sign in sign up
<<
Home , Acanthocyclops, Aegisthidae, Arietellidae, Clausocalanidae, Cyclopinidae, Cylindropsyllidae

J. Ocean Univ. China (Oceanic and Coastal Sea Research) https://doi.org/10.1007/s11802-020-4474-5 ISSN 1672-5182, 2020 19 (6): 1409-1420 http://www.ouc.edu.cn/xbywb/ E-mail:[email protected]

Morphology and Phylogeny of Taeniacanthus yamagutii Shiino, 1957 (: ), a Infecting the Gills of Rosy Goatfish Parupeneus rubescens (Mullidae) in the Arabian Gulf

ABDEL-GABER Rewaida1), 2), *, AL-QURAISHY Saleh1), DKHIL Mohamed A.1), 3), ALGHAMDI Masheil1), ALGHAMDI Jawahir1), and KADRY Mohamed2)

1) Zoology Department, College of Science, King Saud University, Riyadh 11451, Saudi Arabia 2) Zoology Department, Faculty of Science, Cairo University, Cairo 12613, Egypt 3) Department of Zoology and Entomology, Faculty of Science, Helwan University, Cairo 11794, Egypt

(Received February 1, 2020; revised June 18, 2020; accepted July 7, 2020) © Ocean University of China, Science Press and Springer-Verlag GmbH Germany 2020

Abstract The present study was to investigate the copepodid infecting rosy goatfish Parupeneus rubescens, one of the most economically important fishes in the Arabian Gulf. A copepodid species identified from the examined fish specimens belongs to the Taeniacanthidae family and is labeled as Taeniacanthus yamagutii Shiino, 1957, mainly depending on its morphological, mor- phometric, and ultrastructural characteristics, in particular the presence of maxilliped claw with a conspicuous digitiform process at the base, the terminal process of the second maxilla stout, and a setiform element at the tip of each exopod spine of legs 2–4. In order to ensure the accurate identification and exact taxonomic characterization of this species, the 28S rRNA gene sequence was analyzed. The result revealed that the present copepodid species belong to the Taenicanthidae family and has a close relationship with Taeniacanthus yamagutii (gb| KR048852.1) in the same taxon. The present study demonstrated that the rosy goatfish is a host for Taeniacanthus species, which will be helpful to prevent this parasitic infection.

Key words parasitic ; Taeniacanthidae; Taeniacanthus spp.; Arabian Gulf

Sumpf, 1871; Anchistrotos Brian, 1906; Irodes Wilson, 1911; 1 Introduction Phagus Wilson, 1911; Haematophilus Wilson, 1924; Tae- niacanthodes Wilson, 1935; Parataeniacanthus Yamaguti, Taeniacanthidae is a unique family within the copepod 1939 (Accepted as Taeniacanthus Sumpf, 1871); Pseudo- order , comprising members either parasitic to taeniacanthus Yamaguti and Yamasu, 1959; Echinirus Hu- marine fish or associated with sea urchins (Dojiri and Hu- mes and Cressey, 1961; Echinosocius Humes and Cressey, mes, 1982; Boxshall and Halsey, 2004). Taeniacanthids ex- 1961; Metataeniacanthus Pillai, 1963; Scolecicara Ho, 1969; hibit a high degree of host specificity at both the generic Taeniastrotos Cressey, 1969; Clavisodalis Humes, 1970; and specific levels (Boxshall and Halsey, 2004). This fa- Cirracanthus Dojiri and Cressey, 1987; Nudisodalis Do- mily, along with Bomolochidae Sumpf, 1871, Tuccidae Ver- jiri and Cressey, 1987; Biacanthus Tang and Izawa, 2005; voort, 1962, and Tegobomolochidae Avdeev, 1978, are mem- Caudacanthus Tang and Johnston, 2005; Umazuracola Ho, bers of the bomolochiform complex (Dojiri and Cressey, Ohtsuka, and Nakadachi, 2006; Saging Uyeno, Tang, and 1987; Boxshall and Halsey, 2004). They are characterized by the presence of an indistinctly four-segmented antenna; Nagasawa, 2013; Triacanthus Kim and Moon, 2013 (Ac- bearing two pectinate processes, claw-like spines, and se- cepted as Sunchenonacanthus Venmathi Maran, Moon, Ad- tae; a mandible with two subequal spinulated blades; a day, and Tang, 2016); Cepolacanthus Venmathi Maran, maxilla bearing spinulated elements; a concave ventral sur- Moon, Adday, and Tang, 2016; Suncheonacanthus Venma- face of the cephalothorax; and a lamelliform leg 1. There thi Maran, Moon, Adday, and Tang, 2016. are 25 genera with more than 91 species in Taeniacanthi- Research on ectoparasitic copepods has so far been very dae (Tang and Izawa, 2005; Tang and Johnston, 2005; Ho limited. As the number of copepodologists is relatively and Lin, 2006; Walter and Boxshall, 2019). These genera low (Ho, 2001), the morphological and anatomical fea- include Krøyer, 1837; Haemaphilus; Taeniacanthus tures are not enough to recognize and classify copepods (Hamza et al., 2007; Ramdane, 2009). Several molecular * Corresponding author. E-mail: [email protected] approaches have recently been used to check the taxo-

1410 ABDEL-GABER et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2020 19: 1409-1420 nomic status of copepods independently (Fls et al., 2006; 70%, 80%, 90%, 100%) for 10 min, respectively. The sam- Ferrari and von Vaupel Klein, 2019). In copepod taxon- ples were then processed at the critical point drier ‘LEICA, omy, DNA barcoding was used to identify intra- and inter- EM CPD300’ with Freon 13, sputter-coated with gold-pal- specific morphological and molecular distinctions to help ladium in Auto fine coater (JEOL, JEC-3000FC), and fi- their phylogenetic relationship (Yazawa et al., 2008). How- nally examined and photographed under the Etec Auto- ever, very few attempts have been made to use molecular scan at 10-kV Jeol scanning electron microscope (JSM- data to restore interordinal associations within Copepoda, 6060LV) at the Molecular Biological Unit in Prince Naif as a result of the insufficient taxon sampling or sequenc- Health Research Center, King Saud University, Riyadh, ing uncertainty (Kim and Kim, 2000; Ferrari et al., 2010). Saudi Arabia. Huys et al. (2007) found that nuclear ribosomal genes The different body parts of the recovered copepods were 18S and 28S rRNA include semi-conserved domains that measured using the Olympus ocular micrometer and the intersperse with divergent regions, allowing for a wide average values with the range given in parentheses were range of taxonomic levels of phylogenetic reconstruction. employed for analysis. Sewell’s style (1949) was adopted There is a need for more extensive work to gain a better for the armature formula of the swimming legs, in which understanding of the parasitic copepods infecting the Ara- the spines and setae are denoted by Roman and Arabic bian Gulf fish in general and those off Saudi Arabia in numerals, respectively. particular. The purpose of this research is to provide com- plete data on parasitic copepods and their indices in the 2.3 Molecular Analysis rosy goatfish Parupeneus rubescens from the Arabian Gulf 2.3.1 DNA extraction and polymerase chain in Saudi Arabia. In addition, partial sequences of 28S rRNA reaction (PCR) gene have been developed and used to evaluate the phy- Genomic DNA was extracted from ethanol-contained logenetic status of this species within Taeniacanthidae. samples using the DNeasy tissue kit© (Qiagen, Hilden, Germany) following the manufacturer’s instructions. DNA 2 Materials and Methods quality and purity were quantified with the NanoDrop ND-1000 spectophotometer (Thermo Fischer Scientific,

