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Systematic Parasitology

, Volume 96, Issue 1, pp 65–78 | Cite as

Bucephalus damriyasai n. sp. (Digenea: Bucephalidae) from the blacktip trevally Caranx heberi (Bennett) (Perciformes: Carangidae) off Bali, Indonesia

  • Rodney A. BrayEmail author
  • Harry W. Palm
  • Stefan Theisen
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Part of the following topical collections:
  1. Digenea

Abstract

The new species Bucephalus damriyasai n. sp. is described from Caranx heberi (Bennett) from off Bali, Indonesia. It can be distinguished from other Bucephalus spp. recorded from carangid hosts by its narrow elongate body shape and the relatively long distance between the rhynchus and the vitellarium, as well as other features distinguishing it from individual species. The most similar species are differentiated from B. damriyasai n. sp. as follows: B. carangis Yamaguti, 1970 has a much greater length, the rhynchus is smaller and the cirrus-sac is small, not always reaching to the posterior testis; B. fragilis Velasquez, 1959 is a tiny species, the pre-vitelline distance is short and the caecum is saccular; B. gorgon (Linton, 1905) is much longer and relatively broader, the uterus reaches distinctly anterior to the vitellarium and the rhyncheal tentacles appear more complex; B. labracis Paggi & Orecchia, 1965 is distinctly longer, slightly broader, with a slightly larger rhynchus, and has shorter pre-uterine and pre-mouth distances; B. paraheterotentaculatus Velasquez, 1959 is much longer, relatively rather broad, the rhynchus is said to bear 21 tentacles, the post-testicular region and cirrus-sac reach are longer and the caecum is described as saccular; B. sphyraenae Yamaguti, 1952 is longer, slightly broader, the uterus reaches anteriorly to the vitellarium and the caecum is claviform and oriented anteriorly; B. margaritae Ozaki & Ishibashi, 1934 (syn. B. varicus Manter, 1940) is relatively squat, has shorter pre-vitelline and pre-mouth distances and a longer post-testicular distance and cirrus-sac reach; B. yamagutii Gupta & Singh, 1985 is broader, with a relatively short pre-vitelline distance, the caecum extends anteriorly to the pharynx, but not posteriorly and the rhynchus is said to carry five tentacles. The distinctive features of B. damriyasai n. sp. are compared with those of all other marine Bucephalus spp. in a table. The number of bucephalid trematodes known from Indonesian waters is now 13, two of them await further identification. They have been described from the fish families Carangidae, Platycephalidae, Sciaenidae, Serranidae and Sphyraenidae.

Introduction

The Indonesian fish parasite fauna is species-rich, resulting from the high number of fish species surrounding about 17,000 islands of this maritime nation. However, though being a hot spot of aquatic biodiversity, fish parasites are far less studied. As stated by Bray & Palm (2009) and considering recent studies (Bray et al., 2016; Yong et al., 2016; Bray et al., 2017), over 80 fish-parasitic trematode species have been reported from Indonesian waters.

According to Palm & Bray (2014), many fish parasites that have been reported off the Hawaiian Islands in the Central Pacific have an Indo-Pacific or even worldwide distribution. Although it can be expected that a high number of new trematode taxa will be described from Indonesia, the same importance should be placed on having reliable identifications of already known species from other regions. Without proper identification the use of fish parasites as biological indicators (Palm, 2011), of increasing importance in many regions (Truong et al., 2017), is difficult and in some cases impossible. Palm & Rückert (2009), Palm et al. (2011) and Neubert et al. (2016) have developed a method to use grouper fish parasites as biological indicators for pollution and environmental change in Indonesian coastal waters, but several bucephalids recovered were only tentatively identified (Bray & Palm, 2009).

The genus Bucephalus Baer, 1826 includes many species reported from fresh and marine waters. It is characterised by having a sucker-like rhynchus with a hood bearing tentacles (usually seven). The tentacles may be found withdrawn and difficult to see and in such cases the worms look very similar to members of Rhipidocotyle Diesing, 1858. Recent molecular studies by Nolan et al. (2015) have indicated that the genus is polyphyletic, with at least three separate monophyletic groups embedded within an assortment of species of Rhipidocotyle, Prosorhynchoides Dollfus, 1929 and Paurorhynchus Dickerman, 1954.

