Journal of
Marine Science
and Engineering
Article
Novel Comprehensive Molecular and Ecological Study
Introducing Coastal Mud Shrimp (Solenocera Crassicornis)
Recorded at the Gulf of Suez, Egypt
Eman M. Abbas 1 , Fawzia S. Ali 1 , Mohammed G. Desouky 1 , Mohamed Ashour 1 , Ahmed El-Shafei 2,3, * ,
Mahmoud M. Maaty 1 and Zaki Z. Sharawy 1, *
1
2
3
*
Citation: Abbas, E.M.; Ali, F.S.;
Desouky, M.G.; Ashour, M.; El-Shafei,
A.; Maaty, M.M.; Sharawy, Z.Z. Novel
Comprehensive Molecular and
Ecological Study Introducing Coastal
Mud Shrimp (Solenocera Crassicornis)
Recorded at the Gulf of Suez, Egypt.
J. Mar. Sci. Eng. 2021, 9, 9. https://
dx.doi.org/10.3390/jmse9010009
National Institute of Oceanography and Fisheries (NIOF), Cairo 11516, Egypt;
emanabbas03@yahoo.com (E.M.A.); dr_allam84@hotmail.com (F.S.A.); dr.mgaberniof@gmail.com (M.G.D.);
microalgae_egypt@yahoo.com (M.A.); mahmoudmaaty1@yahoo.com (M.M.M.)
PSIPW Chair, Prince Sultan Institute for Environmental, Water and Desert Research, King Saud University,
Riyadh 11451, Saudi Arabia
Department of Agricultural Engineering, College of Food and Agricultural Sciences, King Saud University,
Riyadh 11451, Saudi Arabia
Correspondence: aelshafei1bn.c@ksu.edu.sa (A.E.-S.); zaki_sharawy@yahoo.com (Z.Z.S.);
Tel.: +966-11-4678504 (A.E.-S.); +20-10-0184-5218 (Z.Z.S.)
Abstract: Solenocera crassicornis is a commercially important shrimp of the Solenoceridae family.
The current study investigated the morphology, molecular identification, phylogenetic relationships,
and population dynamics of S. crassicornis in Egypt. Samples were collected monthly (total, 1722;
male = 40.19%, wet weight, 0.89–10.77 g; female = 59.81%, wet weight, 1.55–19.24 g) from Al-Attaka
commercial catch in the Gulf of Suez in the Red Sea. Two barcode markers, 18S rRNA and cytochrome
c oxidase subunit I (COI), were used for molecular identification. COI partial sequences were used to
construct the phylogenetic relationships among different species of genus Solenocera and to infer the
origin of the studied Solenocera crassicornis. The applied molecular markers successfully identified
the studied species to the species level. The genetic distances among S. crassicornis sequences
from different countries revealed the Indo-West Pacific origin of S. crassicornis. The relationship
between total length (TL) and total weight (TW) was TW = 0.035TL2.275 and r2 = 0.805 for males
and TW = 0.007TL3.036 and r2 = 0.883 for females, indicating that females were heavier than males.
Despite its social and economic relevance in the area, information on the hatching, larval rearing,
and farming of S. crassicornis is scarce and requires future studies under Egyptian conditions.
Keywords: Penaeoidea; Solenoceridae; shrimp; Suez Gulf; Red Sea; DNA barcoding; 18S rRNA; COI
Received: 19 October 2020
Accepted: 21 December 2020
Published: 23 December 2020
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1. Introduction
Shrimp is presently the foremost important globally traded fishery product in terms of
value. In numerous tropical developing countries, it is the most profitable fishery trade [1,2].