2.1 Fish Collection Inc., Wilmington, DE, USA) and 20 ng of genomic DNA A total of 80 specimens of the rosy goatfish, Paru- was used for PCR amplification. The 28S rRNA gene re- peneus rubescens (F: Mullidae), were collected from land- gion was amplified by PCR and subsequently sequenced. ing sites on the coasts of the Arabian Gulf off Dammam The PCR for this region was produced in a total of 20 µL City in Saudi Arabia. They were immediately transported of reaction volume containing 4 μL 5× FIREPol® Master to the Laboratory of Parasitology Research, Zoology De- Mix (Solis BioDyne), 2 μL of genomic DNA, 0.6 μL of partment, College of Science, King Saud University, Ri- each primer, and completed to the required volume of 20 yadh, Saudi Arabia. All procedures comply with the ethi- µL by nuclease-free water. PCR amplification was per- cal standards approved by the Institutional Review Board formed using the following primers: 28SF, 5’-ACA ACT (IRB) of King Saud University, Riyadh, Saudi Arabia. Sam- GTG ATG CCC TTA G-3’ and 28SR, 5’-TGG TCC GTG ples of fish were classified according to the standards of TTT CAA GAC G-3’ previously designed by Song et al. the database of fishbase.org. They were thoroughly check- (2008). The amplification technique of the PCR thermo- ed for the presence of parasitic infections on cycler profile and the primer combination used to amplify their body surface, fins, head, gill filaments, oral cavities this genetic marker was done according to Song et al. and other tissues, based on the method described previ- (2008). All PCR products were verified on 1% agarose gel ously by Ravichandran et al. (2007). in 1× Tris-acetate-EDTA (TAE) fixed with 1% ethidium bromide and then visualized with a UV trans-illuminator. The PCR products of the expected size were gel-excised, 2.2 Parasitological Studies purified and cloned using the manufacturer’s instructions 2.2.1 Light microscopic examination for the PureLinkTM Quick Gel Extraction Kit (Qiagen, Parasitic copepods were removed using a special nee- Hilden, Germany). dle. They were washed several times in a saline solution, preserved in 70% ethyl alcohol, dehydrated in a 2-h glyc- 2.3.2 Sequence alignment and phylogenetic analysis erin ethanol series, and mounted as temporary preparations Sequencing was performed on 3130×l Genetic Analy- in lactophenol as described by Pritchard and Kruse (1982). zer (Biosystems® 3130, Thermo Fisher Scientific, USA) Prepared samples were analyzed and photographed using using the Dye Terminator Cycle Sequencing Ready Reac- the Leica DM 2500 microscope (NIS ELEMENTS soft- tion Kit (Perkin Elmer). A BLAST search was carried out ware, ver. 3.8). in the NCBI database to identify related sequences. The resulting sequences were aligned directly with CLUSTAL- 2.2.2 Scanning electron microscopic examination X Multiple Sequence Alignment using other gene region Buffered glutaraldehyde (3%, pH 7.2) was used to fix sequences available from GenBankTM. The alignment was recovered copepod parasites. After 4 h, fixed parasites were updated manually using BIOEDIT 4.8.9 software. Phy- dehydrated in the ascending ethanol series (50%, 60%, logenetic analyses were conducted using maximum par-

ABDEL-GABER et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2020 19: 1409-1420 1411 simony (MP) and Bayesian inference (BI). MP analysis 1; 7 was performed with MEGA version 7.0 (Kumar et al., Leg 2: coxa 0 – 0; basis 1 – 0; exopod I – 0; I – 1; II,I,4; en- 2016) using a maximum likelihood method focused on dopod 0–1; 0–1; III,3 the Tamura-Nei model (Tamura and Nei, 1993). BI analy- Leg 3: coxa 0–0; basis 1–0; exopod 1–0; 1–1; II,I,5; en- sis was carried out with MrBayes ver. 2.01 (Huelsenbeck dopod 0–1; 0–1; III,2 and Ronquist, 2001) using GTR + I + Γ nucleotide substi- Leg 4: coxa 0–0; basis 1–0; exopod I–0; I–1; II,I,4; en- tution model. The tree was drawn to scale, and the branch dopod 0–1; 0–1; I,I,1 lengths in the same units were applied as the evolution Leg 5 uniramous, 2-segmented; basal segment with 1 distances to deduce the phylogenetic tree. dorsolateral seta and spinules on distal border; second seg-

ment 0.175 × 0.082; inner margin straight, with 4 patches of spinules; distal margin with 3 spines and 1 seta. Leg 6 3 Results represented by 3 setae in the area of egg sac attachment. Twenty five out of eighty (31.25%) specimens of the ex- amined rosy goatfish Parupeneus rubescens were found 3.2 Description of Male Specimens (Figs.3 (A–I), to be naturally infected by a copepodid parasite known as 4 (A–G)) Taeniacanthus yamagutii Shiino, 1957 in the gill region Total body length (excluding setae on caudal rami) 1.71 of infected fish. µm (1.65 – 1.79) and width 0.61 (0.54 – 0.72). Cephalotho-

rax 0.321 × 0.634 and comprising about 20% of the total 3.1 Description of Female Specimens (Figs.1 (A–L), body length. Genital somite spinulated and slightly wider

2 (A–H)) than long 0.212 × 0.251. Abdomen 3-segmented; segments

Total body length (excluding setae on caudal rami) 2.20 from anterior to posterior 0.121 × 0.185, 0.118 × 0.171, and µm (2.07–2.43) and width 0.99 (0.87–1.03). Prosome com- 0.175 × 0.151; anal somite armed with spinules as in fe- posed of broad cephalothorax (1st pedigerous somite fused male. Caudal ramus as female but smaller in size, 0.123 × with cephalosome) and 3 narrower pedigerous somites. Ce- 0.049. phalothorax bears a highly sclerotized transverse bar and Appendages as in females, except for the features men- a marginal hyaline membrane. Urosome includes the 5th tioned below. Terminal segment of the second maxilla is pedigerous somite, genital double-somite and free abdo- more slender than that of the female. Maxilliped 4-seg- minal somites. Cephalothorax wider than length, approxi- mented; first segment large, with 1 naked distal seta; se- mately 0.410 × 1.03, comprising less than 20% of the over- cond segment with row of spinules along the inner mar- all body length. Thoracic segments bearing legs 2, 3, and gin and a semicircular group of spinules; third segment 4 relatively large and decreasing in width posteriorly. Ge- small; fourth segment with a curved claw and 2 anterior nital somite wider than long, 0.210 × 0.295, armed with and 1 posterior setae. Leg 5 is similar to that in females ex- spinules. Abdomen 4-segmented; from anterior to poste- cept for the second segment 0.108 × 0.045. rior 0.157 × 0.298, 0.138 × 0.275, 0.072 × 0.223, and 0.199

