora branches [2,3]. Different
distributed under the terms and taxa, including shrimps, crabs, isopods, and copepods, have been described as coral sym-
conditions of the Creative Commons bionts [4], presenting different degrees of specialization in form and function [5]. Several
Attribution (CC BY) license (https:// of these species are obligate symbionts, always and permanently associated with specific
creativecommons.org/licenses/by/ hosts, while other species are facultative symbionts that can also survive outside their
4.0/). host, usually on non-living substrates [1,5]. As a general trend, the coral-associated fauna

Diversity 2022, 14, 72. https://doi.org/10.3390/d14020072 https://www.mdpi.com/journal/diversity

Diversity 2022, 14, 72 2 of 13

depends on the host for feeding and refuge [6,7]. In addition, coral-associated crustaceans
help to maintain coral health by performing cleaning activities, such as removing sedi-
ment and parasites [8,9]. Some species also have an active role in their defense against
predators. For example, species of Trapezia defend the coral from predators, such as the
crown star (Acanthaster planci) [10,11], and the shrimp Alpheus lottini protects the coral
from coralivorous mollusks of the genus Drupella [12]. Crustaceans represent up to 80%
of the coral-associated fauna [1,13], playing multiple ecological roles. They are part of
different trophic relationships: acting as predators, parasites, herbivores, scavengers, and
detritivores. Most obligate symbionts are mucus, suspension, or deposit feeders [1,5]. Thus,
they link primary producers with high-level consumers [14–16]. This strong relationship
between corals and crustaceans can be affected by the changes induced by anthropogenic
activities or climate change [1,7].
The coral ecosystems of the Central Mexican Pacific (CMP) are dominated by sev-
eral species of Pocillopora [17,18]. The most common is P. verrucosa, but other species,
such as P. damicornis, P. capitata, P. eydouxi, P. effusus, P. inflata, and P. meandrina, have
also been recorded [18]. Pocilloporid corals are structurally complex, generating many
microhabitats for crustaceans [1]. However, few studies have focused on the crustacean
diversity associated with pocilloporid corals in this area. Earlier studies in the Mexican
Pacific by Pereyra-Ortega [19] and Hernández [20] described the decapods associated
with Pocillopora corals in Isla Espíritu Santo and the southern area of the Baja California
peninsula. Ramírez-Luna et al. [21] studied the temporal variation of the xanthid crabs
in Huatulco Bay, Oaxaca, and found the largest diversity and abundance during the dry
season. Hernández et al. [22,23] analyzed the impact of coral bleaching and hurricanes
on the diversity and abundance of decapods from La Paz and Loreto Bay, Baja California
Sur. They concluded that these phenomena changed the species richness considerably,
decreasing the abundance of coral-associated decapod species. Two studies have evaluated
the diversity of coral-associated crustaceans in the CMP, including the coastal region from
Nayarit to Michoacan. Hernández et al. [24] performed a visual census of the decapods
in coral ecosystems and found 36 species, with most individuals in or near corals. Ayón-
Parente et al. [25] formulated an inventory of 19 species of caridean shrimps associated
with the Pocillopora from Chamela Bay, Jalisco. Although both studies contributed to the
inventories of the crustaceans associated with pocilloporid corals of the CMP, they did not
offer evidence of possible spatio–temporal changes in their species richness and abundance,
nor did they evaluate the contribution of the different taxonomic categories to diversity.
The average taxonomic distinctness (∆+ ) index has been used to assess biodiversity [26].
Environmental variability, sampling effort, and sampling size can affect most classical
indices based on species richness and evenness [27]. However, the ∆+ and its variation (Λ+ )
are good ecological indicators, because they reflect the taxonomic relatedness of species
within assemblages [28,29]. These indices allow for comparing different studies because
they are independent of sample size and effort and provide a test for the significance of
departure from expectation by chance if no other studies are available for comparison [30].
This analysis determines how certain taxa contribute to the total taxonomic diversity [26].
The taxonomic distinctness and its variation have mainly been used to evaluate biodiversity
in time and space scales in different assemblages such as freshwater fishes [31,32], marine
invertebrates [29,33,34], and insects [35,36].
In this study, the main objective was to use the species richness and taxonomic distinct-
ness to assess the spatio–temporal variation of the decapods and stomatopods associated
with the coral Pocillopora in the CMP. Knowing this information could help us understand
the potential effects of coral reef degradation [7]. This area harbors the highest richness
and coral coverage of the Mexican Pacific [17,18]; its coral ecosystems are dominated by
the Pocillopora genus, which includes up to 80% of coral-associated fauna [1,13]. The CMP
has suffered from a significant human impact and, although some areas are protected,
most of the coral ecosystems are not [18]. Corals are very susceptible to environmental
changes and natural and anthropogenic impacts. These changes affect associated fauna,
Diversity 2022, 14, x FOR PEER REVIEW 3 of 13

