Syst Parasitol (2013) 86:271–283 DOI 10.1007/s11230-013-9451-6
Two new species of mazocraeid monogeneans from Clupanodon punctatus (Temminck & Schlegel) (Clupeiformes: Clupeidae) found in Daya Bay, South China Sea, with the proposal of Chelimazocraes n. g. Kai Yuan • Zhi Xiao • Xuejuan Ding Lin Liu
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Received: 11 March 2013 / Accepted: 19 September 2013 Ó Springer Science+Business Media Dordrecht 2013
Abstract Chelimazocraes liaoi n. g., n. sp. and Chelimazocraes ascidiformis n. sp. (Monogenea: Mazocraeidae) are described from the gills of Clupanodon punctatus (Temminck & Schlegel) in Daya Bay (South China Sea). The new genus is characterised by the following features: (i) the haptor is distinctly separated from the body proper, and the arrangement of the clamps is bilaterally symmetrical but longitudinally heteromorphic; (ii) the anterior three pairs of clamps are of the mazocraeid-type, whereas the fourth pair is of a non-mazocraeid type with three sclerites; (iii) all three pairs of clamps are similar in shape but their size gradually becomes smaller from the anterior to the posterior; (iv) the inner spines of the copulatory organ have a similar shape; and (v) the testes are numerous and arranged longitudinally posterior to the ovary. The two new species are easily distinguished from other members of the Mazocraeidae by the unique structure of the fourth pair of clamps; however, there are some noticeable differences between the two species. The major differences are as follows: (i) the body of C. liaoi n. sp. is significantly larger than that of C. ascidiformis
n. sp.; (ii) the anterior three pairs of clamps consist of different sclerites in the two species; and (iii) the copulatory organ has one pair of outer spines and 15–16 pieces of inner spines in C. liaoi n. sp. (vs two pairs of outer spines and 22–26 pieces of inner spines in C. ascidiformis n. sp.).
Introduction The family Mazocraeidae Price, 1936 consists of nearly 100 species worldwide belonging to 25 genera (Yamaguti, 1963; Unnithan, 1964; Mamaev, 1975, 1981, 1982a, b, 1984; Zhang et al., 2003a). During the past decade, only two additional species have been described within this family (Deepak & Gupta, 2007; Wu & Zhang, 2009). Off China, about 30 species of mazocraeid monogeneans from 12 genera have been reported, most parasitising clupeiform fishes (Zhang et al., 2003b; Wu & Zhang, 2009; Cao & Ding, 2010). In this study, two new species from Clupanodon punctatus (Temminck & Schlegel) are described and a new genus is proposed to accommodate them.
Materials and methods K. Yuan Z. Xiao X. Ding L. Liu (&) Key Laboratory of Ecology and Environmental Science in Guangdong Higher Education, College of Life Science, South China Normal University, Guangzhou 510631, China e-mail: [email protected]
Fishes were collected from Daya Bay in South China Sea and examined fresh. Parasites were picked off the gills with fine needles and processed as described by Zhang et al. (1997). Illustrations were made with the
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aid of a drawing apparatus. The clamps were treated with proteinase K (20 lg/ll, 30 min at room temperature) to separate the sclerites for examination. The nomenclature proposed by Mamaev (1981) was adopted to describe the morphology of the clamp sclerites: scleritum arcuatum anterius (SAA), scleritum antero-supplementarium (SAS), scleritum mediobasale (SMB), scleritum medio-supplementarium (SMS), scleritum postero-supplementarium (SPS), scleritum arcuatum posterius (SAP) and scleritum labiatum (SL). The four pairs of clamps were numbered consecutively starting with the anteriormost pair. The distances measured for haptoral hooks and copulatory spines are shown in Figs. 1 and 5. All measurements are in micrometres and are given as the range followed by the mean and the number of measurements in parentheses. Digestion of the fourth pair of clamps with proteinase K resulted in obtaining three pieces of sclerites. Since this is the first report of sclerites of this kind, we named the parts as scleritum arcuatum exterior (SAE), scleritum confibula interior (SCI) and scleritum obseratum superior (SOS) (Fig. 4). Family Mazocraeidae Price, 1936 Subfamily Mazocraeinae Price, 1936
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hamuli and one pair or none marginal hooklets. Intestinal caeca with diverticula, not extending into haptor, not confluent posteriorly. Testes numerous, postovarian, arranged in longitudinal rows. Copulatory organ with one or two pairs of outer spines and a number of inner spines of similar shape. Vaginal pore absent. Eggs fusiform, with single short filament on posterior pole. Parasites on gills of clupeoid fish. Typespecies: Chelimazocraes liaoi n. sp. Etymology: The generic name refers to the characteristic shape of the fourth pair of clamps, which are like a pair of chelicerae. Remarks The new genus is mainly characterised by its heteromorphic clamps: three anterior pairs with a similar mazocraeid-type structure and a fourth pair of a nonmazocraeid-type. All clamps are symmetrically arranged laterally in two rows on the haptor. Chelimazocraes n. g. can be distinguished from the other genera of the Mazocraeidae by the presence of chelicerae-like structures in the fourth pair of clamps.