Caranx heberi (Bennett) (syn. C. sem Cuvier) is a common carangid throughout the Indo-Pacific region. The only reports of digeneans we are aware of from this host are the bucephalid Bucephalus margaritae Ozaki & Ishibashi 1934 from off Natal, South Africa (Bray, 1984) and an unidentified sclerodistomid Prosorchis sp. from the Arabian Gulf (El-Naffar et al., 1992; Al Kawari et al., 1996). We herewith present a description of new bucephalid species from this host from the Balinese coast, Indonesia.

Materials and methods

The present study is based on material collected during the First Educational Workshop on Marine Fish Parasites in Bali, July 21st - August 2nd 2013, of Indonesian and international students and researchers investigating a wide range of hosts from Balinese waters. Three specimens (15.7–16.7 cm total length, 66.2–70.6 g) of Caranx heberi were caught by artisanal fishermen and landed at Kedonganan Bay, transported alive into the laboratory of the Veterinary Faculty, Udayana (UNUD) University, Denpasar, Bali, and directly studied for fish parasites. Kedonganan Bay is located at the western side of the southern tip of Bali, directly next to the Ngurah Rai Kuta international airport. The airstrip of the airport reaches into the ocean and acts as the northern border of the bay. Kedonganan is a typical fishing village but is heavily influenced by tourism. There is no harbour; the small ships lay directly in front of the beach which is used to land captures. The fishermen catch fish from the Bali Strait and from nearby areas off South Bali and East Java. They use drift nets, troll lines and hand lines. A cooperation of the local fishermen manages the market (Proctor et al., 2003). Digeneans were collected according to the gut wash methodology described by Cribb & Bray (2010). Unfortunately, although these worms were collected with a view to sequencing, these specimens have not yielded usable rDNA.

Whole-mounts were stained with Mayer’s paracarmine, cleared in beechwood creosote and mounted in Canada balsam. Measurements were made through a drawing tube on an Olympus BH-2 microscope, using a Digicad Plus digitising tablet and Carl Zeiss KS100 software adapted by Imaging Associates, and are quoted in micrometres, as the range and the mean in parentheses. ‘Cirrus-sac reach’ is the distance between the posterior extremity of the worm and the anteriormost extent of the cirrus-sac. The type-material is deposited in the following museum collections: the Natural History Museum, London, UK (NHMUK); the National Biodiversity Collection, Museum Zoologicum Bogoriense, Cibinong, Bogor, Java, Indonesia (MZB); and the Natural History Museum, Berlin, Germany (ZMB).

Results

All C. heberi sampled were infected with a new bucephalid (100% prevalence), but levels of intensity were not recorded.

Family Bucephalidae Poche, 1907

Genus Bucephalus Baer, 1827

Bucephalus damriyasai n. sp.

Type-host: Caranx heberi (Bennett) (Perciformes: Carangidae), blacktip trevally.

Type-locality: Off South Bali, Indonesia. Purchased from artisanal fishermen, 23.vii.2013, 26.vii.2013, 31.vii.2013.

Type-specimens: Holotype ZMB E.7629. Paratypes: E.7630–1; MZBTr 246–250; NHMUK 2018.6.7.1–3.

Site in host: Intestine.

ZooBank registration: To comply with the regulations set out in article 8.5 of the amended 2012 version of the International Code of Zoological Nomenclature (ICZN, 2012), details of the new species have been submitted to ZooBank. The Life Science Identifier (LSID) for Bucephalus damriyasai n. sp. is urn:lsid:zoobank.org:act:F68217B4-831B-4D2A-84CE-F731F41CFCFC.

Etymology: This species is named in honour of Professor Dr I Made Damriyasa, Faculty of Veterinary Sciences, Udayana University, for his continuous support of fish parasite research in Balinese waters.

Description (Figs. 1, 2)

[Based on 15 whole-mount preparations.] Body elongate, narrow, gradually widening to maximum at about level of gonads; length 851–1,544 × 76–123 (1,126 × 97); width 7.57–10.4 (8.71)% of body length. Tegument spinous throughout; spines tiny. Rhynchus 67–85 × 55–87 (77 × 71), bearing 7 tentacles, each with side branches and elongate central branch; most often withdrawn and difficult to see; rhynchus length 5.53–8.34 (7.01)% of body length; rhynchus width 77.8–112 (92.7)% of rhynchus length. Mouth at level of ovary, well inside posterior half of body, pre-mouth distance 559–1,011 (737), 63.4–69.1 (65.4)% of body length. Pharynx globular; 48–66 × 47–60 (59 × 55), width 3.82–6.32 (5.00)% of body length. Caecum elongate, 72–450 × 16–44 (351 × 27); length 28.1–44.3 (33.8)% of body length; mostly reaching anterior to pharynx almost to anterior extremity of vitellarium, but with distinct posteriorly directed part overlapping testes, pre-caecal distance 234–706 (452), 27.5–52.6 (38.8)% of body length; caecum to rhynchus distance 164–614 (385).
Figs. 1–2