× 0.203; anal somite bearing patches of spinules. Caudal 3.3 Molecular Analysis

ramus 0.159×0.061 and bearing 6 setae. A total of 477 bp with 54.08% GC content was evalu- Rostral area with a sclerotized ventromedian part. An- ated and deposited in GenBank under the accession num- tennule (antenna 1) 6-segmented; armature formula: 5, 15, ber MN413507.1 for the 28S rRNA gene region of the 8, 4, 2+1 aesthetasc, and 7+1 aesthetasc. Antenna (anten- existing copepoda species. Phylogenetic analyses were per- na 2) 4-segmented first segment with 1 seta; second seg- formed by aligning the partial and complete sequences of ment with 1 short, broad, leaf-like seta; third segment with 28S rRNA gene with 22 taxa of three copepodid orders 2 processes and 1 claw; fourth segment short armed with (Cyclopoida, , and ) (Table 1, Figs.5, 4 claws and 2 setae. Postantennal process relatively short 6). The results showed that 28S rRNA of this species re- tine. Labrum with posterior spinulose margin. Mandible vealed sequence identities 95.35% – 80.13% with Cyclo- with 2 unequal spinulate blades. Maxillule (maxilla 1) lo- poida, 91.47% – 91.05% with Harpacticoida, and 91.02% – bate and apically with 5 setae. Maxilla (maxilla 2) 2-seg- 90.62% with Calanoida (Table 1). Among Cyclopoida, the mented; basal segment naked; elongated distal segment present species is 95.35% – 94.91% identified with Taeni- with 2 small setae in the middle and distal claw-like apex. canthidae family taxa, 94.04% – 92.73% with Bomolochi-

Maxilliped 3-segmented; first segment very broad with 1 dae, 90.43% with Cyclopettidae, 89.46% – 80.13% with Cy- naked seta; second segment very slender, with 1 pair of clopidae, and 82.56% with Clausidiidae. Among Cyclopoida, setae proximally; third segment with terminal claw, dis- the maximum identity (95.45%) with the lowest divergent tally with 2 rows of spinules and proximally with 2 setae value was recorded between the present copepodid species and 1 short process. and Taeniacanthus yamagutii (gb| KR048852.1), followed

Legs 1 – 4 biramous. Leg 1 with 2-segmented exopod and by Anchistrotos kojimensis (94.91%, gb| KR048834.1), Bo- endopod. Legs 2 – 4 with 3-segmented exopod and endo- molochus decapteri (94.04%, gb| KR048838.1), Notho- pod. Spines on exopods of legs 2 – 4 rod-shaped, with blunt bomolochus thambus (92.73%, gb| KR048820.1), Para- tip. Armature of legs 1–4 as follows: cyclopina nana (90.43%, gb| KR048803.1), Pseudotae-

Leg 1: coxa 0 – 1; basis 1 – 1; exopod 1 – 0; 9; endopod 0 – niacanthus congeri (90.29%, gb| KR048819.1), Apocyclops

1412 ABDEL-GABER et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2020 19: 1409-1420

Fig.1 Photomicrographs of the adult female Taeniacanthus yamagutii infecting Parupeneus rubescens. (A, B) Whole mount preparation of: (A) Ventral view; (B) Lateral view; (C–L) High magnifications for different body parts showing: (C) Rostral area; (D) Anterior region of cephalothorax; (E) Postoral appendages; (F) Thoracic zone with legs; (G) First tho- racic leg; (H) Thoracic legs from second to fifth leg; (I) Fourth and fifth thoracic legs with appearance of abdomen and egg sac; (J–L) Urosome with abdomen ended with caudal rami and setae that surrounded with egg sac. AB, abdomen; ANT 1, 1st antenna; ANT 2, 2nd antenna; AS, anal somite; AE, aesthete; CR, caudal rami; ESC, egg sac; GS, genital somite; L1, 1st leg; L2, 2nd leg; L3, 3rd leg; L4, 4th leg; L5, 5th leg; L6, 6th leg; LB, labrum; MAN, mandible; MAP, maxilliped; MAX1, maxilla 1; MAX2, maxilla 2; PR, prosome; RA, rostral area; S, setae; SP, spinule; UR, urosome.

ABDEL-GABER et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2020 19: 1409-1420 1413

Fig.2 Scanning electron micrographs of the adult female Taeniacanthus yamagutii infecting Parupeneus rubescens. (A, B) Whole mount preparation of: (A) Dorsal view; (B) Ventral view; (C–H) High magnifications for different body parts of: (C–E) Anterior region of cephalothorax with postoral appendages; (F, G) Thoracic legs; (H) Abdomen and egg sac. AB, abdomen; ANT 1, 1st antenna; ANT 2, 2nd antenna; AS, anal somite; AE, aesthete; CR, caudal rami; ESC, egg sac; GS, genital somite; L1, 1st leg; L2, 2nd leg; L3, 3rd leg; L4, 4th leg; L5, 5th leg; L6, 6th leg; LB, labrum; MAN, mandible; MAP, maxilliped; MAX1, maxilla 1; MAX2, maxilla 2; PR, prosome; RA, rostral area; S, setae; Sp, spinule; UR, uro- some. panamensis (89.36%, gb| MK370246.1), sp. all of the copepodid species was clearly divided into two (89.32%, gb| MK370278.1), Hemicyclops ctenidis (82.56%, separate clades (Figs.5, 6). The first clade contains some gb| KR048817.1), vernalis (82.16%, gb| KR copepodid species belonging to the Taenicanthidae and Bo- 048812.1), ishidai (81.07%, gb| KR048802.1), molochidae families of the order Cyclopoida, and the other taihokuensis (81.07%, gb| KR048801.1), species belonging to the order of Calanoida. The second albidus (80.76%, gb| KF153696.1), Diacy- clade consisted of other copepodid species belonging to clops bicuspidatus (80.74%, gb| KF153697.1), and Meso- the Cyclopoidae and Cyclopettidae families of the order pehpeiensis (80.13%, gb| KR048797.1) (Table 1). Cyclopoida, and other species belong to the order of Har- The phylogenetic trees showed that the cluster containing pacticoida. Dendrograms revealed the species studied in

1414 ABDEL-GABER et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2020 19: 1409-1420 this research is closely related to Taeniacanthus yamagu- ed to each other with the distinctive generic features and tii (gb| KR048852.1) in the same taxon. identical body proportions. The current study of Taenia- canthus yamagutii is the first report of this parasitic spe- cies as a rosy goatfish ectoparasite. 4 Discussion Taeniacanthus yamagutii was originally described as Taeniacanthidae Wilson, 1911 is a family that flourish ‘Irodes teradontis’ (Bassett-Smith, 1898). Shiino (1957) pro- as fish parasites. Taeniacanthus Sumpf, 1871 is the largest posed that the specimens of Yamaguti were not conspe- of the Taeniacanthidae family, comprising 62 spe- cific to the species described by Bassett-Smith in 1898, and cies of poecilostome copepods parasitic on both cartila- thus established a new species, Irodes yamagutii. This spe- ginous and bony fish (Walter and Boxshall, 2019). The cies was later transferred to the genus Taeniacanthus by present copepodid species is consistent with other Taenia- Yamaguti and Yamasu (1959). T. yamagutii is the most canthus species with special respect to the previously de- closely related species to both T. fugu Yamaguti and Ya- scribed Taeniacanthus yamagutii, which are closely link- masu, 1959, and T. kitamakura Yamaguti and Yamasu, 1959.