Chelimazocraes liaoi n. sp. Chelimazocraes n. g. Diagnosis Mazocraeidae Price, 1936, Mazocraeinae Price, 1936. Haptor distinctly demarcated from body proper, with four pairs of clamps on short peduncles. Three anterior pairs of clamps of open mazocraeid-type, similar in shape, different in size, gradually become smaller starting from anterior to posterior. Clamps with five typical mazocraeid sclerites with different components among species. Fourth pair of clamps cheliceraeshaped, consists of three unique sclerites: scleritum arcuatum exterior (SAE), scleritum confibula interior (SCI), scleritum obseratum superior (SOS). SAE arched, with lower part inflated like spoon and upper end with a circular protuberance and a lateral bar on each side. SCI resembling ‘7’ in lateral view, with inflated lower part like a spoon with a big hole; upper end bifurcates into two fork-like parts. SAE and SCI fixed in their upper ends. SOS U-shaped, on SAE and SCI parts. Terminal lappet short, with two pairs of
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Type-host: Clupanodon punctatus (Temminck & Schlegel). Type-locality: Daya Bay (113°290 –114°490 E, 23°310 – 24°500 N), off Guangdong Province, South China Sea (22 August 2011; 18 September 2011; 15 October 2011; 20 February 2012; 11 March 2012; 14 April 2012). Other localities: Off Zhanjiang (109°310 –110°550 E, 20°–21°350 N), Guangdong Province, South China Sea (7 April 2009); off Sanya (108°560 –109°480 E, 18°090 – 18°370 N), Hainan Island, South China Sea (18 March 2012). Site: Gills. Type-material: Holotype (No. DYW2012022001) and paratypes (Nos DYW2012041401-04, DYW201203 1101-03, DYW2011082201-03, SY2012031801-03, and ZJ2009040701) are deposited in the Fish Parasite Laboratory, College of Life Science, South China Normal University, Guangzhou, China. Two paratypes are deposited in the British Museum (Natural
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Fig. 1 Chelimazocraes liaoi n. g., n. sp. A, Whole worm, ventral view; B, Copulatory organ; C, Hamuli and marginal hooklets (distances measured indicated by a–e); D, Haptor; E, Egg. Scale-bars: A, 1000 lm; B, 20 lm; C, 50 lm; D, 500 lm; E, 100 lm
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History) Collection at the Natural History Museum, London (BMNH 2013.8.9.3; BMNH 2013.8.9.4). Etymology: The species is named after the late Professor Xianghua Liao, the famous Chinese specialist on fish helminths. Description (Figs. 1–3, 4A–C) [Based on 21 specimens; measurements from 10 specimens]. Body elongate, lanceolate, tapering gradually towards anterior and posterior extremities; total
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length 3,400–6,050 (4,099; n = 10); width at ovary level 300–770 (477; n = 10). Buccal suckers 2, circular, septate at anterior end, 63–85 (71; n = 7) in diameter. Pharynx oval, 38–53 (46; n = 8) 9 30–40 (36; n = 8); oesophagus 250–638 (341; n = 10) long, bifurcates into 2 intestinal caeca at level of genital atrium. Caeca with many lateral branches, not confluent posteriorly, extend up to level of first pair of clamps, but not into haptor (Figs. 1A, 2A). Haptor almost triangular, distinctly demarcated from body proper, 300–570 (457; n = 9) long,
Fig. 2 Chelimazocraes liaoi n. g., n. sp. A, Whole worm, ventral view; B, Copulatory organ; C, Posterior part of the haptor (fourth pair of clamps shown); D, Anterior clamp; E, Haptor. Scale-bars: A, 1000 lm; B, 20 lm; C, 100 lm; D, 50 lm; E, 300 lm
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250–450 (361; n = 9) wide at level of first pair of clamps, narrows abruptly after third pair of clamps. Four pairs of clamps, each with short peduncle, arranged symmetrically in 2 lateral rows (Figs. 1D, 2E). Anterior 3 pairs of clamps of mazocraeid open-type, similar in shape, slightly different in size: first pair 65–120 (87; n = 16) 9 75–175 (109; n = 16); second pair 65–115 (85; n = 16) 9 80–168 (102; n = 16); third pair 68–133 (82; n = 14) 9 75–140 (93; n = 14); each clamp with 5 sclerites: SAA, SAS, SMB, SMS and SL (Figs. 2D, 3). Fourth pair of clamps with 3 sclerites (Figs. 2C, 4) different from those in the 3 anterior pairs, 75–158 (98; n = 20) 9 38–88 (50; n = 20). Posterior appendage small, 63–125 (101; n = 9) 9 44–103 (77; n = 9), armed with 2 pairs of hamuli and 1 pair of marginal hooklets (Fig. 1C). Outer hamuli larger, broad at base, with median spur and pointed tip, with measurements: a, 55–65 (60; n = 15); b, 38–45 (41; n = 18); c, 10–15 (13; n = 18); d, 15–20 (17; n = 15); e, 8–18 (11; n = 15). Inner pair of hamuli small, each with curved tip and short handle, 25–28 (26; n = 12) long. Marginal hooklets smallest, 20–25 (23; n = 4) long.
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Testes numerous, oval, 15–25 in number, arranged in 2 or 3 longitudinal rows; testicular region 750–1,510 (1,107; n = 7) long, occupies onefourth of body length; anterior testes larger than posterior. Male copulatory organ located near intestinal bifurcation, 38–45 (43; n = 7) 9 35–40 (38; n = 7), at 343–705 (446; n = 9) from anterior extremity of body, armed with 9 pairs of homomorphic genital spines on muscular pad. Outer pair of spines slightly larger, 10–13 (11; n = 12) long. Fifteen or 16 inner spines 5–10 (7; n = 20) long, arranged in 2 longitudinal rows, 8 and 7–8 on each side (Figs. 1B, 2B). Ovary elongate, pretesticular, folds terminally at mid-body. Vitellarium follicular, extends from anterior of copulatory organ to ends of intestinal caeca, not into haptor. Vitelline reservoir Y-shaped. Uterus extends anteriorly, opens into genital atrium; single egg often observed in uterus. Eggs large, fusiform, with single filament at posterior pole, 243–338 (281; n = 3) long (excluding filament) and 65–70 (68; n = 3) wide (Fig. 1E). Vaginal pore absent.
Fig. 3 Chelimazocraes liaoi n. g., n. sp. Anterior three pairs of clamps and their sclerites. Scale-bar: 50 lm
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Fig. 4 Sclerites of the fourth pair of clamps in Chelimazocraes liaoi n. g., n. sp. (A–C) and C. ascidiformis n. sp. (D, E). A, Cross-shape of the fourth clamp; B, SOS; C, SAE; D, E, SCI from different views. Scale-bars: A, C, D, E, 30 lm; B, 20 lm
Chelimazocraes ascidiformis n. sp. Type-host: Clupanodon punctatus (Temminck & Schlegel). Type-locality: Daya Bay (113°290 –114°490 E, 23°310 – 24°500 N), South China Sea (31 March 2009; 22 August 2011; 20 September 2011; 15 October 2011; 24 November 2011; 20 February 2012; 14 April, 2012). Site: Gills. Type-material: Holotype (No. DYW2012041401) and paratypes (Nos DYW2009033101, DYW2012041402, DYW2011112401-04, DYW2012022001-03, DYW201 1101501-02, and DYW2011082201) are deposited in the
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Fish Parasite Laboratory, College of Life Science, South China Normal University, Guangzhou, China. Two paratypes are deposited in the British Museum (Natural History) Collection at the Natural History Museum, London (BMNH 2013.8.9.1-2). Etymology: The specific name is derived from the coca-cola bottle shaped body. Description (Figs. 4D, E, 5–7) [Based on 26 specimens; measurements from 10 specimens]. Body bottle-shaped, thick, narrows gradually towards anterior extremity, 1,550–2,810 (2,080;
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n = 10) 9 290–550 (394; n = 10). Buccal suckers 2, semi-circular, aseptate, 25–50 (46; n = 8) 9 50–98 (77; n = 8). Pharynx oval, 48–65 (57; n = 8) 9 38–50 (43; n = 8); oesophagus divides into 2 intestinal caeca posterior to copulatory organ. Caeca with lateral diverticula, not confluent posteriorly, extend into haptor (Figs. 5A, 6A).