Bucephalus damriyasai n. sp. 1, Holotype, ventral view; 2, Rhynchus with the seven tentacles labelled for clarity. Scale-bars: 1, 200 µm; 2, 100 µm

Testes 2, oval, tandem or nearly so, in posterior quarter of body; pre-testicular distance 573–1,092 (767), 65.0–71.2 (68.0)% of body length; contiguous or slightly separated, distance 0–19 (8), 0–1.99 (0.78)% of body length; anterior testis 44–78 × 42–69 (58 × 53), length 4.74–5.70 (5.11)% of body length; posterior testis 39–86 × 39–61 (60 × 52), length 4.56–6.47 (5.27)% of body length; post-testicular distance 160–283 (216), 16.9–22.2 (19.3)% of body length. Cirrus-sac elongate, more or less parallel sided, reaching to posterior or anterior testis; 125–254 × 33–58 (172 × 43), length 13.2–16.9 (15.3)% of body length; cirrus-sac reach 208–359 (276), 21.7–28.1 (24.7)% of body length. Seminal vesicle subglobular to oval, in proximal cirrus-sac; 26–52 × 23–41 (37 × 32), length 18.9–25.2 (21.4)% of cirrus-sac length. Pars prostatica long, straight, surrounded by dense layer of gland-cells, lined with filaments; 91–195 (127) long, 20–29 (25) wide. Ejaculatory duct narrow, opens on large, lobed genital lobe, inside genital atrium. Genital atrium large. Genital pore ventral, distinctly separated from posterior extremity by 23–42 (34), 2.46–4.16 (3.07)% of body length.

Ovary oval, 41–75 × 35–62 (55 × 45), length 4.19–6.09 (4.84)% of body length; pre-testicular, contiguous with anterior testis; pre-ovarian distance 543–1,030 (724), 61.4–66.7 (64.2)% of body length; post-ovarian distance 245–457 (332), 26.7–32.0 (29.6)% of body length. Mehlis’ gland overlaps ovary and anterior testis. Uterine seminal receptacle and Laurer’s canal not detected. Uterus not usually reaching anteriorly to vitelline fields, pre-uterine distance 322–853 (514), 33.1–55.2 (45.0)% of body length; uterus to rhynchus distance 254–771 (447), uterus narrow anteriorly to pharynx, wider posteriorly. Eggs numerous, tanned, operculate; 18–25 × 13–19 (22 × 16). Metraterm not detected, obscured by eggs. Vitellarium consists of 2 lateral fields of 14–18 (16) follicles, symmetrical or nearly so, but with one slightly longer than other, long field 180–385 (265) long, 20.3–26.5 (23.3)% of body length; shorter field 168–360 (248) long; anterior extremity usually anterior to uterus and caecum; pre-vitelline distance 359–587 (438), 36.9–42.4 (39.0)% of body length; vitellarium to rhynchus distance 287–504 (363); posterior extremity just anterior to or overlapping pharynx; post-vitelline distance 290–600 (415), 33.5–39.7 (36.9)% of body length.

Excretory pore terminal; anterior extent of vesicle visible in some specimens reaching just anterior to vitellarium.

Discussion

We are aware of 48 described nominal species of Bucephalus in marine fishes and we have examined the descriptions of all except B. arabiana Varma, 1982, the description of which we have been unable to find. We have developed a visual key similar to that to Prosorhynchus developed by Bray & Palm (2009) (http://www.nhm.ac.uk/bray2009). Ten characters are used, most of which are listed as a percentage of body length: 1, Length; 2, Width %; 3, Rhynchus length %; 4, Tentacle number; 5, Pre-vitelline distance %; 6, Pre-uterine distance %; 7, Pre-mouth distance %; 8, Post-testicular distance %; 9, Cirrus-sac reach %; and 10, Egg length.