Shrimp fisheries are not only valuable food resources, but also major economic resources
in Egypt and other developing countries. Worldwide, the commercial shrimp species is
a one of the superfamily Penaeoidea, which is classified into five Penaeidean families:
Penaeidae, Solenoceridae, Sicynoiidae, Aristeidae, and Sergestidae [3,4]. The Solenoceridae family has the economic importance for the commercial catch. All individuals are
marine species, despite some juvenile Penaeidae species inhabiting brackish water and
being occasionally found in almost fresh water. A significant species of the Solenoceridae
family is Solenocera crassicornis, a member of the genus Solenocera Lucas, 1849, which
comprises 38 species [5]. The common name of S. crassicornis (H. Milne Edwards, 1837),
also identified as S. indicus (Nataraj, 1945), is the costal mud shrimp. It is an important commercial shrimp of Indian waters [6] and the main aquatic product for export in China [7].
This species is distributed along the West and East coasts of India; the coast of Malaysia,
J. Mar. Sci. Eng. 2021, 9, 9. https://dx.doi.org/10.3390/jmse9010009
https://www.mdpi.com/journal/jmse
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Mergui Archipelago, and Singapore, North Borneo, and Hong Kong; and the Indo-West
Pacific (from the Malay Archipelago to India and Pakistan), Japan, and China. Its habitat
depth is 40 m, preferring the mud and sandy bottoms [5,8]. Several studies have been
conducted on S. crassicornis dealing with some aspects of its fisheries and biology, such as
age, growth, food, and feeding, breeding, and migration [8–10]; sustainable yield and
population dynamic for S. crassicornis species in the East China Sea [11] and in the waters
of Versova, Mombai [10]. Furthermore, Rajkumar et al. [12] investigated the morphological
and molecular identification of S. crassicornis inhabiting the Coromandel Coast of Tamil
Nadu, India. The developing countries, including Egypt, are the primary producers of
shrimp, due to extensive shrimp activities and overfishing. The demand for shrimp production and subsequent overexploitation can negatively impact shrimp stocks in water
bodies in these countries. Therefore, regular assessment and management of fishery stock,
particularly shrimp species of economic interest, is necessary. It is necessary to understand
genetic structures to start breeding programs domestication and selection for aquaculture.
Approximately 610 tons of shrimp are produced annually, and Penaeidae shrimp contribute
to 8% of the total trawl landings [13]. The unparalleled geographic location of the Red Sea
makes it highly sensitive to biodiversities, communities, and distributions [14]. Since the
operation of the Suez Canal in 1872, the shrimp fauna in the Mediterranean has been
enriched due to the changes and disturbances caused by the migration of some fish species
and the partial change in the ecosystem. S. crassicornis was first recorded in the Mediterranean shelf of Egypt in 1981 by Abdel-Razek et al. [15], identified as S. indicus (Nataraj,
1945). However, there are no published data recording S. crassicornis in the Red Sea in
Egypt. Additionally, there are no data available regarding the identification, occurrence,
distribution, stock assessment, hatching, larval rearing, and farming of S. crassicornis in
Egypt, despite it being an economically important species. The identification and characterization of aquatic organisms are considered a basic step for monitoring biodiversity and
conserving such species [16–18]. In the case of crustaceans, morphology-based identification is an extremely basic science. Crustaceans undergo various larval stages with alterable
and changeable shapes and background coloration due to chromatophores [19]. Therefore,
this identification tool can be ineffective and misleading [20,21]. In such cases, the application of molecular-based identification tools, including DNA barcoding, can resolve
these problems. DNA barcoding applies universal primers to amplify a targeted genomic
region. The efficiency of this method depends on the diverse nature of the targeted region
among species [22,23]. In crustaceans, targeting the region of the cytochrome oxidase
subunit I (COI) mitochondrial gene using the primer pairs described by Folmer et al. [24]
was the most efficient. DNA barcoding is a perfect tool for identification and studying
species diversity within an ecosystem. Several studies have used the COI region to identify
various crustaceans [12,25–27]. Some of the shrimp species of economic interest in Egypt
have been precisely characterized using morphological and genetic analyses [28–31]. Here,
we conducted a comprehensive study of S. crassicornis collected from the Gulf of Suez in
Egypt, including molecular identification, growth parameter assessments, and estimations
of population dynamic parameters. We integrated two barcode regions, namely, 18S rRNA
nuclear barcode and COI mitochondrial barcode, with morphological identification data
to precisely characterize the studied species. Additionally, monthly variations in length
frequency were used to determine S. crassicornis growth parameters and to estimate other
population dynamic parameters.