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Haptor cordiform, demarcated from body proper by distinct constriction, relatively large, 320–520 (428; n = 10) 9 230–450 (384; n = 10), narrows abruptly after third pair of clamps. Four pairs of clamps, each with short peduncle, arranged symmetrically along haptoral margins (Fig. 6E). Anterior 3 pairs similar in shape, smaller in size: first pair 75–113 (98;
Fig. 5 Chelimazocraes ascidiformis n. sp. A, Whole worm, ventral view; B, Copulatory organ; C, Lateral spines of the copulatory organ; D, Measurements of the copulatory spines (D1, D2, lateral spines; D3 median spine); E, Hamuli; F, Egg. Scale-bars: A, 500 lm; B, E, 50 lm; C, 10 lm; F, 100 lm
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Fig. 6 Chelimazocraes ascidiformis n. sp. A, Whole worm, ventral view; B, Copulatory organ; C, Posterior part of the haptor (fourth pair of clamps shown); D, Anterior clamp; E, Haptor. Scale-bars: A, 500 lm; B, D, 50 lm; C, 100 lm; E, 200 lm
n = 20) 9 68–113 (91; n = 20); second pair 73–100 (85; n = 20) 9 53–90 (75; n = 20); third pair 50–75 (58; n = 20) 9 45–65 (53; n = 20); each clamp consisting of 5 sclerites: SAA, SMB (petaliform with 3 lobes), SMS, SPS, and SAP (Figs. 6D, 7). Fourth pair of clamps with 3 sclerites, distinct from those in the 3 anterior pairs (Figs. 4, 6C), 65–75 (73; n = 20) 9 38–48 (41; n = 20). Posterior appendage small, 50–163 (93; n = 10) 9 45–125 (96; n = 9), armed with 2 pairs of hamuli. Outer hamuli larger, with developed inner and outer roots, with measurements: a, 55–65 (62; n = 11); b, 35–40 (38; n = 11); c, 10–13 (11; n = 9);
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d, 18–25 (22; n = 9); e, 8–15 (10; n = 8). Inner pair of hamuli small, each with curved tip and straight handle, 18–25 (21; n = 10) long (Fig. 5E). Testes numerous, 23–50 in number, arranged in several longitudinal rows. Male copulatory organ almost circular, 56–100 (81; n = 6) 9 75–100 (84; n = 6), at 250–550 (394; n = 10) from anterior extremity of body, armed with 2 pairs of differently shaped outer spines and 22–26 similarly shaped inner spines (Figs. 5B, 6B). Inner spines arranged circularly, with curved tip and flat base, with measurements: a, 8–13 (9; n = 6); b, 8–10 (10; n = 8) (see D3 in Fig. 5D). Outer spines 2 pairs, heteromorphic, one
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Fig. 7 Chelimazocraes ascidiformis n. sp. Ventral view of the anterior clamp and its sclerites. Complete structures of the sclerites from SAA and SAP are shown, observed after digestion with Proteinase K. Scale-bar: 50 lm
funnel-shaped, with measurements: a, 30–33 (32; n = 3); b, 18–20 (19; n = 3); the other sickle-shaped, with measurements: a, 10–13 (12; n = 4); b, 15–20 (18; n = 6); c, 10–13 (12; n = 2); d, 20 (n = 2) (see Fig. 5C and D1, D2 in Fig. 5D). Ovary S-shaped, pretesticular, not easily identifiable. Vitellarium follicular, extends from copulatory organ to ends of intestinal caeca, sometimes into haptor. Eggs oval, with single short, thick filament at posterior pole, 163–180 (173; n = 3) long (excluding filament) and 63–120 (92; n = 3) wide (Fig. 5F). Vaginal pore absent. Remarks The two new species are easily distinguished from all previously known mazocraeid species by the unique structure of the fourth pair of clamps. No differences were observed in the structure of the sclerites of the fourth pair of clamps between the two new species,
although their size is different. Three of the sclerites namely the SCI, SAE and SOS, could be clearly identified after proteinase K digestion from the fourth pair of clamps. Although their function remains unknown, this is the first report of a clamp structure of this type. Noticeable differences observed between the two species are shown in Table 1.
Discussion Species of Chelimazocraes n. g. are characterised largely by the structure of the sclerites in the fourth pair of clamps. Thus far, all clamps of the mazocraeid species have been reported to be of the mazocraeidtype, with 5 to 8 sclerites which differ in structure between the different species. In addition to the anterior three pairs of clamps with a normal mazocraeid-type structure, species of Chelimazocraes n. g. also have a non-mazocraeid-type clamp with only
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Table 1 Comparison of the main features of the two species of Chelimazocraes n. g
Body
Haptor
Chelimazocraes liaoi n. sp.
Chelimazocraes ascidiformis n. sp.
Lanceolate, large
Bottle-shaped, small
3,400–6,050 9 300–770
1,550–2,810 9 290–550
(4,099 9 477)* 300–570 9 250–450 (457 9 361)
(2,080 9 394) 320–520 9 230–450 (428 9 384)
Demarcated by a slight constriction from body proper; three anterior pairs of clamps slightly smaller
Demarcated by a distinct constriction from body proper; three anterior pairs of clamps distinctly smaller
SAA, SAS, SMB (cross-shaped), SMS, SL
SAA, SMB (petaliform with 3 lobes), SMS, SPS, SAP 75–113 9 68–113 (98 9 91)
Sclerites of first three pairs of clamps First pair of clamps
65–120 9 75–175 (87 9 109)
Second pair of clamps
65–115 9 80–168 (85 9 102)
73–100 9 53–90 (85 9 75)
Third pair of clamps
68–133 9 75–140 (82 9 93)
50–75 9 45–65 (58 9 53)
Fourth pair of clamps
75–158 9 38–88 (98 9 50)
65–75 9 38–48 (73 9 41)
Copulatory organ
38–45 9 35–40 (43 9 38)
56–100 9 75–100 (81 9 84)
15–16 median spines in two longitudinal rows
22–26 median spines in a circle
Buccal suckers
Two, circular, septate
One, aseptate
Egg
243–338 9 65–70 (281 9 68)
163–180 9 63–120 (173 9 92)
Terminal lappet
Two pairs of hamuli and one pair of hooklets; outer hamuli with broad base
Two pairs of hamuli; outer hamuli with slender base
*Metrical data are given as the range (in micrometres) followed by the mean in parentheses
three unique sclerites which resemble chelicerae (Fig. 4). Chelimazocraes is proposed based on the presence of this new feature. The two species of Chelimazocraes n. g. were found to parasitise the gills of marine clupeoid fishes, the rates of infection being estimated as less than 5% and infection intensities as c.1–3 worms per host. Interestingly, both species always co-occurred with Mazocraeoides gonialosae Tripathi, 1959 and Neomazocraes dorsomatis (Yamaguti, 1938) Price, 1943, which had higher infection intensities (our unpublished data). The three anterior pairs of clamps are similar in structure but differ in size, with the first pair being the largest in Chelimazocraes spp. This feature is similar in species of Pseudoanthocotyloides Price, 1959 and Pseudoanthocotyle Bychowsky & Nagibina, 1954, in which the first pair of clamps is significantly larger than the remaining pairs. In Chelimazocraes spp., however, the anterior three pairs of clamps gradually decrease in size towards the posterior end of the body. The shape of the SMB is also regarded as a distinguishing feature of mazocraeid genera. For example, the SMB is perforated in species of