Eight species have none of the above listed percentage characters more than 10% either more or less than that quoted in the original description or derived from the original illustrations, or are distinctly different in size, tentacle number or egg-size. These are B. carangis Yamaguti, 1970; B. fragilis Velasquez, 1959; B. gorgon (Linton, 1905) (syn. B. introversus Manter, 1940); B. labracis Paggi & Orecchia, 1965; B. paraheterotentaculatus Velasquez, 1959; B. sphyraenae Yamaguti, 1952; B. varicus Manter, 1940 (usually considered a synonym of B. margaritae Ozaki & Ishibashi, 1934); and B. yamagutii Gupta & Singh, 1985.

Bucephalus carangis Yamaguti, 1970 is reported from the black jack Caranx lugubris Poey and the bluefin trevally C. melampygus Cuvier off Hawaii (Yamaguti, 1970; Palm & Bray, 2014). It apparently grows to a much greater size than B. damriyasai n. sp. (to 3,500 µm), the rhynchus is smaller (3–5% of body length), and the cirrus-sac is small, not always reaching to the posterior testis (cirrus-sac reach about 18% of body length).

Bucephalus fragilis Velasquez, 1959 is also reported from carangids, the torpedo scad Megalaspis cordyla (L.), the doublespotted queenfish Scomberoides lysan (Forsskål) and Caranx sp. from off the Philippines, the South China Sea and Masirah Bay off Oman in the northern Indian Ocean (Velasquez, 1959; Parukhin, 1966, 1976). In this tiny species (length 660–900 µm), the pre-vitelline distance is short (about 27% of body-length) and the caecum is saccular.

Bucephalus gorgon (Linton, 1905) (syn. Bucephalus introversus Manter, 1940) is a widely reported species known only from carangids and mainly from members of the genus Seriola in the Pacific, Indian and Atlantic Oceans. It was described by Linton (1905) as Gasterostomum gorgon in the yellowtail amberjack Seriola lalandi Valenciennes from the North-West Atlantic at Beaufort, North Carolina. Eckmann (1932) placed this species in Bucephalus. It was redescribed and illustrated (apparently a badly contracted specimen) by Linton (1940) as Nannoenterum gorgon from S. lalandi at Woods Hole, Massachusetts. Bartoli et al. (2005) redescribed this species from the greater amberjack Seriola dumerili (Risso) off Corsica in the western Mediterranean Sea. They considered Bucephalus introversus Manter, 1940, from the crevalle jack Caranx hippos (L.), S. dumerili, S. lalandi and Seriola sp. from the eastern Pacific off Mexico and Columbia (Manter, 1940a) as a synonym of B. gorgon. Further descriptions and descriptive matter have been given by Oshmarin (1965) from Seriolanigromaculata’ off Vietnam; Corkum (1967) from S. dumerili, and the banded rudderfish Seriola zonata (Mitchill) off Louisiana; Fischthal et al. (1982) from S. dumerili off Israel in the eastern Mediterranean; and Luque & Oliva (1993) from S. lalandi (as S. mazatlana) off Antofagasta, Chile. Other hosts recorded are the threadfin jack, Carangoides otrynter (Jordan & Gilbert), the white trevally Pseudocaranx dentex (Bloch & Schneider) and the Almaco jack Seriola rivoliana Cuvier and the distribution includes the Gulf of Mexico and off Canary Islands in the Atlantic, the Balearic Sea in the western Mediterranean, the Gulf of Mannar in the Indian Ocean and the South China Sea and off New South Wales and Victoria, eastern Australia in the Pacific Ocean (Bravo-Hollis & Sogandares-Bernal, 1956; Parukhin, 1966; Nahhas & Powell, 1971; Parukhin, 1976; Fischthal, 1982; Montero et al., 2002; Gijon-Botella et al., 2007; Hutson et al., 2007). Nolan et al. (2015) used sequences of B. gorgon from S. dumerili in the Gulf of Mexico to show that the closest sequenced relative is Prosorhynchoides ovatus (Linton, 1898).

Linton (1905, p. 364) described the “anterior sucker (i.e. a rhynchus) surrounded by a crown of about eighteen tentacles”; in most cases, the anterior end of his specimens was withdrawn (his figure 241; incorrectly oriented). Linton (1940) redescribed the species with an anterior sucker provided with about 20 tentacles, the specimens being “all macerated”. Bartoli et al. (2005) stated that “the rhynchus of B. gorgon consists of seven large retractile tentacles, each of them provided with one or two small basal processes”. Bucephalus gorgon is usually described as much longer and relatively broader than B. damriyasai n. sp., the uterus reaches distinctly anterior to the vitellarium. The rhyncheal tentacles appear much more complex in B. gorgon, particularly as described by Bartoli et al. (2005).