Fig.3 Photomicrographs of the adult male Taeniacanthus yamagutii infecting Parupeneus rubescens. (A, B) Whole mount preparation of: (A) Ventral view; (B) Lateral view; (C) Rostral area with antenna; (D) Postoral appendages; (E–H) Tho- racic legs; (F) Abdomen with caudal rami. AB, abdomen; ANT 1, 1st antenna; ANT 2, 2nd antenna; AS, anal somite; AE, aesthete; CR, caudal rami; GS, genital somite; L1, 1st leg; L2, 2nd leg; L3, 3rd leg; L4, 4th leg; L5, 5th leg; LB, labrum; MAN, mandible; MAP, maxilliped; MAX1, maxilla 1; MAX2, maxilla 2; PR, prosome; RA, rostral area; S, setae; SP, spi- nule; UR, urosome.

ABDEL-GABER et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2020 19: 1409-1420 1415

Fig.4 Photomicrographs of the adult adult male Taeniacanthus yamagutii infecting Parupeneus rubescens. (A, B) Whole mount preparation of: (A) Ventral view; (B) Dorsal view; (C–G) High magnifications for different body parts showing: (C, D) Anterior region of cephalothorax with postoral appendages; (E–G) Thoracic legs. AB, abdomen; ANT 1, 1st antenna; ANT 2, 2nd antenna; AS, anal somite; CR, caudal rami; GS, genital somite; L1, 1st leg; L2, 2nd leg; L3, 3rd leg; L4, 4th leg; L5, 5th leg; LB, labrum; MAN, mandible; MAP, maxilliped; PR, prosome; RA, rostral area; S, setae; SP, spinule; UR, urosome.

Table 1 Copepod species used in phylogenetic analyses of Taeniacanthus yamagutii specimens obtained in this study Parasite species Order/family Accession no. Percent identity (%) GC content Taeniacanthus yamagutii Cyclopoida/Taeniacanthidae KR048852.1 95.35% 54.9% Anchistrotos kojimensis Cyclopoida/Taeniacanthidae KR048834.1 94.91% 52.1% Bomolochus decapteri Cyclopoida/Bomolochidae KR048838.1 94.04% 55.0% Nothobomolochus thambus Cyclopoida/Bomolochidae KR048820.1 92.73% 55.7% parvipilis Harpacticoida/ MK097466.1 91.47% 57.4% Pontostratiotes sp. Harpacticoida/ MF077835.1 91.47% 58.1% Stenocaropsis sp. Harpacticoida/ MF077828.1 91.05% 60.1% Kyphocalanus sp. Calanoida/Kyphocalanidae MF959859.1 91.02% 56.6% Calanoida/ EU477089.1 91.02% 54.5% Paraugaptilus buchani Calanoida/ HM997028.1 90.62% 56.0% Paracyclopina nana Cyclopoida/Cyclopettidae KR048803.1 90.43% 60.8% Pseudotaeniacanthus congeri Cyclopoida/Taeniacanthidae KR048819.1 90.29% 57.55% Apocyclops panamensis Cyclopoida/ MK370246.1 89.36% 60.5% (to be continued)

1416 ABDEL-GABER et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2020 19: 1409-1420

(continued) Parasite species Order/family Accession no. Percent identity (%) GC content Halicyclops sp. Cyclopoida/Cyclopidae MK370278.1 89.32% 63.2% Hemicyclops ctenidis Cyclopoida/Clausidiidae KR048817.1 82.56% 56.8% Acanthocyclops vernalis Cyclopoida/Cyclopidae KR048812.1 82.16% 60.5% Tropocyclops ishidai Cyclopoida/Cyclopidae KR048802.1 81.07% 58.7% Thermocyclops taihokuensis Cyclopoida/Cyclopidae KR048801.1 81.07% 58.7% Cyclopoida/Cyclopidae KF153696.1 80.76% 59.6% bicuspidatus Cyclopoida/Cyclopidae KF153697.1 80.74% 59.7% pehpeiensis Cyclopoida/Cyclopidae KR048797.1 80.13% 60.6%

Fig.5 Maximum parsimony analysis based on the 28S rRNA gene sequence demonstrating the position of the present co- pepodid species.

Fig.6 Phylogenetic position of the recovered copepod species based on Bayesian analysis of the 28S rRNA gene sequence.

ABDEL-GABER et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2020 19: 1409-1420 1417

The most distinctive characters of T. yamagutii are the ter- armature of 12,6,3,1+2,7 aesthetasc; 2-segmented antenna minal process of the second maxilla stout, maxilliped claw with proximal segment bears 3 simple and 2 pectinate claws; with a conspicuous digitiform process at the base, a seti- third exopodal segment of 1st leg bears 6 plumose setae; form element at the tip of each exopod spine of the legs T. upenei upeneoides Yamaguti, 1954 getting the armature