2. Materials and Methods
2.1. Sample Collection and Morphology
Random S. crassicornis samples were collected monthly for 12 months starting from
June 2019 by trawl nets from Al-Attaka commercial catch in the Gulf of Suez, the Red Sea.
The collected shrimp samples were identified as S. crassicornis (H. Milne Edwards, 1837)
based on morphological characteristics, as described in the literature [8,9,15]. The length
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frequency for 1722 S. crassicornis individuals, comprising 692 males (2.3–11.0 cm) and
1030 females (3.9–13.3 cm), was estimated.
2.2. Growth Parameters and Population Dynamics
2.2.1. Population structure
To prevent prejudice due to various measuring tools for researchers and for a more
accurate methodology, we estimated singular lengths to the closest 0.1 cm by using a
MATLAB routine (MathWorks Inc., Natick, MA, USA) to singular shrimp snapshots taken
with a MEGA 0.I.S USB camera (Leica, Wetzlar, Germany) outfitted with a DC VARIOELMARIT 1:2.8-49/6.3-25.2 A SPH lens (Leica). The snapshots created a record that could
be easily stored and used for additional estimations and confirmatory checks if necessary.
Manual fixation of singular shrimp with a complete rostrum on millimeter paper was
done (to stay away from the natural warp of the shrimp body). The estimations were
characterized as: (a) Total length (TL): The space from the tip of the rostrum to the end of
the telson, cm; (b) carapace length (CL): The space from the posterior margin of the orbit to
the posterior edge of the carapace, mm; and (c) total weight (TW): Weighed in grams by
using an electronic digital balance (±0.01 g; Sartorius, Göttingen, Germany).
2.2.2. Growth Parameters, Mortality, and Exploitation Rates
We applied the ELEFAN1 program to length frequency inputs to evaluate asymptotic
length (L∞ ) and to estimate the growth coefficient (K) for each sex separated utilizing von
Bertalanffy growth function (VBGF) development work [32] as follows:
Lt = L∞ [1 − e− K(t − t0) ]
(1)
where: Lt is TL at age t, L∞ is the asymptotic TL, K is the curvature value, and t0 is the
theoretical age when TL is zero.
To compare the growth performance of both males and females [33] as follows:
ϕ = log10 k + 2 log10 L∞
(2)
where: K and L∞ are Bertalanffy equation constant.
The instantaneous rate of natural mortality (M) was also estimated [33] as follows:
log10(M) = −0.0066 − 0.279 log10(L∞) + 0.6543 log10(K) + 0.4634 log10(T)
(3)
where: T is the temperature of water.
Total mortality instantaneous rate (Z) was evaluated by applying the FiSAT II program,
using a length-converted fishing curve [34] according to the equation ln (N/∆t) = a + bt,
where N is the number of crabs in a particular size class, ∆t is the time required to attain that
class (years), t is the relative age (years), a is the intercept, and b is the regression coefficient
(b = Z). Hence, fishing mortality (F) for both sexes were estimated as F = Z − M. Then,
the exploitation rates (E) were estimated as the following: E = F/Z [35]. As indicated by
Pauly [36], the ascending left arm of the CL-converted catch curve was utilized to examine
the probability of capture of every length class. The modified Beverton and Holt [37]
relative yield per recruit (Y/R) model by Pauly and Soriano [38] was utilized and then
incorporated into FiSAT II programming to gauge the degrees of exploitation that would
give ideal yields. Investigations of Emax (the exploitation rate giving highest relative yield
per recruit), E0.1 (exploitation rate at which the marginal raise in Y/R is 10% of its value at
E = 0), and E0.5 (the identical exploitation to half of the unexploited relative biomass per
recruit, B/R) were evaluated.