Bucephalus labracis Paggi & Orecchia, 1965 was originally found in the European seabass, Dicentrarchus labrax (L.) in the Tyrrhenian Sea (Paggi & Orecchia, 1965). It has subsequently been reported from the same host off Israel, off the Iberian Peninsula, in the Tunisian and Algerian lagoons and off Sardinia (Fischthal, 1982; Muñoz et al., 1989; Gargouri Ben Abdallah & Maamouri, 2005; Gijon-Botella et al., 2007; Culurgioni et al., 2010; Culurgioni et al., 2014; Brahim Tazi et al., 2016). This species grows to 3,310 µm long, is slightly or distinctly broader with a slightly larger rhynchus, has shorter pre-uterine (about 23–29%) and pre-mouth (about 54–57%) distances. Metacercariae have been reported in the big-scale sand smelt Atherina boyeri Risso, the common goby Pomatoschistus microps (Krøyer), the black-striped pipefish Syngnathus abaster Risso, the leaping mullet Chelon saliens (Risso), the golden grey mullet, C. auratus (Risso) and the gilthead seabream Sparus aurata L. (see Gargouri Ben Abdallah & Maamouri, 2005; Culurgioni et al., 2014; Culurgioni et al., 2015). The first intermediate host is the carpet shell Tapes decussatus (L.) (Gargouri Ben Abdallah & Maamouri, 2005). Another species has been described under this name, Bucephalus labracis Nisreen Ezz El-Dien, Abdel-Rahman, El-Gawady, Imam & Fahmy, 1990, from the same host species in the Suez Canal at Ismailia, Egypt (Nisreen Ezz El-Dien et al., 1990). The description is poor, but it does not appear to be conspecific with its senior homonym and may not be in this genus.

Bucephalus paraheterotentaculatus Velasquez, 1959 was originally reported in the blackbanded trevally Seriolina [as Seriola] nigrofasciata (Rüppell) from Malabon, Rizai, Luzon Island, Philippines (Velasquez, 1959). It has subsequently been reported in S. nigrofasciata, S. dumerili and Seriola sp. from the South China Sea and Masirah Bay off Oman in the Northern Indian Ocean (Parukhin, 1966, 1976). This species grows to 4,070 µm long, is relatively rather broad (maximum width about 12–13% of length), the rhynchus bears “21 tentacles grouped in multiples of 3 conforming to the basic number of 7”, the post-testicular region is about 31% of body length and the cirrus-sac reach is about 36% of body length. The caecum is described as saccular.

Bucephalus sphyraenae Yamaguti, 1952 was originally reported from Sphyraena sp. off Makassar, Sulawasi, Indonesia (Yamaguti, 1952). Subsequently it has been reported from the blackfin barracuda Sphyraena qenie Klunzinger (as S. tessera), the false stonefish Scorpaenopsis diabolus (Cuvier), the obtuse barracuda, Sphyraena obtusata Cuvier and the yellowstripe barracuda Sphyraena chrysotaenia Klunzinger from the Red Sea, off Okinawa, Japan and the Arabian Gulf off Kuwait (Parukhin, 1970; Dyer et al., 1988; Nahhas et al., 2006). This species grows to 2,800 µm, its width is about 12–16% of body length and the uterus reaches anteriorly to the vitellarium. The caecum is claviform and oriented anteriorly.