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Cribromazocraes Mamaev, 1981, but H-shaped in species of Neomazocraes Price, 1934. In Chelimazocraes spp., the SMB is cross-shaped with two protruding flanks in C. liaoi n. sp. and three petaliform-like lobes in C. ascidiformis n. sp. Several perforations are present on the SMB in both species of Chelimazocraes, and this is similar to that in Pseudoanthocotyle pavlovskyi Bychowsky & Nagibina, 1954. The clamp sclerite SAS was absent in C. ascidiformis, which is similar to members of Neomazocraes Price, 1934. This suggests that Chelimazocraes spp. have a similar clamp structure and arrangement to species of Pseudoanthocotyloides, Pseudoanthocotyle and Neomazocraes. Haptoral characteristics and clamp variations are important features that are used to distinguish mazocraeid genera. Although in species of Mazocraeoides Price, 1936, Pseudomazocraeoides Price, 1961, and Reimericotyle Mamaev, 1984, the haptor is not obviously developed and the clamps are located along the body (Fig. 8A), in most other genera the haptor is well developed at the posterior end of the body and the clamps are arranged on the haptor. However, the rank, number, structure and size of the clamps vary in
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Fig. 8 Diagrammatic illustration showing haptoral characteristics and clamp variations in 26 genera of Mazocraeidae. A, Haptor not developed and clamps located along the body (Mazocraeoides, Pseudomazocraeoides and Reimericotyle); B, Four pairs of clamps with similar size and structure arranged symmetrically on the haptor (Anchovicola, Clupeocotyle, Cribromazocraes, Kuhnia, Leptomazocraes, Mazocraes, Neomazocraes, Ophicotyle, Paramazocraes and Pseudokuhnia); C, First pair of clamps the largest, the other three pairs of similar size (Pseudoanthocotyle, Pseudoanthocotyloides, Scomberocola and Taurimazocraes); D, Two anterior pairs of clamps significantly larger than the two posterior pairs (Etrumeicotyle and Neoclupeocotyle); E, Fourth pair of clamps with a unique structure (Chelimazocraes n. g.); F, Only one small clamp on one side of the haptor (Grubea); G, Four clamps on one side, larger than the opposite ones (Neogrubea and Paragrubea); H, Two large clamps on one side with different sclerites (Heteromazocraes and Heterocotyle); I, Three large clamps on one side with different sclerites (Sinomazocraes)
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different genera. Most mazocraeid species are armed with four pairs of clamps, which are similar in size and structure, and have a bilaterally symmetrical arrangement in species of at least 10 genera, including Anchovicola Unnithan, 1964, Clupeocotyle Hargis, 1955, Cribromazocraes Mamaev, 1981, Kuhnia Sproston, 1945, Leptomazocraes Mamaev, 1975, Mazocraes Hermann, 1782 Neomazocraes Price, 1934, Ophicotyle van Beneden & Hesse, 1863, Paramazocraes Tripathi, 1959 and Pseudokuhnia Rohde & Watson, 1985 (Fig. 8B). In four genera, the most anterior pair of clamps is the largest, whereas the other three pairs of clamps are of a similar size (Pseudoanthocotyle Bychowsky & Nagibina, 1954, Pseudoanthocotyloides Price, 1959, Scomberocola Unnithan, 1964 and Taurimazocraes Mamaev, 1982) (Fig. 8C). In species of Etrumeicotyle Mamaev, 1981 and Neoclupeocotyle Price, 1961, the two anterior pairs of clamps are significantly larger than the two posterior pairs (Fig. 8D). However, in the species of Chelimazocraes, although clamps are arranged bilaterally and symmetrically, they differ in both the size and structure of the clamps, which exhibit great variation (Fig. 8E). Clamps may also be arranged asymmetrically and bilaterally on the haptor. In species of Grubea Diesing, 1858, four large clamps of a similar size are located on one side of the haptor, whereas only a single small one is on the other (Fig. 8F), and, in species of Neogrubea Dillon & Hargis, 1968 and Paragrubea Mamaev, 1982, four small clamps are present on the opposite side but the clamp structure on both sides is similar (Fig. 8G). However, in species of Heteromazocraes Mamaev, 1981 and Heterocotyle Unnithan, 1964, the two large clamps on one side have component sclerites that are different from the two small clamps on the same side and the four clamps on the other side; in fact, the latter six clamps have similar sclerites (Fig. 8H). Similarly, in the species of Sinomazocraes Zhang, Liu, Fang & Ding, 2003, three large clamps on one side have component sclerites that are different from both the fourth small clamp on the same side and the four clamps on the other side; the latter five clamps have similar sclerites (Fig. 8I). It appears that, if two or three large clamps are present on one side, then their structure is different from that of the small clamps. It is possible that a species with only one large clamp on one side may exist, but this has not been seen. Whether
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the differences in clamps are related to the nature of the host or to other factors has yet to be determined. Acknowledgements This work was supported by the National Natural Science Fund of China (Nos. 31093430, 31172051). We would like to thank Dr David I. Gibson of the Natural History Museum, London, for his great help with literature and suggestions. We are grateful to Prof. Jianying Zhang for his comments on the manuscript. We owe a lot to Drs Aneta Kostadinova and David Gibson who helped to improve the English of the manuscript.
References Cao, S. M., & Ding, X. J. (2010). Monogenea of Chinese marine fishes XX.: a new Chinese record of genus Grubea. Journal of South China Normal University, 2, 105–106 (In Chinese). Deepak, K. D., & Gupta, V. (2007). Report of a new species, Paramazocraes lutjanusi n. sp. from the gills of marine fish, Lutjanus johnii (Cuv. and Val.) from Puri coast India. Flora and Fauna (Jhansi), 13, 363–366. Mamaev, Y. L. (1975). [Monogeneans of clupeiform fishes from the South China Sea (Mazocraeidae and Diclidophoroidea).] Trudy Biologo-Pochvennogo Instituta, Vladivostok, 26, 102–114 (In Russian). Mamaev, Y. L. (1981). Some new monogenean species and genera of the family Mazocraeidae. Helminthologia, 18, 169–187. Mamaev, Y. L. (1982a). [Monogeneans of the subfamily Grubeinae price, 1961 (Family Mazocraeidae).] Parazitologiya, 16, 457–463 (In Russian). Mamaev, Y. L. (1982b). Notes on the systematics of mazocraeid monogeneans with a redescription of some poorly studied taxa. Helminthologia, 19, 25–39. Mamaev, Y. L. (1984). On the specific composition and morphological characteristics of the genus Pseudomazocraeoides (Monogenea, Mazocraeidae). Angewandte Parasitologie, 25, 26–32. Unnithan, R. V. (1964). On five new species of monogenetic trematodes parasitic on the gills of marine fishes from the south west coast of India. Treubia, 26, 159–178. Wu, X. M., & Zhang, J. Y. (2009). Study on Monogenea of Chinese marine fishes: one new species of the genus Grubea (Mazocraeidae, Grubeinae) from Guangdong, China. Journal of South China Normal University, 4, 97–99 (In Chinese). Yamaguti, S. (1963). Systema helminthum. Vol. IV. Monogenea and Aspidocotylea. New York: Interscience Division, John Wiley & Sons, 699 pp. Zhang, J. Y., Liu, L., & Ding, X. J. (1997). Monogenea of Chinese marine fishes. VII. A new species and two new records of the Tetronchoididae from fishes of the South China and East China Seas. Systematic Parasitology, 38, 197–201. Zhang, J. Y., Liu, L., Fang, J. P., & Ding, X. J. (2003a). Monogenea from the middle Yangtze Valley: Sinomazocraes
Syst Parasitol (2013) 86:271–283 changjiangensis n. g., n. sp. (Family Mazocraeidae Price, 1936) on a clupeiform fish from Hubei Province, China. Systematic Parasitology, 54, 103–109.
283 Zhang, J. Y., Yang, T. B., Liu, L., & Ding, X. J. (2003b). A list of monogeneans from Chinese marine fishes. Systematic Parasitology, 54, 111–130.