To assess the allometry, the TW-TL relationship, the equation of Le-Cren’s [39] was
used as follows:
TW = a TLb
(4)
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where: TL (cm): Is the carapace length, TW (g): Is the total body wet weight, while a is
intercept parameter and b is allometric parameter.
2.3. Molecular Analysis
2.3.1. DNA Extraction and Polymerase Chain Reaction Amplification
Genomic DNA was extracted from the axial muscle of the collected samples, according
to Sambrook et al. [40]. Briefly, 100–200 mg of muscle tissue sample was ground in TES
buffer (10 mM Tris-HCl, 25 mM EDTA, 140 mM NaCl, and pH 7.8) containing 0.5 mg mL−1
proteinase K and 1% SDS. The homogenates were incubated for 2 h at 56 ◦ C. Total genomic
DNA was extracted using a conventional phenol-chloroform procedure and precipitated
with absolute ethanol. The DNA pellets were eluted in TE buffer (100 mM Tris-HCl and
10 mM EDTA, pH 8). The concentrations of DNA of all samples were measured using
a Nanodrop spectrophotometer (Biodrop, Cambridge, England). Following DNA isolation, two barcode regions were amplified for species identification, namely, a 683-bp
fragment from the coding region of the mitochondrial gene (COI) and a 469-bp partial
fragment of the 18S rRNA nuclear gene. Polymerase Chain Reaction (PCR) was performed
on a GeneAmp PCR System 9700 Thermal Cycler (Applied Biosystems, Foster City, CA,
USA) utilizing the primer pairs LCO1490 (5′ -GGTCAACAAATCATAAAGATATTGG-3′ )
and HCO2198 (5′ -TAAACTTCAGGGTGACCAAAAAATCA-3′ ) [24], and Ebi18S-F (5′ CGCCTACAATGGCTATAACGGGTAAC-3′ ), and Ebi18S-R (5′ -GGTTAGAACTAGGGCG
GTATCTGATC-3′ ) [29] for COI and 18S rRNA amplification, respectively. The PCR reactions were conducted in 25 µL as a total volume containing 12.5 µL of 1x MyTaqTM HS Red
Mix (Bioline, London, UK), 30 ng of template DNA, and 0.4 µM of each primer. The PCR
program for amplification of the COI region was: Initial denaturation for 5 min at 94 ◦ C,
followed by 40 cycles of denaturation for 1 min at 94 ◦ C, annealing for 1 min at 45 ◦ C,
and extension for 1.30 min at 72 ◦ C, and a final extension for 7 min at 72 ◦ C. The cycling profile for 18S rRNA amplification was: Denaturation for 5 min at 95 ◦ C, followed by 35 cycles
of denaturation for 30 s at 95 ◦ C, annealing for 30 s at 48 ◦ C, and extension C for 2 min at
72◦ , and a final extension for 7 min at 74 ◦ C. The amplicons were electrophoresed at 120 V
on a 2.5% agarose gel and stained with ethidium bromide (25 µg mL−1 ) for visualization.
PCR products having single bands with the expected amplicon size were purified using
Isolate II PCR and Gel Kit (Bioline). The purified PCR products were sequenced using a
BigDye Terminator v3.1 Cycle Sequencing Kit [41] on an ABI 3730 Sequencer (both Applied
Biosystems). The sequencing reaction was applied as follows: 96 ◦ C for 2 min, followed by
25 cycles at 96 ◦ C for 10 s, at 50 ◦ C for 5 s, and at 60 ◦ C for 4 min.