Diversity 2022, 14, 72 3 of 13

protected, most of the coral ecosystems are not [18]. Corals are very susceptible to envi-
ronmental changes and natural and anthropogenic impacts. These changes affect associ-
ated fauna, especially symbiotic species. Evidence has shown that the Pocillopora-associ-
especially
ated faunasymbiotic species. Evidence
has a spatio–temporal has shown
variation due tothat the Pocillopora-associated
environmental fauna has
drivers [3,6,21,37]. We
ahypothesized
spatio–temporal variation due to environmental drivers [3,6,21,37]. We hypothesized
that the sites with the most discontinuous coral cover and highest human
that the sites with the most discontinuous coral cover and highest human intervention
intervention (local tourism, fishing, etc.) would have the lowest richness and taxonomic
(local tourism, fishing, etc.) would have the lowest richness and taxonomic distinctness,
distinctness, along with a high abundance of coral-associated fauna due to the low cover-
along with a high abundance of coral-associated fauna due to the low coverage and greater
age and greater isolation of the host coral colonies.
isolation of the host coral colonies.
2. Materials
2. and Methods
Materials and Methods
2.1. Study
2.1. Study Area
Area
The study
The study area
area included
included four
four coral
coral ecosystems
ecosystems in in the
the Central
Central Mexican
Mexican Pacific
Pacific (CMP):
(CMP):
Chamela and
(i) Chamela and (ii)
(ii) Cuastecomate-Punta
Cuastecomate-Punta Melaque Melaque in southern Jalisco, and (iii) Carrizales
and (iv)
(iv) Punto
PuntoBBininColima
Colima (Figure
(Figure1).1).
TheThe
CMP CMPis part of theofeastern
is part tropical
the eastern PacificPacific
tropical ecore-
gion spanning from Baja California to northern Peru and the Galapagos
ecoregion spanning from Baja California to northern Peru and the Galapagos Islands, Islands, Ecuador
[38]. In the
Ecuador summer,
[38]. In the the CMP is
summer, influenced
the by the California
CMP is influenced Current, the
by the California Cabo Corrientes
Current, the Cabo
Upwelling,Upwelling,
Corrientes the Mexican theWarm
MexicanPool, and the
Warm Costa
Pool, and Rica Coastal
the Costa Current.
Rica CoastalHowever, these
Current. How-
currents
ever, have
these a weaker
currents effect
have duringeffect
a weaker the winter
during andthespring
winterdue to the
and colddue
spring water
to from the
the cold
California
water fromCurrent and the
the California warm and
Current water thefrom
warmthewater
Cortés
fromCurrent [39]. Current
the Cortés Furthermore, the
[39]. Fur-
thermore,
Mexican Warm the Mexican
Pool isWarm
part ofPool
the isWestern
part of the Western Hemisphere
Hemisphere Warm Pool,Warm whichPool, which
induces an
induces an important annual climatic variation in the water temperature
important annual climatic variation in the water temperature to develop the El Niño- to develop the El
Niño-Southern
Southern OscillationOscillation
(ENSO) (ENSO)
[40,41].[40,41].
TheseThese
currentscurrents
provideprovide
the CMPthe CMP with species
with species from
from different
different biogeographic
biogeographic provinces
provinces [38]. [38]. Hurricanes,
Hurricanes, tropical
tropical storms,
storms, and upwellings
and upwellings also
also significantly
significantly impact
impact the coral
the coral colony
colony structure
structure and and associated
associated faunafauna
[18].[18].

Figure 1. Study area in the

the CMP.
CMP. Site codes: (a)
(a) CH,
CH, Chamela;
Chamela; (b)
(b)CT,
CT, Cuastecomate-Punta
Cuastecomate-Punta Melaque,
Melaque,
Jalisco; (c) CA, Carrizales; and (d) PB, Punto B, Colima.
Jalisco; (c) CA, Carrizales; and (d) PB, Punto B, Colima.