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Two new species of mazocraeid monogeneans from Clupanodon punctatus (Temminck & Schlegel) (Clupeiformes: Clupeidae) found in Daya Bay, South China Sea, with the proposal of Chelimazocraes n. g. Kai Yuan • Zhi Xiao • Xuejuan Ding Lin Liu
•
Received: 11 March 2013 / Accepted: 19 September 2013 Ó Springer Science+Business Media Dordrecht 2013
Abstract Chelimazocraes liaoi n. g., n. sp. and Chelimazocraes ascidiformis n. sp. (Monogenea: Mazocraeidae) are described from the gills of Clupanodon punctatus (Temminck & Schlegel) in Daya Bay (South China Sea). The new genus is characterised by the following features: (i) the haptor is distinctly separated from the body proper, and the arrangement of the clamps is bilaterally symmetrical but longitudinally heteromorphic; (ii) the anterior three pairs of clamps are of the mazocraeid-type, whereas the fourth pair is of a non-mazocraeid type with three sclerites; (iii) all three pairs of clamps are similar in shape but their size gradually becomes smaller from the anterior to the posterior; (iv) the inner spines of the copulatory organ have a similar shape; and (v) the testes are numerous and arranged longitudinally posterior to the ovary. The two new species are easily distinguished from other members of the Mazocraeidae by the unique structure of the fourth pair of clamps; however, there are some noticeable differences between the two species. The major differences are as follows: (i) the body of C. liaoi n. sp. is significantly larger than that of C. ascidiformis
n. sp.; (ii) the anterior three pairs of clamps consist of different sclerites in the two species; and (iii) the copulatory organ has one pair of outer spines and 15–16 pieces of inner spines in C. liaoi n. sp. (vs two pairs of outer spines and 22–26 pieces of inner spines in C. ascidiformis n. sp.).
Introduction The family Mazocraeidae Price, 1936 consists of nearly 100 species worldwide belonging to 25 genera (Yamaguti, 1963; Unnithan, 1964; Mamaev, 1975, 1981, 1982a, b, 1984; Zhang et al., 2003a). During the past decade, only two additional species have been described within this family (Deepak & Gupta, 2007; Wu & Zhang, 2009). Off China, about 30 species of mazocraeid monogeneans from 12 genera have been reported, most parasitising clupeiform fishes (Zhang et al., 2003b; Wu & Zhang, 2009; Cao & Ding, 2010). In this study, two new species from Clupanodon punctatus (Temminck & Schlegel) are described and a new genus is proposed to accommodate them.
Materials and methods K. Yuan Z. Xiao X. Ding L. Liu (&) Key Laboratory of Ecology and Environmental Science in Guangdong Higher Education, College of Life Science, South China Normal University, Guangzhou 510631, China e-mail: [email protected]
Fishes were collected from Daya Bay in South China Sea and examined fresh. Parasites were picked off the gills with fine needles and processed as described by Zhang et al. (1997). Illustrations were made with the
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aid of a drawing apparatus. The clamps were treated with proteinase K (20 lg/ll, 30 min at room temperature) to separate the sclerites for examination. The nomenclature proposed by Mamaev (1981) was adopted to describe the morphology of the clamp sclerites: scleritum arcuatum anterius (SAA), scleritum antero-supplementarium (SAS), scleritum mediobasale (SMB), scleritum medio-supplementarium (SMS), scleritum postero-supplementarium (SPS), scleritum arcuatum posterius (SAP) and scleritum labiatum (SL). The four pairs of clamps were numbered consecutively starting with the anteriormost pair. The distances measured for haptoral hooks and copulatory spines are shown in Figs. 1 and 5. All measurements are in micrometres and are given as the range followed by the mean and the number of measurements in parentheses. Digestion of the fourth pair of clamps with proteinase K resulted in obtaining three pieces of sclerites. Since this is the first report of sclerites of this kind, we named the parts as scleritum arcuatum exterior (SAE), scleritum confibula interior (SCI) and scleritum obseratum superior (SOS) (Fig. 4). Family Mazocraeidae Price, 1936 Subfamily Mazocraeinae Price, 1936
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hamuli and one pair or none marginal hooklets. Intestinal caeca with diverticula, not extending into haptor, not confluent posteriorly. Testes numerous, postovarian, arranged in longitudinal rows. Copulatory organ with one or two pairs of outer spines and a number of inner spines of similar shape. Vaginal pore absent. Eggs fusiform, with single short filament on posterior pole. Parasites on gills of clupeoid fish. Typespecies: Chelimazocraes liaoi n. sp. Etymology: The generic name refers to the characteristic shape of the fourth pair of clamps, which are like a pair of chelicerae. Remarks The new genus is mainly characterised by its heteromorphic clamps: three anterior pairs with a similar mazocraeid-type structure and a fourth pair of a nonmazocraeid-type. All clamps are symmetrically arranged laterally in two rows on the haptor. Chelimazocraes n. g. can be distinguished from the other genera of the Mazocraeidae by the presence of chelicerae-like structures in the fourth pair of clamps.
Chelimazocraes liaoi n. sp. Chelimazocraes n. g. Diagnosis Mazocraeidae Price, 1936, Mazocraeinae Price, 1936. Haptor distinctly demarcated from body proper, with four pairs of clamps on short peduncles. Three anterior pairs of clamps of open mazocraeid-type, similar in shape, different in size, gradually become smaller starting from anterior to posterior. Clamps with five typical mazocraeid sclerites with different components among species. Fourth pair of clamps cheliceraeshaped, consists of three unique sclerites: scleritum arcuatum exterior (SAE), scleritum confibula interior (SCI), scleritum obseratum superior (SOS). SAE arched, with lower part inflated like spoon and upper end with a circular protuberance and a lateral bar on each side. SCI resembling ‘7’ in lateral view, with inflated lower part like a spoon with a big hole; upper end bifurcates into two fork-like parts. SAE and SCI fixed in their upper ends. SOS U-shaped, on SAE and SCI parts. Terminal lappet short, with two pairs of