Bucephalus varicus Manter, 1940 is usually considered one of several synonyms of B. margaritae Ozaki & Ishibashi, 1934. A fairly high proportion of records of Bucephalus species from carangids are of B. margaritae and its synonyms. It was originally described as a furcocercous cercaria from the pearl oyster Pinctada imbricata Röding (as Pinctada imbricata mertensii) off Japan (Ozaki & Ishibashi, 1934). A series of papers by Sakaguchi (1962, 1964, 1966a, b, 1968) reported on the completion of the life-cycle of this species and concluded that it was conspecific with B. varicus Manter, 1940. Manter (1940a) in describing B. varicus from “a young specimen of an unidentified species of Caranx, or jack” off Bahia Honda, Panama, considered that B. polymorphus of Nagaty (1937) from carangids in the Red Sea was a misidentification, as B. polymorphus is a freshwater species. Overstreet (1969) and Velasquez (1975) considered B. pseudovaricus Velasquez, 1959 synonymous with B. varicus. Bray (1984) also considered that B. retractilis Yamaguti, 1959, B. carangoides Yamaguti, 1970 and B. ulua Yamaguti, 1970 are synonyms of B. margaritae. Nahhas et al. (2006) “confirm this synonymy” and described the worm from the cleftbelly trevally Atropus atropos (Bloch & Schneider), the largemouth queenfish Scomberoides commersonnianus Lacépède, the Malabar trevally Carangoides malabaricus (Bloch & Schneider), the whipfin silver-biddy Gerres filamentosus Cuvier and the pickhandle barracuda Sphyraena jello Cuvier in the Arabian Gulf off Kuwait. Chinchilla et al. (2006) accepted these synonymies, and described the worm from the southern sennet Sphyraena picudilla Poey off Venezuela. Marchiori et al. (2010) also accepted the synonymy and described the life-cycle in the brown or South American rock mussel Perna perna (L.), the combtooth blenny Hypleurochilus fissicornis (Quoy & Gaimard) and the southern kingcroaker Menticirrhus americanus (L.) in the waters off Brazil. Many of the more recent records of B. margaritae are of non-carangid hosts. Al-Zubaidy (2011) described B. margaritae and B. varicus as separate species, from the great barracuda Sphyraena barracuda (Edwards) and the orange-spotted trevally Carangoides bajad (Forsskål), respectively, from Yemeni Red Sea coastal waters off Hodeidah. The illustrations suggest that several species are involved. Nolan et al. (2015) used sequences of worms identified as B. margaritae from Caranx crysos (Mitchill), from the Gulf of Mexico in their molecular study and showed that, of sequenced species, it is the sister of B. cynoscion Hopkins, 1956. Bucephalus margaritae differs from B. damriyasai n. sp. in its relatively squat shape, short pre-vitelline distance, shorter pre-mouth distance and longer post-testicular distance and cirrus-sac reach. The species has been described many times under the same or different names and clearly needs careful revision. It is likely, if not virtually certain, that a complex of similar species is now known under this name.

Bucephalus yamagutii Gupta & Singh, 1985 is reported only from the Malabar trevally Carangoides malabaricus (Bloch & Schneider) (as Caranx malabaricus) off the Puri coast in the Bay of Bengal (Gupta & Singh, 1985). It is relatively broad (width about 16% of length), with a relatively short pre-vitelline distance (about 28% of body-length) and the caecum extends anteriorly to the pharynx, but not posteriorly. The rhynchus is said to carry five tentacles.

The features that distinguish marine Bucephalus spp. from B. damriyasai n. sp. are tabulated in Table 1.
Table 1

Comparative table of marine Bucephalus spp. Bold indicates major distinctions, italics indicates minor distinctions. Column 3: Width %; 4: Rhynchus length %; 6: Pre-vitelline distance %; 7: Pre-uterine distance %; 8: Pre-mouth distance %; 9: Post-testicular distance %; 10: Cirrus-sac reach %

 

Length

3

4

Tentacle number

6

7

8

9

10

Eggs

Source

B. damriyasai n. sp.

851–1,544

8–10

6–8

7

37–42

33–55

63–69

17–22

22–28

18–25 × 13–19

Present study

B. anguillae Špakulová, Macko, Berrilli & Dezfuli, 2002

1,118–1,658

27–29

17–18

7

21–37

16–17

54–60

22–28

34–42

28–30 × 18

Špakulová et al. (2002)

 

1,160–2,320

26–34

15–16

5 (retracted)

28

18

57

15

26

20–34 × 10–18

Gargouri-Ben Abdullah & Maamouri (2002)

B. arabiansis Dwivedi, 2007

1,020–1,530

17–35

10–16

5

12

13

68

23

44

20–30 × 10–30

Dwivedi (2007)

B. baeri Maillard & Saad-Fares, 1981

1,320–2,640

15–17

10–13

7

32

17

45

22

28

24–27 × 14–16

Maillard & Saad-Fares (1981)

B. barina Srivastava, 1938

1,520–2,800

24–33

7–9

5

24

14

55

36

39

15–19 × 9–11

Srivastava (1938)

B. binidentacularis Wang, 1977

1,600

35

11

[? 6]

15

13

53

38

46

21–25 × 14–16

Wang (1977)

B. brevitentaculatus Corkum, 1967

660–1,330

28–40

9–11

7

15

19

54

37

50

20 × 13

Corkum (1967)

B. carangis Yamaguti, 1970

1,150–3,500

10–14

3–5

7

34

38

59

22

18

17–23 × 11–14

Yamaguti (1970)

B. carangoides Yamaguti, 1970

1,000–1,650

35–44

14–15

7

21

12

56

39

43

16–21 × 10–14

Yamaguti (1970)

B. confusus Velasquez, 1959

2,800

12.5

4

20

?