Some of the general characteristics of the sampled sites are as follows: (1) Chamela
(CH) is formed by different small islands and islets; its coral ecosystems are patchy and
isolated, and the benthos has a high coverage of rubble, sand, and dead coral. This site
Diversity 2022, 14, 72 4 of 13

is important for fishing and local tourism. (2) Cuastecomate-Punta Melaque (CT) has a
discontinuously distributed high coral cover, characterized by small reef patches with
fleshy macroalgae stands, sand, and rocks. (3) Carrizales (CA) is located in Ceniceros Bay;
it is a short beach defined by two small and fringing coral reefs on each side of the shore
with ~100% live coral cover. (4) Punto B (PB) is located in Santiago Bay near the Julualpan
Lagoon’s mouth and is considered a highly touristic area. Its coral community has scarce,
isolated coral colonies but great coverage of sponges, calcareous algae, and sandy and
rocky substrates.
Three samples of live Pocillopora corals were collected in each coral ecosystem using
randomly placed 0.25 m2 quadrants. Each sample position was marked using a global
positioning system (GPS). A total of 48 samples were collected during September 2017,
January and September 2018, and January 2019. All samplings were obtained by scuba
diving at a 10 m depth. Each coral sample was covered with a plastic bag to avoid losing
organisms and detached using a hammer and chisel. Subsequently, the coral was carefully
fragmented to collect all the organisms between and within the Pocillopora branches. All live
decapods and stomatopods were fixed with 70% ethylic alcohol. Samples were identified
to the most precise taxonomic level possible in the Molecular Ecology, Microbiology, and
Taxonomy Laboratory (LEMITAX), Universidad de Guadalajara. The specialized litera-
ture for identification included Rathbun [42], Haig [43], Abele and Kim [44], Castro [45],
Anker et al. [46], Hendrickx et al. [47], Ayón-Parente [48], García-Madrigal and Andréu-
Sánchez [49], Hermoso-Salazar [50], Salgado-Barragán and Hendrickx [51], and Hiller and
Lessios [52]. A presence/absence matrix was constructed to perform the ecological analysis.

2.2. Data Analysis

The spatial and temporal variation of the taxonomic diversity was evaluated with a
three-way experimental design with crossed factors expressed as:

Y = µ + Yei + Se j + Sik + Yei xSe j + Yei xSik + Se j xSik + Yei xSe j xSik + εijk (1)

where Y is the variable under analysis (taxonomic diversity), and µ is the mean of the
analyzed variable. The year factor (Yei ) had two levels (years), and each year was composed
of two seasons (dry and wet seasons), so the first year included September 2017 and January
2018, and the second included September 2018 and January 2019. The season factor (Sej )
had two levels: wet (September 2017 and 2018) and dry (January 2018 and 2019). The
site factor (Sik ) had four levels corresponding to the studied coral ecosystems. Finally, εijk
represented the accumulated error. All factors were considered as fixed effects (model
type I).
The sampling effort was evaluated using sample-based rarefactions at three levels
(i.e., site, season, and year) with the observed species richness and the expected richness
estimated using non-parametric estimators Chao 1, Chao 2, Jackknife 1, Jackknife 2, ICE, and
ACE. These estimators were based on rare species; they estimated the number of potential
species considering the incidence and abundance data recorded in the samplings [53]. The
total observed richness (SObs ) was calculated for each ecosystem with the Mao Tao function.
Then, the coral ecosystems were compared in pairs with individual-based rarefactions and
95% confidence intervals. All rarefaction curves were built with 10,000 randomizations
without replacement. Species rarity was also calculated (singletons, doubletons, unique,
and duplicate species), and the species were identified. These analyses were performed in
the software EstimateS 9.1 [54]. The absolute density of each species (represented as the
number of individuals per m2 ) and their absolute frequency were also estimated.
The taxonomic diversity analysis considered each site’s taxonomic differences and
singularities regarding the seasonal variation and the years analyzed. Thus, the average tax-
onomic distinctness (∆+ ) analysis was performed to evaluate the species’ distribution and in-
Diversity 2022, 14, 72 5 of 13