2 – 4. of a 5-segmented antennule 13+3+2, 6+3, 1+3, 3+1+2, 7 In addition, it has some similarities to other Taenia- setae; and exopod of 1st leg with 8 plumose setae. canthus species, such as T. ostracionis Richiardi, 1870, T. It also distinguished from T. acanthocepolae, T. neoper- moa Lewis, 1967, T. larsonae Tang et al., 2011, and T. cis, T. dentatus, with a maxillary hook has a stout base thackerae Tang et al., 2011. The similarities include the and a curved claw; the third segment of the antenna has same antennule armature; the presence of spinules row on two spine-setae and four strong claws. With regard to T. the ventromedian surface and along the posterior margin ostracionis, T. larsonae, T. thackerae, there are some struc- of the labrum; the lobate maxillule carrying semi-pinnate tural changes as the presence of two sclerotized structures seta, anterior knob-like process and 2 long and 2 short on each side of T-shaped plate of rostral area; and caudal naked setae; the third exopodal segment of leg 3 bearing rami bears 7 setae. Lewis (1967) noted some differences 5 setae; and a terminal rod-shaped spines on each exopo- with T. moa having a cephalothorax with a transverse dor- dal spine of legs 2 – 4. It is quite similar to T. mcgroutheri sal striae; and a distomedial corner of a maxilliped basis Tang et al., 2011, and T. kiemae Tang, 2011 as they all have with a bilobed protrusion; T. aluteri having a flagellum at a spinulate terminal process on the basis of maxilla, and the distal end of each exopodal spine of legs 2 – 4; and T. their endopod of maxilliped are elongated, claw-like and pectinatus Yamaguti and Yamasu, 1959 having multiple strongly curved. Additionally, they all bear a large thorn- rows of spinules on large pectinate process of antenna; like process on the proximal anterior surface, a minute and a subterminal flagellum on each spine of free exopo- basal seta and a small spiniform process on the posterior dal segment of leg 5. surface. It is also similar to T. brayae Tang et al. 2011 as In addition, it differs from T. brayae, and T. mcgrouthe- they both have the same antennule armature, endopodal ri having a highly protuberant rostral area that lacks a scle- segment of maxilliped with a terminal curved claw. rotized structure on the ventral surface; the second endo- There are some similarities to T. acanthocepolae Yama- podal segment of antenna bears 2 unequal pectinate pro- guti, 1939, T. neopercis Yamaguti and Yamasu, 1959, and cesses and a claw-like spine. It is different from T. mcgrou- T. dentatus Sebastian, 1964. They all have a lateral border theri, having 14 setae on the second antennulary segment. of cephalothorax provided with a thin flexible membrane It’s different from T. lagocephali Izawa, 1986, having the originating from the ventral side. The maxillule has three setal formula of the antennule as 15,5,3,4,2+1 aesthete, setae, the outer seta is stout and the middle one is rela- 7+1 aesthete; and maxilliped with a long claw on 5th tively small. It is also quite similar to T. acanthocepolae segment that bears 2 proximal setae and ridge-like teeth. by the presence of a mandible tipped with 2 unequal blades In the case of a comparison to T. ballistae, there are bearing marginal serrations along the posterior margin; some differences, such as the rostral area broadly pro- the same maxillule structure; the third segment with max- truded anteriorly but without sclerite on its ventral surface; illiped with a curved claw carrying a tiny seta. It is simi- and the distal segment of maxilla tipped with 2 pinnate lar with T. anguillaris Devi & Shyamasundari, 1980, and spines in addition to a tiny subterminal seta. In addition, it T. lagocephali Pearse, 1952, as they all have slightly pro- differs from T. neopercis having post-antennal process with truded anteriorly rostral area with one sclerite in the ven- a curved, sharply pointed process; and labrum fringed with tro-median area of the flask-shaped, and 2 unequal blades spinules. It differed from T. acanthocepolae, and T. an- with marginal serrations on the mandible. Additionally, it guillaris having an armature formula of antennule as is similar to T. lagocephali, and T. balistae Claus, 1864, and 5,15,4,3,4,2+1 aesthete, and 7+1 aesthete; T. neopercis T. anguillaris by having a curved claw on the distal seg- having inclusion of 5 setae on the third exopodal segment ment of maxilliped. of legs 2 and 4, and the presence of 8 setae on the distal It has some similarities to T. platycephali Yamaguti, segment of the endopod of leg 1. 1939, T. kitamakura, T. aluteri Avdeev, 1977, T. compara- In addition, T. occidentalis Wilson, 1924 has a diffe- tus Dojiri and Cressey, 1987, having a rostrum with cir- rence of an apical spine that is at least twice as long as cular ventral sclerotization; the same structure of the an- proximal outer spine on terminal exopodal segment of leg tennule and maxillule; the terminal segment of the maxil- 2. It is different from T. similis Dojiri and Cressey, 1987, liped with 2 small setae proximally and strongly curved and T. ryukyuensis Tang et al., 2016 having caudal ramus distal claw. It is also similar to T. cynoglossi Rangnekar bears seven setae; and terminal segment of maxilla with and Murti, 1960, as they both have the terminal exopod spinulated terminal process; T. dojirii Tang et al., 2016 hav- segment of leg 4 with formula II,I,4. ing a maxillipedal claw with bristles on a large proximal There are, however, some differences with other Tae- seta; T. singularis Kim and Moon, 2013 having maxilli- niacanthus species, such as T. balistae Claus, 1864 hav- ped with short terminal claw; T. rotundiceps Shiino, 1957 ing an antennule armature of 5,11,7,4,2+1 aesthetasc, 7+1 having leg 5 exopod about 3 times as long as wide; and T. aesthetasc; sharp curved tine of post-antennal process; and sebastichthydis Yamaguti, 1939 having a ventral surface the presence of sickle-shaped claw of maxilliped; T. upe- of anal somite with 2 pairs of spinule rows. Dojiri and nei Yamaguti, 1954 having 5-segmented antennule with Cressey (1987) described a discrepancy between our para-