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Type-host: Clupanodon punctatus (Temminck & Schlegel). Type-locality: Daya Bay (113°290 –114°490 E, 23°310 – 24°500 N), off Guangdong Province, South China Sea (22 August 2011; 18 September 2011; 15 October 2011; 20 February 2012; 11 March 2012; 14 April 2012). Other localities: Off Zhanjiang (109°310 –110°550 E, 20°–21°350 N), Guangdong Province, South China Sea (7 April 2009); off Sanya (108°560 –109°480 E, 18°090 – 18°370 N), Hainan Island, South China Sea (18 March 2012). Site: Gills. Type-material: Holotype (No. DYW2012022001) and paratypes (Nos DYW2012041401-04, DYW201203 1101-03, DYW2011082201-03, SY2012031801-03, and ZJ2009040701) are deposited in the Fish Parasite Laboratory, College of Life Science, South China Normal University, Guangzhou, China. Two paratypes are deposited in the British Museum (Natural
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Fig. 1 Chelimazocraes liaoi n. g., n. sp. A, Whole worm, ventral view; B, Copulatory organ; C, Hamuli and marginal hooklets (distances measured indicated by a–e); D, Haptor; E, Egg. Scale-bars: A, 1000 lm; B, 20 lm; C, 50 lm; D, 500 lm; E, 100 lm
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History) Collection at the Natural History Museum, London (BMNH 2013.8.9.3; BMNH 2013.8.9.4). Etymology: The species is named after the late Professor Xianghua Liao, the famous Chinese specialist on fish helminths. Description (Figs. 1–3, 4A–C) [Based on 21 specimens; measurements from 10 specimens]. Body elongate, lanceolate, tapering gradually towards anterior and posterior extremities; total
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length 3,400–6,050 (4,099; n = 10); width at ovary level 300–770 (477; n = 10). Buccal suckers 2, circular, septate at anterior end, 63–85 (71; n = 7) in diameter. Pharynx oval, 38–53 (46; n = 8) 9 30–40 (36; n = 8); oesophagus 250–638 (341; n = 10) long, bifurcates into 2 intestinal caeca at level of genital atrium. Caeca with many lateral branches, not confluent posteriorly, extend up to level of first pair of clamps, but not into haptor (Figs. 1A, 2A). Haptor almost triangular, distinctly demarcated from body proper, 300–570 (457; n = 9) long,
Fig. 2 Chelimazocraes liaoi n. g., n. sp. A, Whole worm, ventral view; B, Copulatory organ; C, Posterior part of the haptor (fourth pair of clamps shown); D, Anterior clamp; E, Haptor. Scale-bars: A, 1000 lm; B, 20 lm; C, 100 lm; D, 50 lm; E, 300 lm
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250–450 (361; n = 9) wide at level of first pair of clamps, narrows abruptly after third pair of clamps. Four pairs of clamps, each with short peduncle, arranged symmetrically in 2 lateral rows (Figs. 1D, 2E). Anterior 3 pairs of clamps of mazocraeid open-type, similar in shape, slightly different in size: first pair 65–120 (87; n = 16) 9 75–175 (109; n = 16); second pair 65–115 (85; n = 16) 9 80–168 (102; n = 16); third pair 68–133 (82; n = 14) 9 75–140 (93; n = 14); each clamp with 5 sclerites: SAA, SAS, SMB, SMS and SL (Figs. 2D, 3). Fourth pair of clamps with 3 sclerites (Figs. 2C, 4) different from those in the 3 anterior pairs, 75–158 (98; n = 20) 9 38–88 (50; n = 20). Posterior appendage small, 63–125 (101; n = 9) 9 44–103 (77; n = 9), armed with 2 pairs of hamuli and 1 pair of marginal hooklets (Fig. 1C). Outer hamuli larger, broad at base, with median spur and pointed tip, with measurements: a, 55–65 (60; n = 15); b, 38–45 (41; n = 18); c, 10–15 (13; n = 18); d, 15–20 (17; n = 15); e, 8–18 (11; n = 15). Inner pair of hamuli small, each with curved tip and short handle, 25–28 (26; n = 12) long. Marginal hooklets smallest, 20–25 (23; n = 4) long.
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Testes numerous, oval, 15–25 in number, arranged in 2 or 3 longitudinal rows; testicular region 750–1,510 (1,107; n = 7) long, occupies onefourth of body length; anterior testes larger than posterior. Male copulatory organ located near intestinal bifurcation, 38–45 (43; n = 7) 9 35–40 (38; n = 7), at 343–705 (446; n = 9) from anterior extremity of body, armed with 9 pairs of homomorphic genital spines on muscular pad. Outer pair of spines slightly larger, 10–13 (11; n = 12) long. Fifteen or 16 inner spines 5–10 (7; n = 20) long, arranged in 2 longitudinal rows, 8 and 7–8 on each side (Figs. 1B, 2B). Ovary elongate, pretesticular, folds terminally at mid-body. Vitellarium follicular, extends from anterior of copulatory organ to ends of intestinal caeca, not into haptor. Vitelline reservoir Y-shaped. Uterus extends anteriorly, opens into genital atrium; single egg often observed in uterus. Eggs large, fusiform, with single filament at posterior pole, 243–338 (281; n = 3) long (excluding filament) and 65–70 (68; n = 3) wide (Fig. 1E). Vaginal pore absent.
Fig. 3 Chelimazocraes liaoi n. g., n. sp. Anterior three pairs of clamps and their sclerites. Scale-bar: 50 lm
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Fig. 4 Sclerites of the fourth pair of clamps in Chelimazocraes liaoi n. g., n. sp. (A–C) and C. ascidiformis n. sp. (D, E). A, Cross-shape of the fourth clamp; B, SOS; C, SAE; D, E, SCI from different views. Scale-bars: A, C, D, E, 30 lm; B, 20 lm
Chelimazocraes ascidiformis n. sp. Type-host: Clupanodon punctatus (Temminck & Schlegel). Type-locality: Daya Bay (113°290 –114°490 E, 23°310 – 24°500 N), South China Sea (31 March 2009; 22 August 2011; 20 September 2011; 15 October 2011; 24 November 2011; 20 February 2012; 14 April, 2012). Site: Gills. Type-material: Holotype (No. DYW2012041401) and paratypes (Nos DYW2009033101, DYW2012041402, DYW2011112401-04, DYW2012022001-03, DYW201 1101501-02, and DYW2011082201) are deposited in the
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Fish Parasite Laboratory, College of Life Science, South China Normal University, Guangzhou, China. Two paratypes are deposited in the British Museum (Natural History) Collection at the Natural History Museum, London (BMNH 2013.8.9.1-2). Etymology: The specific name is derived from the coca-cola bottle shaped body. Description (Figs. 4D, E, 5–7) [Based on 26 specimens; measurements from 10 specimens]. Body bottle-shaped, thick, narrows gradually towards anterior extremity, 1,550–2,810 (2,080;
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n = 10) 9 290–550 (394; n = 10). Buccal suckers 2, semi-circular, aseptate, 25–50 (46; n = 8) 9 50–98 (77; n = 8). Pharynx oval, 48–65 (57; n = 8) 9 38–50 (43; n = 8); oesophagus divides into 2 intestinal caeca posterior to copulatory organ. Caeca with lateral diverticula, not confluent posteriorly, extend into haptor (Figs. 5A, 6A).