2.3.2. Sequencing and Phylogenetic Analysis
The raw data of sequences for COI and 18S rRNA were treated using the free software
Chromas Lite v2.1 (Technelysium Pty Ltd., available from http://technelysium.com.au/)
and compared with the available sequences in the databases of GenBank (https://blast.
ncbi.nlm.nih.gov/Blast.cgi) using BLAST searches. The COI sequences were also compared
using the Barcode of Life Data System (BOLD) species identification portal (http://www.
barcodinglife.org). A Barcode Index Number (BIN) was assigned [42] for the COI sequences
of the study specimens, to confirm their concordance with sequence clusters available in
the BOLD database. The partial coding sequences of COI (683 bp) and 18S rRNA (469 bp)
of the investigated samples were deposited in the GenBank, EMBL, and DDBJ global
databases under the accession numbers LC477203–LC477205 and LC477340. Due to the
abundance of the available COI sequences on the GenBank Database compared to 18S
rRNA sequences, COI barcode region was used as a reference region for further molecular
analysis. COI sequences for Solenocera species were retrieved from the GenBank database
and aligned with the obtained sequences of the Egyptian S. crassicornis by CLUSTALW
software in MEGAX [43]. To locate S. crassicornis in relation to its relatives from the same
genus, the genetic distances among species of Solenocera were estimated based on Kimura
two-parameter distance model (K2P) using Group Mean Distance software impeded in
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MEGAX software package. MEGAX was used to apply the best fitting models to the COI
datasets of nucleotide sequences and disparity estimates using the general time-reversible
model [44]. Phylogenetic trees were constructed in MEGAX using the method of maximum
likelihood (ML), with 1000 bootstrap replicates.
3. Results
3.1. Morphology, Population Dynamics, and Growth Parameters
3.1.1. Morphology
The body and legs of S. crassicornis are reddish (Figure 1). The antennules were
banded with white and dark red. Except for some white areas, the uropods were dark
red. The rostrum is short and extends to approximately 2-3 of the eyes, with an upper
border with 7 to 8 teeth and a robustly convex lower border. The postrostral crest was
obviously raised, slightly interrupted by a little notch over the cervical groove, and the
height of the posterior section gradually decreases posteriorly. The orbital, antennal,
hepatic spines, and postorbital were unmistakable on the carapace, however, without
pterygostomian spines. The hepatic spine closes at the edge of a little round pit just behind
the pterygostomian angle. The orbital edge sharp, there was a little postorbital pit over
the postorbital spine, and the branchiocardiac carina and sulcus were well determined.
The antennular flagella were sensibly long and tube-like. The telson has a couple of
horizontal spines.
Figure 1. Solenocera crassicornis (H. Milne Edwards, 1837) caught from Al-Attaka, the Gulf of Suez,
Red Sea of Egypt.
All shrimp samples were pooled by sex to determine relationships between TL-TW and
TL-CL (n = 1722; male, 40.19%; female, 59.81%) were analyzed as shown in Figures 2 and 3.
The TW were ranged from 0.89 to 10.77 g and from 1.55 to 19.24 g for males and females,
respectively. While the TL ranged from 2.3 to 11.0 cm and from 3.9 to 13.3 cm for males and
females, respectively. Meanwhile, CL were ranged from 0.9 to 3.2 and from 1.3 to 4.5 cm for
males and females, respectively.
Figure 2. Length-weight relationship for males (a) and females (b) of S. crassicornis from the Gulf of Suez, Egypt.
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Figure 3. The relationship between total length and carapace length for males (a) and females (b) of
S. crassicornis from the Gulf of Suez, Egypt.
3.1.2. TL-TW Relationship
The length-weight relationship between (TL) and total weight (TW) was TW = 0.035TL2.275
and r2 = 0.805 for males and TW = 0.007TL3.036 and r2 = 0.883 for females. Overall,∞ TW re−
−
gression analyses showed positive allometric growth (b > 3) in females
in contrast with males
−
−
(negative allometric growth), indicating that females were heavier than males with a growing
− −
−
length TL (Figure 2).