cidence as well as their taxonomic relations [28]. This analysis also measured the taxonomic
distance between two species and its variation (Λ+ ), according to the following equations:
" #
∆+ = ∑ ∑ ωij /[S(S − 1)/2] (2)
i< j
" #
+
Λ = ∑ ∑ ωij−v 2 / [S(S − 1) / ] (3)
i6= j

where S represents the number of species, and ωij denotes the assigned weight of each
supraspecific taxonomic level. An eight-level taxonomic aggregation matrix was built,
including species, genus, family, subfamily, suborder, order, subclass, and class. According
to Warwick and Clarke [55], the taxa were weighted as follows: ω = 1, species within the
same genus; ω = 2, species within the same family but different genus; ω = 3, species within
the same subfamily but in a different family; and so on. The ∆+ and Λ+ were estimated for
each site, season, and year. The models were created with a 95% confidence interval, and
the statistical significance was tested with 10,000 permutations.
The ∆+ analysis was followed by a taxonomic dissimilarity analysis (Γ+ ), which is
described as:  
S S
∑i=1 1 min j ωij + ∑ j=2 1 mini ωij
 
Γ+= (4)
(S1 + S2 )
where Γ+ denotes the gamma+ taxonomic dissimilarity, S1 represents the number of species
in the first sample, S2 is the number of species in the second sample, and ωij denotes the
path length between species i and j.
A non-parametric multidimensional scaling (nMDS) and a cluster analysis were per-
formed using the taxonomic dissimilarity (Γ+ ) matrix to explore the crustacean taxonomic
differentiation patterns across the spatio–temporal experimental design (site, season, and
year). The cluster analysis was built with the average group linking method and similarity
profile analysis (SIMPROF) to assess group formation using 10,000 permutations. Therefore,
nMDS ordination was coupled with the cluster analysis outputs. All analyses (i.e., ∆+ , Λ+ ,
Γ+ , nMDS, and cluster analysis) were performed in PRIMER 7.0.21 and PERMANOVA
+1 [56].

3. Results
A total of 12,647 specimens were collected, representing 21 families, 43 genera, and
88 species (Supplementary Material, Table S1). For each quadrant, the number of species
collected ranged from 13 to 38, and the number of individuals ranged from 36 to 705.
The most diverse families were Alpheidae (21 species) and Porcellanidae (20 species). Ten
families (47%) were represented by a single species (Supplementary Material, Table S1). The
sample-based rarefaction showed that the sampling effort had an adequate representativity
(79.6%) of the species richness expected by chance (Supplementary Material, Figure S1).
The sampling effort ranged between 77.9% and 91.6% of representativity for all sites. The
seasons showed 84.6% of representativity during the dry season and 85.7% in the wet
season (Supplementary Material, Table S2). The representativity for year one was 79.5%,
and for year two it was 88% (Supplementary Material, Table S2).
The most abundant species were Trapezia corallina, with 1720 individuals (13.6% of
total abundance); Trapezia bidentata, with 1489; Pachychelles biocellatus, with 1028; Petrolisthes
haigae, with 955; Alpheus lottini, with 820; Petrolisthes hians, with 619; and Trapezia formosa,
with 579. Together, these species represented more than half of the collected specimens
(Supplementary Material, Table S1). Of the total, 38 species (43% of the total) were repre-
sented by less than 10 individuals. Of these, 17 species had only 1 individual (singletons),
and 4 had only 2 individuals (doubletons). Consequently, the contribution of singletons and
Diversity 2022, 14, 72 6 of 13