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Haptor cordiform, demarcated from body proper by distinct constriction, relatively large, 320–520 (428; n = 10) 9 230–450 (384; n = 10), narrows abruptly after third pair of clamps. Four pairs of clamps, each with short peduncle, arranged symmetrically along haptoral margins (Fig. 6E). Anterior 3 pairs similar in shape, smaller in size: first pair 75–113 (98;
Fig. 5 Chelimazocraes ascidiformis n. sp. A, Whole worm, ventral view; B, Copulatory organ; C, Lateral spines of the copulatory organ; D, Measurements of the copulatory spines (D1, D2, lateral spines; D3 median spine); E, Hamuli; F, Egg. Scale-bars: A, 500 lm; B, E, 50 lm; C, 10 lm; F, 100 lm
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Fig. 6 Chelimazocraes ascidiformis n. sp. A, Whole worm, ventral view; B, Copulatory organ; C, Posterior part of the haptor (fourth pair of clamps shown); D, Anterior clamp; E, Haptor. Scale-bars: A, 500 lm; B, D, 50 lm; C, 100 lm; E, 200 lm
n = 20) 9 68–113 (91; n = 20); second pair 73–100 (85; n = 20) 9 53–90 (75; n = 20); third pair 50–75 (58; n = 20) 9 45–65 (53; n = 20); each clamp consisting of 5 sclerites: SAA, SMB (petaliform with 3 lobes), SMS, SPS, and SAP (Figs. 6D, 7). Fourth pair of clamps with 3 sclerites, distinct from those in the 3 anterior pairs (Figs. 4, 6C), 65–75 (73; n = 20) 9 38–48 (41; n = 20). Posterior appendage small, 50–163 (93; n = 10) 9 45–125 (96; n = 9), armed with 2 pairs of hamuli. Outer hamuli larger, with developed inner and outer roots, with measurements: a, 55–65 (62; n = 11); b, 35–40 (38; n = 11); c, 10–13 (11; n = 9);
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d, 18–25 (22; n = 9); e, 8–15 (10; n = 8). Inner pair of hamuli small, each with curved tip and straight handle, 18–25 (21; n = 10) long (Fig. 5E). Testes numerous, 23–50 in number, arranged in several longitudinal rows. Male copulatory organ almost circular, 56–100 (81; n = 6) 9 75–100 (84; n = 6), at 250–550 (394; n = 10) from anterior extremity of body, armed with 2 pairs of differently shaped outer spines and 22–26 similarly shaped inner spines (Figs. 5B, 6B). Inner spines arranged circularly, with curved tip and flat base, with measurements: a, 8–13 (9; n = 6); b, 8–10 (10; n = 8) (see D3 in Fig. 5D). Outer spines 2 pairs, heteromorphic, one
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Fig. 7 Chelimazocraes ascidiformis n. sp. Ventral view of the anterior clamp and its sclerites. Complete structures of the sclerites from SAA and SAP are shown, observed after digestion with Proteinase K. Scale-bar: 50 lm
funnel-shaped, with measurements: a, 30–33 (32; n = 3); b, 18–20 (19; n = 3); the other sickle-shaped, with measurements: a, 10–13 (12; n = 4); b, 15–20 (18; n = 6); c, 10–13 (12; n = 2); d, 20 (n = 2) (see Fig. 5C and D1, D2 in Fig. 5D). Ovary S-shaped, pretesticular, not easily identifiable. Vitellarium follicular, extends from copulatory organ to ends of intestinal caeca, sometimes into haptor. Eggs oval, with single short, thick filament at posterior pole, 163–180 (173; n = 3) long (excluding filament) and 63–120 (92; n = 3) wide (Fig. 5F). Vaginal pore absent. Remarks The two new species are easily distinguished from all previously known mazocraeid species by the unique structure of the fourth pair of clamps. No differences were observed in the structure of the sclerites of the fourth pair of clamps between the two new species,
although their size is different. Three of the sclerites namely the SCI, SAE and SOS, could be clearly identified after proteinase K digestion from the fourth pair of clamps. Although their function remains unknown, this is the first report of a clamp structure of this type. Noticeable differences observed between the two species are shown in Table 1.
Discussion Species of Chelimazocraes n. g. are characterised largely by the structure of the sclerites in the fourth pair of clamps. Thus far, all clamps of the mazocraeid species have been reported to be of the mazocraeidtype, with 5 to 8 sclerites which differ in structure between the different species. In addition to the anterior three pairs of clamps with a normal mazocraeid-type structure, species of Chelimazocraes n. g. also have a non-mazocraeid-type clamp with only
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Table 1 Comparison of the main features of the two species of Chelimazocraes n. g
Body
Haptor
Chelimazocraes liaoi n. sp.
Chelimazocraes ascidiformis n. sp.
Lanceolate, large
Bottle-shaped, small
3,400–6,050 9 300–770
1,550–2,810 9 290–550
(4,099 9 477)* 300–570 9 250–450 (457 9 361)
(2,080 9 394) 320–520 9 230–450 (428 9 384)
Demarcated by a slight constriction from body proper; three anterior pairs of clamps slightly smaller
Demarcated by a distinct constriction from body proper; three anterior pairs of clamps distinctly smaller
SAA, SAS, SMB (cross-shaped), SMS, SL
SAA, SMB (petaliform with 3 lobes), SMS, SPS, SAP 75–113 9 68–113 (98 9 91)
Sclerites of first three pairs of clamps First pair of clamps
65–120 9 75–175 (87 9 109)
Second pair of clamps
65–115 9 80–168 (85 9 102)
73–100 9 53–90 (85 9 75)
Third pair of clamps
68–133 9 75–140 (82 9 93)
50–75 9 45–65 (58 9 53)
Fourth pair of clamps
75–158 9 38–88 (98 9 50)
65–75 9 38–48 (73 9 41)
Copulatory organ
38–45 9 35–40 (43 9 38)
56–100 9 75–100 (81 9 84)
15–16 median spines in two longitudinal rows
22–26 median spines in a circle
Buccal suckers
Two, circular, septate
One, aseptate
Egg
243–338 9 65–70 (281 9 68)
163–180 9 63–120 (173 9 92)
Terminal lappet
Two pairs of hamuli and one pair of hooklets; outer hamuli with broad base
Two pairs of hamuli; outer hamuli with slender base
*Metrical data are given as the range (in micrometres) followed by the mean in parentheses
three unique sclerites which resemble chelicerae (Fig. 4). Chelimazocraes is proposed based on the presence of this new feature. The two species of Chelimazocraes n. g. were found to parasitise the gills of marine clupeoid fishes, the rates of infection being estimated as less than 5% and infection intensities as c.1–3 worms per host. Interestingly, both species always co-occurred with Mazocraeoides gonialosae Tripathi, 1959 and Neomazocraes dorsomatis (Yamaguti, 1938) Price, 1943, which had higher infection intensities (our unpublished data). The three anterior pairs of clamps are similar in structure but differ in size, with the first pair being the largest in Chelimazocraes spp. This feature is similar in species of Pseudoanthocotyloides Price, 1959 and Pseudoanthocotyle Bychowsky & Nagibina, 1954, in which the first pair of clamps is significantly larger than the remaining pairs. In Chelimazocraes spp., however, the anterior three pairs of clamps gradually decrease in size towards the posterior end of the body. The shape of the SMB is also regarded as a distinguishing feature of mazocraeid genera. For example, the SMB is perforated in species of