φ
3.1.3. TL-CL Relationship
A linear equation was estimated for males as CL = 0.3872 + 0.2581(TL), r2 = 0.7394,
and CL = 0.2399 + 0.2916(TL), r2 = 0.805 for females. The size of the female carapace was
larger than that of the male (Figure 3).
−
−
3.1.4. Growth Parameters
−
−
−
−
The growth parameters evaluated using ELEFAN1 for males and females were
L∞ = 115.5 mm and 136.5 mm, respectively, with K = 0.76 yr−1 and t0 = −0.0366 for males
and K = 1.1 yr−1 and t0 = −0.08184 for females.
The VBGF was Lt = 115.5 [1 − e−0.76(t + 0.0366) ] for males and Lt = 136.5 [1 − e−1.1(t + 0.8184) ]
for females.
The obtained results of growth performance index (ϕ) were 4.01 and 4.31 for males
and females, respectively.
3.1.5. Mortality Rate
Total mortality (Z) for males = 3.99 yr−1 and females = 3.05 yr−1 , while the natural
mortality (M) was 1.91 yr−1 and 1.35 yr−1 for males and females, respectively. Fishing mortality (F) for males and females were 2.08 yr−1 and 1.70 yr−1 , respectively. Meanwhile,
exploitation rates (E) were 0.52 and 0.56 for males and females, respectively (Figure 4).
Figure 4. Cumulated catch curve based on length composition data for males (a) and females (b) of
S. crassicornis from the Gulf of Suez, Egypt.
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3.1.6. Length at First Capture
The length at first capture (LC), at which 50% of the shrimp are vulnerable to capture
(L50%), was estimated as 72.3 mm and 94.6 mm for males and females, respectively (Figure 5).
Figure 5. Probability of capture (L50% or LC) for males (a) and females (b) of S. crassicornis from the Gulf of Suez, Egypt.
3.1.7. Relative Yield per Recruit
The relationships between Y/R and B/R of both males and females showed that Emax ,
E0.1, and E0.5 were the same for males and females (0.421, 0.355, and 0.278, respectively)
(Figure 6).
Figure 6. Relationship between the relative yield per recruit (Y/R) and biomass per recruit (B/R) applying knife-edge
procedure for males (a) and females (b) of S. crassicornis from the Gulf of Suez, Egypt. “Red line =− E0.5 − Green− = E0.1 −
Yellow = Emax ”.
3.2. Molecular Analysis
Positive PCR amplifications were manifested by the tested samples using the primer
pairs of both eukaryotic18S rRNA and COI mitochondrial genes. PCR amplicons of 469
and 683 bp were obtained for the 18S rRNA and COI target regions, respectively. BLAST
comparisons of the resultant 18S rRNA sequences showed 99% similarity with S. crassicornis,
which was confirmed by both the alignment of the obtained COI sequences (99% similarity
with S. crassicornis) and the morphological examination results.
The COI sequences obtained for the specimens in our study were assigned a BIN
(BOLD ABE7069). BOLD identified the nearest neighbor of the study species as S. koelbeli
(BOLD ACS4793), with a p-distance of 0.32%. The analysis of Group Mean genetic distances
among S. crassicornis from different countries (Egypt, China, and India) showed that the
pairwise distances for the Egyptian S. crassicornis ranged from 0.024 in relation to its Indian
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reference group to 0.048 in relation to the Chinese S. crassicornis counterparts. On the other
hand, the estimation of the genetic distance among the species of Solenocera revealed that S.
melantho was the closest to S. crassicornis with a genetic distance of 0.071. Where, S. pectinata
was the most distant from S. crassicornis with a genetic distance of 0.27. Values of genetic
distances among species of Solenocera genus are presented in Table 1.