doubletons to the species richness was 23.8%. In addition, 14 species were collected in only
1 sample (uniques) and 7 in 2 samples (duplicates) (Supplementary Material, Table S1).
Individual-based rarefactions in pairwise comparisons showed that the species rich-
ness between sites was similar because their confidence intervals (95%) overlapped
(Supplementary Material, Figure S2). An exception was Chamela and Carrizales, which had
the highest and lowest number of species, respectively (Supplementary Material, Figure
S2). The highest total species richness and abundance recorded over the sampling period
were as follows: for Chamela, 69 species and 2371 individuals; for Cuastecomate-Punta
Melaque, 64 species and 3266 individuals; for Carrizales, 58 species and 2752 individuals;
and for Punto B, 68 species and 4258 individuals (Supplementary Material, Table S1). The
total species richness was similar between years and between seasons (Supplementary Ma-
terial, Figure S3). Year one showed 78 species and 5957 individuals, and year two showed
76 species and 6690 individuals. The wet season showed 79 species and 5276 individuals,
and the dry season showed 73 species and 7361 individuals (Supplementary Material,
Table S1). Synalpheus arostris and Neogonodactylus pumilus were recorded for the first time
in the Mexican Pacific and showed a geographic extension of 3950 km to the north. Six
other species were recorded for the first time in the Central Mexican Pacific: Lophopanopeus
frontalis, Daldorfia trigona, Pilumnus gonzalensis, Pilumnus reticulatus, Tumidotheres margarita,
and Megalobrachium tuberculipes. In Chamela, 50% of the species were collected for the first
time, in Cuastecomate-Punta Melaque, 76%, and in Carrizales and Punto B, 63%.
The average taxonomic distinctness (∆+ ) analysis at the site level showed that the
∆ values for all the sites fell inside the probability funnel or within the 95% confidence
+

intervals (p > 0.05). Chamela had the lowest ∆+ values despite having the greatest number
of species (Figure 2). Punto B had the highest ∆+ values above the global ∆+ of the model.
However, the Λ+ values for all sites fell within the probability funnel, indicating that the
sampled sites were representative of the taxonomic diversity of the area. The seasons had
different ∆+ values because the wet season fell within the probability funnel, but the dry
season was outside the funnel (p < 0.05). The Λ+ values for the dry season were outside the
funnel, so the taxonomic representativity during the dry season was lower than expected
by chance (Figure 2). The ∆+ and Λ+ values between years were similar and fell inside the
probability funnel (Figure 2).
The nMDS ordination showed that the taxonomic dissimilarity (Γ+ ) differed among
the sites (Figure 3). The cluster analysis based on the SIMPROF procedure confirmed a
group constituted by the southern sites (i.e., Carrizales and Punto B) and two separate
entities (i.e., Chamela and Cuastecomate-Punta Melaque). This was also observed in the
nMDS ordination. Carrizales and Punto B shared several species (e.g., Pseudosquillisma
adiastalta, Pomagnathus corallinus, and Synalpheus arostris) and genera (e.g., Trapezia, Liomera,
and Pomaghnathus), and they had almost the same families, except for the Pinnotheridae,
which was only present in Punto B (and Cuastecomate-Punta Melaque). Conversely,
Cuastecomate-Punta Melaque had a different crustacean fauna compared to the other sites
and showed a mixture of taxa shared with Chamela and Punto B. Cuastecomate-Punta
Melaque presented 34 genera and 17 families; these families were the same as Punto B,
except for Panopeidae, which was found exclusively in this site, and Pseudosquillidae,
which was absent. Chamela is the northernmost site and the most distant from the others.
It was different because it had one superfamily (Parthenopoidea) not found elsewhere and
two absent superfamilies (Eriphioidea and Pinnotheroidea). In Chamela, two families that
were not found in other sites were collected (Parthenopidae and Lysmatidae), and four
families (Panopeidae, Oziidae, Pseudosquillidae, and Pinnotheridae) were absent.
Diversity 2022, 14,
Diversity 14, x72FOR PEER REVIEW 7 7ofof 13
13
Diversity 2022, 14, x FOR PEER REVIEW 7 of 13

Figure 2. Average taxonomic distinctness analysis (Δ++) by site (a), season (c), and year (e); and its
Figure Average
Figure2.2.ΛAverage taxonomic distinctness
+ for (b) taxonomic distinctnessanalysis (∆
(Δ+)) by site (a),
(a),season (c), and
andyear
year(e);
(e);and
andits
variation site, (d) season, and (f)analysis
year. Codes: by
CH,siteChamela;
season (c),Cuastecomate-Punta
CT, its
variation
variation ΛΛ
++ for (b) site, (d) season, and (f) year. Codes: CH, Chamela; CT, Cuastecomate-Punta
for (b) site, (d) season,
Melaque; CA, Carrizales; PB, Punto B. and (f) year. Codes: CH, Chamela; CT, Cuastecomate-Punta
Melaque;
Melaque;CA,CA,Carrizales;
Carrizales;PB,PB,Punto
PuntoB.B.