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Cribromazocraes Mamaev, 1981, but H-shaped in species of Neomazocraes Price, 1934. In Chelimazocraes spp., the SMB is cross-shaped with two protruding flanks in C. liaoi n. sp. and three petaliform-like lobes in C. ascidiformis n. sp. Several perforations are present on the SMB in both species of Chelimazocraes, and this is similar to that in Pseudoanthocotyle pavlovskyi Bychowsky & Nagibina, 1954. The clamp sclerite SAS was absent in C. ascidiformis, which is similar to members of Neomazocraes Price, 1934. This suggests that Chelimazocraes spp. have a similar clamp structure and arrangement to species of Pseudoanthocotyloides, Pseudoanthocotyle and Neomazocraes. Haptoral characteristics and clamp variations are important features that are used to distinguish mazocraeid genera. Although in species of Mazocraeoides Price, 1936, Pseudomazocraeoides Price, 1961, and Reimericotyle Mamaev, 1984, the haptor is not obviously developed and the clamps are located along the body (Fig. 8A), in most other genera the haptor is well developed at the posterior end of the body and the clamps are arranged on the haptor. However, the rank, number, structure and size of the clamps vary in
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Fig. 8 Diagrammatic illustration showing haptoral characteristics and clamp variations in 26 genera of Mazocraeidae. A, Haptor not developed and clamps located along the body (Mazocraeoides, Pseudomazocraeoides and Reimericotyle); B, Four pairs of clamps with similar size and structure arranged symmetrically on the haptor (Anchovicola, Clupeocotyle, Cribromazocraes, Kuhnia, Leptomazocraes, Mazocraes, Neomazocraes, Ophicotyle, Paramazocraes and Pseudokuhnia); C, First pair of clamps the largest, the other three pairs of similar size (Pseudoanthocotyle, Pseudoanthocotyloides, Scomberocola and Taurimazocraes); D, Two anterior pairs of clamps significantly larger than the two posterior pairs (Etrumeicotyle and Neoclupeocotyle); E, Fourth pair of clamps with a unique structure (Chelimazocraes n. g.); F, Only one small clamp on one side of the haptor (Grubea); G, Four clamps on one side, larger than the opposite ones (Neogrubea and Paragrubea); H, Two large clamps on one side with different sclerites (Heteromazocraes and Heterocotyle); I, Three large clamps on one side with different sclerites (Sinomazocraes)
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different genera. Most mazocraeid species are armed with four pairs of clamps, which are similar in size and structure, and have a bilaterally symmetrical arrangement in species of at least 10 genera, including Anchovicola Unnithan, 1964, Clupeocotyle Hargis, 1955, Cribromazocraes Mamaev, 1981, Kuhnia Sproston, 1945, Leptomazocraes Mamaev, 1975, Mazocraes Hermann, 1782 Neomazocraes Price, 1934, Ophicotyle van Beneden & Hesse, 1863, Paramazocraes Tripathi, 1959 and Pseudokuhnia Rohde & Watson, 1985 (Fig. 8B). In four genera, the most anterior pair of clamps is the largest, whereas the other three pairs of clamps are of a similar size (Pseudoanthocotyle Bychowsky & Nagibina, 1954, Pseudoanthocotyloides Price, 1959, Scomberocola Unnithan, 1964 and Taurimazocraes Mamaev, 1982) (Fig. 8C). In species of Etrumeicotyle Mamaev, 1981 and Neoclupeocotyle Price, 1961, the two anterior pairs of clamps are significantly larger than the two posterior pairs (Fig. 8D). However, in the species of Chelimazocraes, although clamps are arranged bilaterally and symmetrically, they differ in both the size and structure of the clamps, which exhibit great variation (Fig. 8E). Clamps may also be arranged asymmetrically and bilaterally on the haptor. In species of Grubea Diesing, 1858, four large clamps of a similar size are located on one side of the haptor, whereas only a single small one is on the other (Fig. 8F), and, in species of Neogrubea Dillon & Hargis, 1968 and Paragrubea Mamaev, 1982, four small clamps are present on the opposite side but the clamp structure on both sides is similar (Fig. 8G). However, in species of Heteromazocraes Mamaev, 1981 and Heterocotyle Unnithan, 1964, the two large clamps on one side have component sclerites that are different from the two small clamps on the same side and the four clamps on the other side; in fact, the latter six clamps have similar sclerites (Fig. 8H). Similarly, in the species of Sinomazocraes Zhang, Liu, Fang & Ding, 2003, three large clamps on one side have component sclerites that are different from both the fourth small clamp on the same side and the four clamps on the other side; the latter five clamps have similar sclerites (Fig. 8I). It appears that, if two or three large clamps are present on one side, then their structure is different from that of the small clamps. It is possible that a species with only one large clamp on one side may exist, but this has not been seen. Whether
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the differences in clamps are related to the nature of the host or to other factors has yet to be determined. Acknowledgements This work was supported by the National Natural Science Fund of China (Nos. 31093430, 31172051). We would like to thank Dr David I. Gibson of the Natural History Museum, London, for his great help with literature and suggestions. We are grateful to Prof. Jianying Zhang for his comments on the manuscript. We owe a lot to Drs Aneta Kostadinova and David Gibson who helped to improve the English of the manuscript.
References Cao, S. M., & Ding, X. J. (2010). Monogenea of Chinese marine fishes XX.: a new Chinese record of genus Grubea. Journal of South China Normal University, 2, 105–106 (In Chinese). Deepak, K. D., & Gupta, V. (2007). Report of a new species, Paramazocraes lutjanusi n. sp. from the gills of marine fish, Lutjanus johnii (Cuv. and Val.) from Puri coast India. Flora and Fauna (Jhansi), 13, 363–366. Mamaev, Y. L. (1975). [Monogeneans of clupeiform fishes from the South China Sea (Mazocraeidae and Diclidophoroidea).] Trudy Biologo-Pochvennogo Instituta, Vladivostok, 26, 102–114 (In Russian). Mamaev, Y. L. (1981). Some new monogenean species and genera of the family Mazocraeidae. Helminthologia, 18, 169–187. Mamaev, Y. L. (1982a). [Monogeneans of the subfamily Grubeinae price, 1961 (Family Mazocraeidae).] Parazitologiya, 16, 457–463 (In Russian). Mamaev, Y. L. (1982b). Notes on the systematics of mazocraeid monogeneans with a redescription of some poorly studied taxa. Helminthologia, 19, 25–39. Mamaev, Y. L. (1984). On the specific composition and morphological characteristics of the genus Pseudomazocraeoides (Monogenea, Mazocraeidae). Angewandte Parasitologie, 25, 26–32. Unnithan, R. V. (1964). On five new species of monogenetic trematodes parasitic on the gills of marine fishes from the south west coast of India. Treubia, 26, 159–178. Wu, X. M., & Zhang, J. Y. (2009). Study on Monogenea of Chinese marine fishes: one new species of the genus Grubea (Mazocraeidae, Grubeinae) from Guangdong, China. Journal of South China Normal University, 4, 97–99 (In Chinese). Yamaguti, S. (1963). Systema helminthum. Vol. IV. Monogenea and Aspidocotylea. New York: Interscience Division, John Wiley & Sons, 699 pp. Zhang, J. Y., Liu, L., & Ding, X. J. (1997). Monogenea of Chinese marine fishes. VII. A new species and two new records of the Tetronchoididae from fishes of the South China and East China Seas. Systematic Parasitology, 38, 197–201. Zhang, J. Y., Liu, L., Fang, J. P., & Ding, X. J. (2003a). Monogenea from the middle Yangtze Valley: Sinomazocraes
Syst Parasitol (2013) 86:271–283 changjiangensis n. g., n. sp. (Family Mazocraeidae Price, 1936) on a clupeiform fish from Hubei Province, China. Systematic Parasitology, 54, 103–109.
283 Zhang, J. Y., Yang, T. B., Liu, L., & Ding, X. J. (2003b). A list of monogeneans from Chinese marine fishes. Systematic Parasitology, 54, 111–130.
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