1418 ABDEL-GABER et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2020 19: 1409-1420 sitic species and T. digitatus, T. glomerosus, T. papulosus, was detected to be a distinct species with a very closely T. pollicaris, and T. williamsi, of rounded process tipped relationship with T. yamagutii (KR048852.1). with a nipple-like knob on the first maxilla. It could be concluded that the present study provided Accurate and reliable identification of parasite species valuable information of a copepodid species named as T. is necessary for biodiversity assessment (Cepeda et al., yamagutii, Shiino, 1957, which can infect rosy goatfish 2012). DNA sequence analysis of target genes offers in- Parupeneus rubescens and in the future, other genes will valuable information for such analyses. This research in- be studied to provide more information about this species, vestigated the variation of a portion of the 28S rRNA gene which will be helpful to prevent the infection of the fishes as a marker for the identification and classification of eco- in the local area. logically significant cyclopoid copepod genus Taeniacan- thus in the Arabian Gulf fish. In the 28S rRNA fragment, Acknowledgement D1–D2 region was chosen to analyze, which was suggest- ed by Sonnenberg et al. (2007) as a taxonomic marker due This study was supported by Researchers Supporting to its heterogeneity. Previous studies have used this mar- Project (No. RSP-2020/25), King Saud University, Riyadh, ker for the analysis of copepods and other taxa (Huys et al., Saudi Arabia. 2006, 2012; Brown et al., 2010; Blanco-Bercial et al., 2011; Hayward et al., 2011; Yeom et al., 2018). References Previously, Huys and Boxshall (1991) summarized ten taxonomic orders of copepods, nine of which had marine Avdeev, G. V., 1977. Two new and one known species of para- representatives. Huys et al. (2002) and Ho et al. (2003) sitic copepods of the Anchistrotos Brian, 1906 genus (Cyclo- reported that Copepoda are classified into three infraclasses: poida, Taeniacanthidae) from the Indian Ocean. Izvestiya Tik- hookeanskogo Nauchno-lssledovatehkogo Institute Rybnogo Progymnoplea Lang, 1948 (or Platycopioida Fosshagen and Khozyaistva i Okeanografii (TINRO), 101: 132-138. Iliffe, 1985); Gymnoplea Giesbrecht, 1892 (or Calanoi- Avdeev, G. V., 1978. Sistematicheskoe polozhenie roda Tegobo- da Sars, 1903); and Podoplea Giesbrecht, 1892. The pre- molochus Izawa, 1976 (Copepoda, Cyclopoida). Izvestiya Tik- sent phylogenetic trees include two clades representing hookeanskogo Nauchno-issledovatel’skogo Instituta Rybnogo the last two infraclasses. Ho (1990), Ho et al. (2003) and Khozyaistva i Okeanografii (TINRO), 102: 119-122. Blanco-Bercial et al. (2011) stated that Calanoida is the Bassett-Smith, P. W., 1898. Some new parasitic copepods found most basal taxon of Neocopepoda, and the sister-group of on fish at Bombay. Annals and Magazine of Natural History, Podoplea. This conclusion is in agreement with the pre- Series 7, 1: 1-17. sent results. Dahms (2004), Jenner (2009), and Schizas et al. Blanco-Bercial, L., Bradford-Grieve, J., and Bucklin, A., 2011. (2015) reported that Podoplea had been divided into two Molecular phylogeny of the Calanoida (Crustacea: Copepoda). main clades. The first clade is named ‘MHPSM-clade’, in- Molecular Phylogenetics and Evolution, 59: 103-113. Boxshall, G. A., 1979. The planktonic copepods of the north- cluding Thorell, 1859; Poecilostoma- eastern Atlantic Ocean: Harpacticoida, Siphonostomatoida and toida Thorell, 1859; Sars, 1901; Harpacticoi- Mormonilloida. Bulletin of the British Museum (Natural His- da Sars, 1903; Mormonilloida Boxshall, 1979. The second tory), Zoology, 35 (3): 201-264. is named as ‘MCG-clade’, comprising Cyclopoida Burmeis- Boxshall, G. A., and Halsey, S. H., 2004. An Introduction to ter, 1835; Gurney, 1933; and Gelyelloida Copepod Diversity. Part II. The Ray Society, London, 966pp. Huys, 1988. This phylogenetic classification has been ob- Brian, A., 1906. Copepodi parassiti dei Pesci d’Italia. Stab. Tipo- served herein. In fact, Harpacticoida is a basal-branch group Litografico R. Istituto Sordomuti, Genova, 1-191. of Podoplea and strongly linked to Cyclopoida, which has Brown, L., Bresnan, E., Graham, J., Lacaze, J. P., Turrell, E., and been accepted by Eyun (2017). The current study reveal- Collins, C., 2010. Distribution, diversity and toxin composi- ed the paraphyletic status of Cyclopoida, which is consis- tion of the genus Alexandrium (Dinophyceae) in Scottish wa- ters. European Journal of Phycology, 45: 375-393. tent with the results of Martínez-Arbizu (2000). Burmeister, H., 1835. Beschreibung einiger neuen oder weniger Previously, Dole-Olivier et al. (2000) and Kim and Moon bekannten Schmarotzerkrebse, nebst allgemeinen Betrachtun- (2013) reported that Cyclopoida is made up of more than gen über die Gruppe, welcher sie angehören. Nova Acta Phy- 12 families, 80 genera, and 450 marine species. In the pre- sico-Medica Academiae Caesareae Leopoldino-Carolinae Na- sent study, this order was expressed by 5 families, inclu- turae Curiosorum (Acta der Kaiserlichen Leopoldinisch-Caro- ding Taeniacanthidae, Bomolochidae, Cyclopettidae, Cyclo- linischen Deutschen Akademie der Naturforscher), Halle, 17 pidae, and Clausidiidae. In addition, our molecular analy- (1): 269-336. sis provided nodal support for a monophyletic bomolo- Cepeda, G. D., Blanco-Bercial, L., Bucklin, A., Berón, C. M., and chiform complex consisting of the first two very closely Viñas, M. D., 2012. Molecular systematic of three species of related families. It was based on the evidence gathered by (Copepoda, Cyclopoida) from the Atlantic Ocean: Comparative analysis using 28S rDNA. PLoS One, 7 (4): e35861. Ho et al. (2006) and Huys et al. (2012). Furthermore, this Claus, C., 1864. Beiträge zur Kenntniss der Schmarotzerkrebse. phylogeny has shown that the bomolochiform family and Zeigschrift für Wissenschaftliche Zoologie,, 14: 365-382. the Clausidiidae family form a monophyletic group, which Cressey, R. F., 1969. Five new parasitic copepods from Califor- is in agreement with the data obtained by Huys et al. (2012). nia inshore fish. Proceedings of the Biological Society of Wa- Herein, Taeniacanthidae includes three genera Taeniacan- shington, 82: 409-428. thus, Anchistrotos, and Pseudotaeniacanthus. By compa- Dahms, H. U., 2004. Exclusion of the Polyarthra from Harpac- ring 28S rRNA gene sequences, the species in this study ticoida and its reallocation as an underived branch of the Co-

ABDEL-GABER et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2020 19: 1409-1420 1419