Figure 3. Non-metric multidimensional scaling (nMDS) ordination shows the taxonomic dissimilar-
Figure
ity of the 3. Non-metric multidimensional scaling (nMDS) corals
ordination shows the taxonomic in dissimilar-
Figure 3. crustacean
Non-metricdiversity associatedscaling
multidimensional with Pocillopora
(nMDS) ordinationamong
showsthethe
studied sites dissimilarity
taxonomic the CMP.
ity of the
Groups crustacean
were separateddiversity
as a associated
function of with
the Pocillopora
cluster corals
analysis with among
an the studied
average group sites in the
linking CMP.
method
of the crustacean diversity associated with Pocillopora corals among the studied sites in the CMP.
Groups
and were separated
the similarity profileas analysis
a function of the cluster
(SIMPROF). analysis
Codes: CH,with an average
Chamela; CT, group linking method
Cuastecomate-Punta
Groups
and the were separated
similarity as a function
profile of the cluster analysis with an average group linking method and
Melaque; CA, Carrizales; PB,analysis
Punto B.(SIMPROF). Codes: CH, Chamela; CT, Cuastecomate-Punta
the similarity
Melaque; CA,profile analysis
Carrizales; PB,(SIMPROF).
Punto B. Codes: CH, Chamela; CT, Cuastecomate-Punta Melaque;
CA, Carrizales; PB, Punto B.
4. Discussion
4. Discussion
This study recorded most of the Pocillopora obligate symbiotic crustacean species re-
portedThis study recorded
by previous studies,most of the Trapezia
including Pocillopora obligate
bidentata, T.symbiotic crustacean
corallina, T. digitalis, T.species re-
formosa,
ported by previous studies, including Trapezia bidentata, T. corallina, T. digitalis, T. formosa,
Diversity 2022, 14, 72 8 of 13

4. Discussion
This study recorded most of the Pocillopora obligate symbiotic crustacean species
reported by previous studies, including Trapezia bidentata, T. corallina, T. digitalis, T. formosa,
Alpheus lottini, Hapalocarcinus marsupialis, and some species of Synalpheus. However, we did
not find some species known to be associated with Pocillopora, such as Fennera chacei, Alpheus
sulcatus, Palaemonella holmesi, Stenorhynchus debilis, Thor algicola, and Petrolisthes galathinus,
which had been previously reported in the study area [24,25]. Nonetheless, we obtained
two new records for the Mexican Pacific and six new records for the CMP (Supplementary
Material, Table S1), increasing the known information regarding regional crustaceans.
Several species collected during this study, i.e., Tumidotheres margarita, Typton sp.,
and Pontonia sp., have been reported as endosymbionts of sponges, ascidians, or bivalves.
These hosts are frequently associated with pocilloporid corals, and these decapods might
be recognized as having a secondary association with pocilloporid corals. Tumidotheres
margarita is an endosymbiont of the bivalves Barbatia reevaena, Limaria pacifica, and Pinc-
tada mazatlanica [57], which are known as Pocillopora-associated mollusks in the Mexican
Pacific [58]. Typton tortugae and T. serratus have been recorded as being associated with
sponges living on corals [59]. In this study, some sponges were found to be associated with
corals, and a similar association could exist in the cases of T. hephaestus and T. granulosus.
Shrimps of the genus Pontonia are reported as obligate symbionts of the bivalves Pinna
spp. and P. mazatlanica [60]. We assumed that the Pontonia specimens collected during this
study were dislodged from their host during the collecting process or after the samples
were preserved.
Our study increased the inventory of crustaceans associated with Pocillopora coral in
the Mexican Pacific from 59 [20–24] to 88 species. Comparatively, in Huatulco, Oaxaca, a
method similar to the one used here (0.25 m2 quadrants) recorded 47 species of brachyuran
crabs in pocilloporid corals [21]. In La Paz and Loreto Bay, Baja California Sur, 44 species of
decapods were recorded [22]. Furthermore, a study covering almost the entire Mexican
Pacific, from the Gulf of California to Oaxaca, recorded 36 crustacean species associated
with pocilloporids [24]. The difference between the number of species reported herein and
by Hernández et al. [24] may be a consequence of the visual census they performed. With
this method, some close species are easily confused (e.g., Synalpheus spp., Trapezia spp., and
Alpheus spp.) or overlooked (e.g., Hapalocarcinus marsupialis). The expected species richness
estimated by the sample-based rarefaction was 20% higher than the observed richness due
to the large number of rare species collected. Expected species richness is a good indicator
of the potential species expected in the area. The sample-based rarefaction confirmed that
the sampling effort was sufficient to elucidate the actual number of crustacean species
associated with the Pocillopora coral in the CMP.
Decapod crustacean fauna associated with Pocillopora coral has been studied in many
tropical and subtropical regions of the world’s oceans. The species diversity recorded in this
study is superior to the 36 species associated with Pocillopora off the Arabian coast in the
Red Sea [61]. However, it is lower than the diversity reported from Oahu (Hawaii), where
127 species were found associated with Pocillopora damicornis [62], and then the 91 species
reported more recently in 751 colonies of P. meandrina, also in Oahu [3]. For the northern
Great Barrier Reef, Australia, 102 species were found in 50 colonies of P. damicornis [63]. It
is important to mention that the obligate symbiotic composition observed in our study is
similar to what has been reported for the Red Sea and the Great Barrier Reef, i.e., all three
studies share the same brachyuran crabs (Trapezia bidentata, T. digitalis, and Domecia hispida)
and caridean shrimps (Alpheus lottini, Synalpheus charon, and Harpiliopsis depressa).
A previous study indicated that the number of species present in coral ecosystems
depends on the size of the coral colony [64]. The authors reported species richness ranging
from 3 to 22 per colony (1500 cm3 size) in the Gulf of Panama; in Costa Rica, 20 cm diameter
colonies had 18 species [65]. Despite using quadrants of the same size, this study collected
13–18 species and 36–711 individuals per 0.25 m2 of coral sample. These differences
in abundance and richness are substantial and cannot only be attributed to colony size.
Diversity 2022, 14, 72 9 of 13