COI-based ML tree (Figure 7) for Solenocera species (from different countries) grouped
the studied Solenocera species into two distinct clusters. The first cluster branched into
three clades that included S. crassicornis from different countries and S. melantho in the first
clade; S. choprai, S. hextii, S. koelbeli, and S. annectens in the second clade. The second cluster
included S. pectinate, S. rathbuni, and S. agassizi in the first clade and S. membranacea in the
second clade. COI-based ML phylogenetic tree among different species of Solenocera is
shown at Figure 7.
Figure 7. COI-based maximum likelihood (ML) phylogenetic tree among Solenocera species all over
the world.
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Table 1. COI (cytochrome oxidase subunit I)-based pairwise genetic distances among Solenocera species worldwide.
S. choprai
S. agassizi
S. annectens
S. crassicornis
S. hextii
S. koelbeli
S. melantho
S. membranacea
S. pectinata
S. choprai
S. agassizi
0.203
S. annectens
0.152
0.194
S. crassicornis
0.161
0.195
0.169
S. hextii
0.136
0.181
0.162
0.137
S. koelbeli
0.228
0.226
0.229
0.146
0.190
S. melantho
0.175
0.190
0.181
0.071
0.148
0.148
S. membranacea
0.204
0.172
0.174
0.192
0.190
0.233
0.195
S. pectinata
0.169
0.170
0.181
0.188
0.179
0.270
0.192
0.176
S. rathbuni
0.154
0.161
0.161
0.148
0.138
0.215
0.165
0.171
0.134
S. rathbuni
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4. Discussion
This novel study introduces S. crassicornis, the lone species of Solenocera in Egypt. Our
results provide useful clues about its morphological and molecular characterization, growth
parameters, and population dynamics. DNA barcoding has been established as universal
tools to identify different species of organisms during the last decade. This molecularbased approach involves sequencing a short and standardized gene region to identify and
recognize species such as fish [20]. DNA barcoding does not look to disregard the morphological assessment, and its general purpose is to build an alliance between molecular and
morphological taxonomists for quick and unequivocal species identification [30].
Although Solenocera encompasses 38 species, DNA barcoding studies of these species
are rare. This study is the first to integrate two molecular markers, namely, the nuclear marker 18S rRNA and the mitochondrial marker COI, to characterize S. crassicornis.
The analysis of both markers showed 99% similarity with their reference sequences in the
GenBank database, demonstrating a high discrimination level of both markers at a high
taxonomic level, and molecular identification matched the morphological identification
of the species under examination. The phylogenetic relationship between the Egyptian
S. crassicornis and the other S. crassicornis from China and India revealed the close relationship between the specimens from Egypt and their counterparts from India (both of them
were clustered in a sub-clade), while the specimens from China were grouped in a separate
cluster of the ML tree. These phylogenetic relationships clarified the Indo-West Pacific
origin of S. crassicornis [5,45] and suggested its existence in the Red Sea as a migratory
species that translocated from the Indian Ocean. This may explain the high comparability
despite the natural geographical barrier between these distant areas. Abbas et al. [28]
reported that Penaeid shrimps are an effective migratory species that can migrate over vast
distances. For instance, Melicertus plebejus was collected approximately 900 km from its origin in Australia [46]. Interestingly, our study is the first to construct a phylogenetic tree of
species of Solenocera capable of separating them according to genetic distance and locating
S. crassicornis in the correct position in relation to its close relatives of the same genus.
In the current work, monthly variations of length frequency were utilized to decide the
growth parameters of S. crassicornis, and to evaluate other population dynamic parameters.
The results of morphometric measurements in the present study clearly demonstrated
that the female reached both larger size and higher growth rate than males showing sexspecific growth this is due to the higher growth performance index for females than males
of the same age group. This observed growth difference is common for many shrimp
species [29,47]. The population parameters are consistent with that of S. crassicornis estimated growth parameters reported from the same species in other regions [11,48,49].