pepoda (Arthropoda, Crustacea). Invertebrate Zoology, 1 (1): 582-594. 29-51. Ho, J. S., Ohtsuka, S., and Nakadachi, N., 2006. A new family of Devi, D. V. U., and Shyamasundari, K., 1980. Studies on the Co- poecilostomatoid copepods (Umazuracolidae) based on speci- pepod pararsites of fishes of the Waltair Coast: Family Tae- mens parasitic on the black scraper (Thamnaconus modestus) niacanthidae. Crustacea, 39 (2): 197-208. in Japan. Zoological Science, 23: 483-496. Dojiri, M., and Cressey, R. F., 1987. Revision of the Taeniacan- Huelsenbeck, J. P., and Ronquist, F., 2001. MrBayes: Bayesian thidae (Copepoda: ) parasitic on fishes and inference of phylogenetic trees. Bioinformatics, 17: 754-755. sea urchins. Smithsonian Contributions to Zoology, 447: 1-250. Humes, A. G., 1970. Clavisodalis heterocentroti gen. et sp. n., a Dojiri, M., and Humes, A. G., 1982. Copepods (Poecilostomata: cyclopoid copepod parasitic on an echinoid at Eniwetok Atoll. Taeniacanthidae) from sea urchins (Echinoidea) in the south- Journal of Parasitology, 56 (3): 575-583. west Pacific. Zoological Journal of the Linnean Society, 74: 381- Humes, A. G., and Cressey, R. F., 1961. Copepodes Taeniacan- 436. thides parasites d’un oursin a Madagascar. Memoirs de I'In- Dole-Olivier, M. J., Galassi, D. M. P., Marmonier, P., and Creu- stitut Scientifique de Madagascar, Series F, 3: 1-24. zé Des Châtelliers, M., 2000. The biology and ecology of lo- Huys, R., 1988. Gelyelloida, a New Order of Stygobiont Cope- tic microcrustaceans. Freshwater Biology, 44: 63-91. pods from European Karstic Systems. Boxshall, G. A., and Sch- Eyun, S. I., 2017. Phylogenomic analysis of Copepoda (Arthro- minke, H. K., eds., Springer Netherlands, 485-495. poda, Crustacea) reveals unexpected similarities with earlier Huys, R., and Boxshall, G. A., 1991. Copepod Evolution. The Ray proposed morphological phylogenies. BMC Evolutionary Bio- Society, London, 468pp. logy, 17: 23. Huys, R., Fatih, F., Ohtsuka, S., and Llewellyn-Hughes, J., 2012. Ferrari, F. D., and von Vaupel Klein, J. C., 2019 Rhabdomoplea, Evolution of the bomolochiform superfamily complex (Co- a new superorder for the thaumatopsylloid copepods: The con- pepoda: Cyclopoida): New insights from ssrDNA and morpho- sequence of an alternative hypothesis of copepod phylogeny. logy, and origin of umazuracolids from polychaete-infesting Crustaceana, 92: 177-188. ancestors rejected. International Journal for Parasitology, 42: Ferrari, F. D., Ivanenko, V. N., and Dahms, H. U., 2010. Body ar- 71-92. chitecture and relationships among basal copepods. Journal Huys, R., Llewellyn-Hughes, J., Conroy-Dalton, S., Olson, P. D., of Crustacean Biology, 30: 465-477. Spinks, J. N., and Johnston, D. A., 2007. Extraordinary host Fls, R. H., Llewellyn-Hughes, J., Olson, P. D., and Nagasawa, K., switching in siphonostomatoid copepods and the demise of 2006. Small subunit rDNA and Bayesian inference reveal Pec- the Monstrilloida: Integrating molecular data, ontogeny and tenophilus ornatus (Copepoda incertae sedis) as highly trans- antennulary morphology. Molecular Phylogenetics and Evo- formed , and support assignment of Chondracan- lution, 43: 368-378. thidae and Xarifiidae to Lichomolgoidea (Cyclopoida). Bio- Huys, R., Llewellyn-Hughes, J., Olson, P. D., and Nagasawa, K., logical Journal of the Linnean Society, 87: 403-425. 2006. Small subunit rDNA and Bayesian inference reveal Pec- Fosshagen, A., and Iliffe, T. M., 1985. Two new generea of Ca- tenophilus ornatus (Copepoda incertae sedis) as highly trans- lanoida and a new order of Copepoda, Platycopioida, from ma- formed Mytilicolidae, and support assignment of Chondra- rine caves on Bermuda. Sarsia, 70: 345-358. canthidae and Xarifiidae to Lichomolgoidea (Cyclopoida). Bio- Giesbrecht, W., 1892. Systematik und Faunistik der pelagischen logical Journal of the Linnean Society, 87: 403-425. Copepoden des Golfes von Neapel. Fauna Und Flora des Gol- Huys, R., Lopez-Gonzalez, P. J., Roldan, E., and Luque, A. A., fes von Neapel, 19: 1-831. 2002. Brooding in cocculiniform limpets (Gastropoda) and fa- Gurney, R., 1933. British Fresh-Water Copepoda. III. Cyclopoi- milial distinctiveness of the Nucellicolidae (Copepoda): Mis- da. Ray Society, London, 384pp. conceptions reviewed from a chitonophilid perspective. Bio- Hamza, F., Boxshall, G., and Kechemir-Issad, N., 2007. A new logical Journal of the Linnean Society, 75 (2): 187-217. species of Prohatschekia Nune-Ruivo, 1954 (Copepoda: Hat- Izawa, K., 1986. On the development of parasitic copepoda. III schekiidae) parasitic on Scorpaena elongata (Cadenat) of Al- Taeniacanthus lagocephali Pearse (Cyclopoida: Taeniacanthi- geria. Systematic Parasitology, 67: 119-124. dae). Publications of the Seto Marine Biological Laboratory, Hayward, C. J., Svane, I., Lachimpadi, S. K., Itoh, N., Bott, N., 31 (1): 37-54. and Nowak, B. F., 2011. Sea lice infections of wild fishes near Jenner, R. A., 2009. Higher-level crustacean phylogeny: Consen- ranched southern bluefin tuna (Thunnus maccoyii) in South sus and conflicting hypotheses. Structure & Deve- Australia. Aquaculture, 320: 178-182. lopment, 39 (2): 143-153. Ho, J. S., 1969. Copepods of the family Taeniacanthidae (Cyclo- Kim, I. H., and Moon, S. Y., 2013. Ten new species of parasitic poida) parasitic on fishes in the Gulf of Mexico. Bulletin of cycloopoid copepods (Crustacea) belonging to the families Bo- Marine Science, 19: 111-130. molochidae, Philichthyidae, and Taeniacanthidae from marine Ho, J. S., 1990. Phylogenetic analysis of copepod orders. Jour- fishes in Korea. Ocean Science Journal, 48 (4): 361-398. nal of Crustacean Biology, 10: 528-536. Kim, J., and Kim, W., 2000. Molecular phylogeny of poecilo- Ho, J. S., and Kim, I. H., 2001. New species of Hatschekia Po- stome copepods based on the 18S rDNA sequences. Korean che, 1902 (Copepoda: ) parasitic on marine fish- Journal of Biological Sciences, 4: 257-261. es of Kuwait. Systematic Parasitology, 49: 73-79. Krøyer, H., 1837. Om Snyltekrebsene, isaer med Hensyn til den Ho, J. S., and Lin, C. L., 2006. Two species of Makrostrotos gen. danske Fauna. Naturhistorisk Tidsskrift, 1 (2): 172-208. nov. (Copepoda: Taeniacanthidae) parasitic on the laced mo- Kumar, S., Stecher, G., and Tamura, K., 2016. MEGA7: Mole- ray (Gymnothorax favagineus Bloch and Schneider) in Tai- cular evolutionary genetics analysis version 7.0 for bigger wan. Zoological Studies, 45: 578-585. datasets. Molecular Biology and Evolution, 33: 1870-1874. Ho, J. S., Dojiri, M., Gordon, H., and Deets, G. B., 2003. A new Lang, K., 1948. Copepoda ‘Notodelphyoida’ from the Swedish species of Copepoda (Thaumatopsyllidae) symbiotic with a west-coast with an outline on the systematics of the Copepods. brittle star from California, USA, and designation of a new Arkiv för Zoologi, 40 (14): 1-36. order Thaumatopsylloida. Journal of Crustacean Biology, 23: Lewis, A. G., 1967. Copepod parasitic on teleost fishes