To predict the species richness or abundance in colonies with stable conditions, some
authors considered coral complexity (e.g., inter-branch space, penetration depth, and size
of living space) [9], but in some cases, this factor was unable to explain the changes between
different colonies [63]. For example, species such as the symbiotic Trapezia are not limited
by coral complexity; they only need a healthy coral fragment for their survival [66]. Other
characteristics, such as the percentage of live tissue and habitat degradation, could also
influence the richness and abundance shifting. The species richness and abundance increase
when the proportion of live coral tissue cover decreases [7,63]; this might happen because
coral loss allows other species to move to new colonies. Moreover, coral mortality increases
the abundance in single colonies [15], which may occur for two reasons: (1) the death of
symbionts allows for other opportunistic species to move to more stable colonies, or (2) coral
loss induces migrations of individuals looking for new space to live [7,9]. This situation
could be happening in Punto B, where the coral colonies are isolated, fewer colonies are
available, and the ecosystem is subject to anthropogenic pressure [18]. Symbiont loss does
not seem to be a problem in Punto B because of the abundant obligate symbionts found in
all samples.
The average taxonomic distinctness (∆+ ) varied between sites and seasons. The ∆+
values fell inside the 95% probability funnel, meaning they were a good representation
of the taxonomic diversity of decapods and stomatopods associated with pocilloporid
corals. However, Chamela had a lower ∆+ value despite having the greatest species
richness among the four sites. This contrast occurred because Chamela featured the fewest
supraspecific taxonomic hierarchies since many species belonged to the same families, i.e.,
Alpheidae (17 species) and Porcellanidae (18 species). In contrast, Punto B had the highest
∆+ value above the global ∆+ of the model and sustained almost the same species richness
as Chamela. Punto B shared the taxonomic hierarchies with other sites and did not present
any exclusive hierarchy.
Regarding the temporal variation of the taxonomic diversity, the ∆+ values fell outside
the probability funnel in the dry season, meaning a relatively low taxonomic diversity
change during this season; six genera (Areopaguristes, Aniculus, Daldorfia, Bottoxanthodes,
Pontonia, and Pseudosquillisma), two families (Parthenopidae and Pseudosquillidae), and
one superfamily (Parthenopoidea) were not recorded in this season. In contrast, the taxo-
nomic diversity was better represented during the wet season, when the Parthenopoidea
superfamily was present, portrayed by Daldorfia trigona, a species not collected in the dry
season. Moreover, 15 species and 6 genera were exclusively collected during the wet season
(Supplementary Material, Table S1). Years one and two had similar species richness and
taxonomic structure. Likewise, both ∆+ values fell into the probability funnel close to the
global ∆+ level, demonstrating that the studied years adequately represented the taxonomic
diversity estimated by the global ∆+ model.
The nMDS ordination coupled with cluster analysis showed that Chamela had the
highest taxonomic dissimilarities (Γ+ ) among the studied sites. Chamela—the northernmost
site—was the most different with the highest taxonomic dissimilarity, the lowest ∆+ , and
the highest species richness. The Chamela samples contained one superfamily, two families,
and four genera exclusive to this site, but several superfamilies, families, and genera present
in the other sites were absent. It has been suggested that a low taxonomic distinctness can
indicate a loss in the taxonomic diversity due to anthropogenic stress [30]. However, in this
study, Punto B was the most anthropogenically affected site and displayed the highest ∆+
values. Despite moderate disturbances, symbiotic species tend to stay in their host for a
long time [9,63]. Nevertheless, some symbionts (e.g., Trapezia) can migrate to other coral
colonies in search of more suitable habitat [66,67]. Limited habitat availability makes them
pile up in the colony, increasing species richness and abundance. This phenomenon could
affect the ∆+ values in Punto B, increasing the values higher than the global ∆+ of the model.
The low levels of taxonomic diversity in Chamela might be attributed to other variables,
including the spatial process [68], benthic heterogeneity, habitat availability [69], or habitat
Diversity 2022, 14, 72 10 of 13