Chakraborty et al. [48] studied the S. crassicornis in in Maharashtra coast and reported that
the population dynamics parameters for males and females individually was L∞ = 92 mm,
K = 1.5 yr−1 , Z = 6.00 yr−1 , M = 3.20 yr−1 , F = 3.60 yr−1 , and E = 0.53 for males and
L∞ = 139 mm, K = 2.00 yr−1 , Z = 10.36 yr−1 , M = 6.92 yr−1 , F = 3.44 yr−1 , and E = 0.67
for females. Such wide deviations in the growth parameters assessed by different researchers are due to differences in observed sizes, age, sample size, and environmental
conditions [50–52]. Pauly et al. [36] cited that the equation could be utilized for shrimps
or prawns and any marine invertebrates because these marine organisms share similar
resources, habitats, and predators as fish, and they are probably not going to differ widely
in their vital parameters [53]. Our results clearly indicated the overfishing situation in the
Suez gulf (E > 0.5). These results agreed with Xue et al. [11] that studied S. crassicornis in
the East China Sea and with Chakraborty et al. [48,49] in Maharashtra coast.
5. Conclusions
The current work is a novel study presents S. crassicornis (H. Milne Edwards, 1837),
as a lone commercially important shrimp species of the Solenoceridae family (Penaeoidea
superfamily) in the Red Sea, Egypt. This species is distributed in the Indo-West Pacific,
Japan, China, Hong Kong, and North Borneo. The first record of this species in the
J. Mar. Sci. Eng. 2021, 9, 9
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Mediterranean shelf of Egypt was in 1981, identified as S. indicus (Nataraj, 1945). Our study
is the first report investigating this species in Al-Attaka, a commercial landing site of the
Gulf of Suez, the Red Sea Shelf of Egypt. Morphological features, molecular identification,
and DNA barcoding (18S rRNA nuclear markers and COI mitochondrial markers) were
investigated of this species in the Gulf of Suez to precisely identify this Indian-water species
as S. crassicornis (H. Milne Edwards, 1837). Despite the social and economic relevance of
S. crassicornis in the area, information about the hatching, larval rearing, and farming of
S. crassicornis is scarce. Finally, the current novel study is an opportunity to understanding
the impacts on wild fisheries of this economic species in the Red Sea, as well as, it is a good
opportunity to understanding genetic structures to start breeding programs domestication
and selection for aquaculture of this economically commercial species under Egyptian
conditions.
Author Contributions: Conceptualization, E.M.A. and Z.Z.S.; methodology, E.M.A., M.A., F.S.A.,
M.G.D., A.E.-S. and Z.Z.S.; software, E.M.A., Z.Z.S., F.S.A. and M.G.D.; validation, M.G.D., A.E.-S.,
Z.Z.S., M.M.M. and M.A.; formal analysis, Z.Z.S., M.G.D., F.S.A., M.M.M. and A.E.-S.; investigation,
M.A., A.E.-S. and Z.Z.S.; resources, E.M.A. and A.E.-S.; data curation, M.A., Z.Z.S., A.E.-S., M.M.M.
and M.G.D.; writing—original draft preparation, E.M.A., F.S.A., M.A., M.G.D. and Z.Z.S.; writing—
review and editing, M.A. and A.E.-S.; visualization, E.M.A., A.E.-S. and Z.Z.S.; supervision, E.M.A.,
M.A. and Z.Z.S.; project administration, E.M.A., A.E.-S. and Z.Z.S.; and funding acquisition, A.E.-S.
All authors have read and agreed to the published version of the manuscript.
Funding: This research was funded by the Vice Deanship of Scientific Research Chairs (DSRVCH) at
King Saud University.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Informed consent was obtained from all subjects involved in the study.
Data Availability Statement: The data presented in this study are available on request from the
corresponding authors.
Acknowledgments: The authors are grateful to the Deanship of Scientific Research, King Saud
University for funding this research project through Vice Deanship of Scientific Research Chairs
(DSRVCH) at King Saud University.
Conflicts of Interest: The authors declare no conflict of interest.
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