1420 ABDEL-GABER et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2020 19: 1409-1420

of the Hawaiian Islands. Proceedings of the United States Na- Australia. Folia Parasitologica, 58 (3): 233-239. tional Museum, 121: 1-204. Tang, D., and Izawa, K., 2005. Biacanthus pleuronichthydis (Ya- Martínez-Arbizu, P., 2000. The paraphyly of Sars, maguti, 1939) gen. n., comb. n. (Copepoda: Taeniacanthidae), 1913, and the phylogenetic position of poecilostome families and ectoparasite of flatfishes from Japanese waters. Zootaxa, within Cyclopoida Burmeister, 1835 (Copepoda: Crustacea). 1071: 47-60. PhD thesis. University of Oldenburg. Tang, D., and Johnston, M. D., 2005. Caudacanthus, a new ge- Pearse, A. S., 1952. Parasitic crustacea from the Texas Coast. Pub- nus for Caudacanthus narcini (Pillai, 1963) comb. nov. (Poe- lications of the Institute of Marine Science (University of Texas), cilostomatoida: Taeniacanthidae), a parasitic copepod of ba- 2: 5-42. toid fishes (Chondrichthyes: Elasmobrachii) from the Indo- Pillai, N. K., 1963. Copepods of the family Taeniacanthidae pa- West Pacific. Zoological Studies, 44: 337-346. rasitic on South Indian fishes. Crustaceana, 6: 110-128. Tang, D., Uyeno, D., and Nagasawa, K., 2011. Parasitic cope- Pritchard, M. H., and Kruse, G. O. W., 1982. The Collection and pods of the family Taeniacanthidae (Crustacea) from trigger- Preservation of Parasites. Technical Bulletin No. 1. Uni- fishes (Teleostei, Balistidae) and filefishes (Teleostei, Mona- versity of Nebraska Press, Lincoln, 141pp. canthidae) collected in the Indo-West Pacific region. Zootaxa, Ramdane, Z., 2009. Identification et écologie des ectoparasites 3103: 33-56. Crustacés des poissons Téléostéens de la côte Est algérienne. Tang, D., Uyeno, D., and Nagasawa, K., 2016. A review of the Thèse de doctorat de l’Université Badji Moktar Annaba, 235pp. Taeniacanthus balistae species group (Crustacea: Copepoda: Rangnekar, P. G., and Murti, N. N., 1960. Two new copepods Taeniacanthidae), with descriptions of two new species. Zo- from the fishes of Bombay. Journal of the University of Bom- otaxa, 4174 (1): 212-236. bay, 29 (3): 206-210. Thorell, T., 1859. Till Kannedomen om vissa parasitiskt lefvan- Ravichandran, S., Ajith Kumar, T. T., Ronald Ross, P., and Mu- de Entomostraceer. Ofvers. K. VetenskAkad. Forh Stockh, 16 thulingam, M., 2007. Histopathology of the infestation of pa- (8): 355-362. rasitic isopod Joryma tartoor of the host fish Parastromates Uyeno, D., Tang, D., and Nagasawa, K., 2013. Saging cebuana, niger. Research Journal of Parasitology, 2 (1): 68-71. a new genus and species of taeniacanthid copepod (Cyclo- Richiardi, S., 1870. Intorno ad una nuova specie del genere Bo- poida) parasitic on a filefish (Actinopterygii: Monacanthidae) molochus (B. ostracionis). Archivio per la Zoologia, I'Anato- collected from Cebu Island, the Phillippines. The Raffles Bul- mia e la Fisiologia, Series II, 11: 47-59. letin of Zoology, 61 (2): 515-523. Sars, G. O., 1901. Copepoda Calanoida. An Account of the Crus- Venmathi Maran, B. A., Moon, S. Y., Adday, T. K., and Tang, D., tacea of Norway with Short Descriptions and Figures of All 2016. Cepolacanthus kimi, a new genus and species of cope- the Species, 4: 1-28. pod (Cyclopoida: Taeniacanthidae) parasitic on bandfish Acan- Sars, G. O., 1903. An Account of the Crustacea of Norway, with thocepola abbreviata (Valenciennes, 1835) (Actinopterygii: Ce- Short Descriptions and Figures of all the Species Copepoda. polidae) caught off the Iraqi coast. Zootaxa, 4174: 249-258. Bergen Museum, Norway, 13-30. Vervoort, W., 1962. A review of the genera and species of the Schizas, N. V., Dahms, H. U., Kangtia, P., Corgosinho, P., and Ga- Bomolochidae (Crustacea, Copepoda), including the descrip- lindo, A. M., 2015. A new species of Claus, 1863 tion of some old and new species. Zoologische Verhandelin- (Copepoda: Harpacticoida: ) from Caribbean me- gen, 56: 1-111. sophotic reefs with remarks on the phylogenetic affinities of Walter, T. C., and Boxshall, G., 2019. World of Copepods Data- Polyarthra. Marine Biology Research, 11 (8): 789-803. base. http://www.marinespecies.org/copepoda on 2020-08-27, Sebastian, M. J., 1964. Taeniacanthus dentatus sp. nov., a cope- DOI: 10.14284/356. pod parasite of the fish Bembrops caudimaculata Steindach- Wilson, C. B., 1911. North American parasitic copepods belong- ner. Journal of the Marine Biological Association of India, 6 ing to the family Frgasilidae. Proceedings of the United States (1): 94-97. National Museum, 39: 263-400. Sewell, R. B. S., 1949. The littoral and semi-parasitic Cyclo- Wilson, C. B., 1924. New North American parasitic copepods, poida, Monstrilloida and Notodelphyoida. Scientific Reports new hosts, and notes on copepod nomenclature. Proceedings of the John Murray Expedition, 9 (2): 17-199. of the United States National Museum, 64: 1-22. Shiino, S. M., 1957. Copepods parasitic on Japanese fishes, 16: Wilson, C. B., 1935. Parasitic copepods from the Dry Tortugas. Bomolochidae and Taeniacanthidae. Report of the Faculty of Papers of the Tortugas Laboratory, 29: 327-347. Fisheries (Prefectural University of Mie), 2 (3): 411-428. Yamaguti, S., 1939. Parasitic copepods from fishes of Japan. Part Song, Y., Wang, G. T., Yao, W. J., Gao, G., and Nie, P., 2008. Phy- 5. Caligoida, III. Volumen Jubilare pro Professore Sadao Yoshi- logeny of freshwater parasitic copepods in the Ergasilidae da, 2: 443-487. (Copepoda: Poecilostomatoida) based on 18S and 28S rDNA Yamaguti, S., 1954. Parasitic copepods from fishes of Celebes sequences. Parasitological Research, 102 (2): 299-306. and Borneo. Publications of the Seto Marine Biological Labo- Sonnenberg, R., Nolte, A., and Tautz, D., 2007. An evaluation of ratory, 3 (3): 137-160. LSU rDNA D1-D2 sequences for their use in species identi- Yamaguti, S., and Yamasu, T., 1959. Parasitic copepods from fishes fication. Frontiers in Zoology, 4: 6. of Japan with descriptions of 26 new species and remarks on Sumpf, K., 1871. Über eine neue Bomolochiden Gattung nebst two known species. Biol Jour Okayama Univ, 5: 89-165. Bemerkungen über die Mundwerkzeuge der sogenannten Poe- Yazawa, R., Yasuike, M., Leong, J., von Schalburg, K. R., Cooper, cilostomen. Inaugural-Dissertation, Universität Göttingen, 32pp. G. A., Beetz-Sargent, M., Robb, A., Davidson, W. S., Jones, S. Tamura, K., and Nei, M., 1993. Estimation of the number of nu- R. M., and Koop, B. F., 2008. EST and mitochondrial DNA cleotide substitutions in the control region of mitochondrial sequences support a distinct pacific form of , DNA in humans and chimpanzees. Molecular Biology and Evo- salmonis. Marine Biotechnology, 10: 741-749. lution, 10: 512-526. Yeom, J., Nikitin, M. A., Ivanenko, V. N., and Lee, W., 2018. A Tang, D., 2011. A new species of Taeniacanthus (Copepoda: Tae- new minute ectosymbiotic harpacticoid copepod living on the niacanthidae) parasitic on two pufferfish species, Marilyna me- sea cucumber Eupentacta fraudatrix in the East/Japan Sea. raukensis and M. darwinii (Teleostei: Tetraodontidae), from Peer Journal, 6: e4979. (Edited by Qiu Yantao)