type [70]. In addition, it is important to remember that the variety of microhabitats is one
of the main factors driving the diversity and abundance of coral-associated crustaceans [7].
In conclusion, the sampling effort in this study allowed for obtaining more than 70%
of the expected species, indicating a good taxonomic representativity. The species richness
and the taxonomic distinctness were within the expected values, despite being lower
during the dry season. Most of the expected coral-obligated symbionts were collected,
except for Fennera chacei, a small species frequently living in the coral base, which probably
escaped during the collecting process. In contrast with the initial hypothesis, the sites with
the most discontinuous coral cover and the largest human intervention did not have the
lowest taxonomic distinctness (Punto B). However, as expected, the greatest abundance
was observed in Punto B; this can be explained by the low coral availability, environmental
variables, or anthropogenic stress. The present study should be complemented with α, γ,
and β diversity analysis to assess the spatio–temporal differences in this particular species
assemblage. It is also important to consider the influence of environmental variables,
reef structural complexity, and human impact on the richness and abundance of these
crustacean species, particularly in the obligate coral-symbiotic species. This study helped us
to understand the crustacean assemblage associated with corals in the CMP and the spatio–
temporal variations in their taxonomic diversity. Furthermore, it increased the taxonomic
inventory of the coral-associated species in the studied region and the Mexican Pacific.

Supplementary Materials: The following supporting information can be downloaded at: https:
//www.mdpi.com/article/10.3390/d14020072/s1, Table S1: Crustacean species list organized by
families, Table S2: Sample-based rarefaction results, Figure S1: Sample-based rarefaction curves for
the study area, Figure S2: Individual-based rarefaction curves between sites, Figure S3: Individual-
based rarefaction curves between climatic seasons and sampling years.
Author Contributions: Conceptualization and methodology, A.A.-D., F.A.R.-Z. and M.A.-P.; formal
analysis and investigation, A.A.-D. and F.A.R.-Z.; resources, F.A.R.-Z.; data curation, A.A.-D. and
M.A.-P.; writing–original draft preparation, A.A.-D. and F.A.R.-Z.; writing—review and editing,
F.A.R.-Z., M.A.-P., E.R.-J., M.d.C.E.-G., M.E.H. and O.V.-P.; project administration and funding
acquisition, F.A.R.-Z. All authors have read and agreed to the published version of the manuscript.
Funding: A.A.-D. was funded by a doctoral fellowship (371662) from the Consejo Nacional de
Ciencia y Tecnología (CONACYT). The scientific research project 257987 was funded by CB2015
from CONACYT.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: The authors confirm that the data supporting the findings of this study
are available within the article and its Supplementary Material. Likewise, the data are available upon
request from the corresponding author.
Acknowledgments: The authors would like to thank Sharix Rubio-Bueno and Karen A. Madrigal-
González for their help in the fieldwork. We thank Enrique Godínez-Domínguez (CUCSUR-U. de G.)
for his support with boats during the fieldwork.
Conflicts of Interest: The authors declare no conflict of interest.

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