?

?

?

?

24 × 13–18

Linton (1940)

B. cynoscion Hopkins, 1956

600–1,400

17–34

8–16

5 (or 7)

13

8

57

30

32

20–25 × 13–15

Hopkins (1956)

B. elacatus Yadav, 1977

4,160–5,120

13–15

2–3

4

36

25

53

18

23

24–25 × 9–11

Yadav (1977)

B. fischthali Gupta & Tiwari, 1985

2,520–4,000

18–27

6–8

6

23

25

63–64

21–23

33

32–35 × 32–35

Gupta & Tiwari (1985)

B. fragilis Velasquez, 1959

660–900

15–26

6

7

27

33

59

27

30

17–18 × 9–13

Velasquez (1959)

B. gorgon (Linton, 1905)

1,562–2,750

7–15

8–12

7

31–45

17–24

59–65

18–22

26–28

21–24 × 13–15

Bartoli et al. (2005)

 

1,650

22

11

about 18

29

45

?

16

34

22 × 14

Linton (1905)

 

2,380–3,130

11–14

7–10

about 20

28

8–30

?

?

?

18–21 × 10–12

Linton (1940)

 

2,238

12

9

22

33

17

59

25

28

?

Corkum (1967)

 

2,700

9

9

?

27

21

60

31

25

19–20 × 13–14

Oshmarin (1965)

B. hainanensis Shen, 1990

1,337–2,278

27–28

6–7

7

19

17

54

30

34

15–18 × 9–12

Shen (1990)

B. harpodontis Wang, 1980

1,200–1,600

11

7

8

22

34

44

26

28

24–26 × 16–18

Wang (1980)

B. heterotentaculatus Bravo-Hollis & Sogandares-Bernal, 1956

2,080–3,420

12–13

8–11

7

36

18

56–78

24

29

22–28 × 13–17

Bravo-Hollis & Sogandares-Bernal (1956)

B. hexalobatus Bilqees, Khatoon & Haseeb, 2006a

3,790–3,850

21–22

?

?

?

?

?

?

?

20–24 × 17–19

Bilqees et al. (2006)

B. introversus Manter, 1940

1,202–1,707

17–19

14–20

7

46

30

61

14

35

22–26 × 12–15

Manter (1940a)

B. introversus Manter, 1940

1,720–2,940

16

3–4

?

?

?

?

?

?

23 × 17

Luque & Oliva (1993)

B. jagannathai Verma, 1936

1,100–1,700

32–38

11–15

6

21

17

51

24

43

19–20 × 12–13

Verma (1936)

B. kaku Yamaguti, 1970

1,500–4,700

11–13

6–7

11

53

25

48

19

23

21–25 × 12–16

Yamaguti (1970)

B. kanagurtai Gupta & Tiwari, 1985

3,200–3.570

26–27

7–8

7

23

25

64–76

31

37

40–70 × 40–70 (?)

Gupta & Tiwari (1985)

B. kathetostomae (Manter, 1934)

688–1,434

20–49

12–21

5

19

26

39–55

42

53

18–20 × 10–11

Manter (1934)

B. labracis Paggi & Orecchia, 1965

1,980–3,310

11–14

10–11

7

46

23

54

16

21

20–21 × 18–19

Paggi & Orecchia (1965)

 

1,370–2,750

15–18

10–14

?

?

?

?

?

?

22–24 × 13–15

Maillard (1976)

 

1,200-2,600

22-30

13-15

7

30

29

57

18

?

20-38 x 12-23

Gargouri Ben Abdullah & Maamouri (2005)

B. labracis Nisreen Ezz El-Dien, Abdel-Rahman, El-Gawady, Imam & Fahmy, 1990

709–727

28–29

13–21

numerous

41

45

71

19

45

19–24 × 9–10

Nisreen Ezz El-Dien et al. (1990)

B. leognathi Velasquez, 1959

680

44

13

6

29

30

51

39

36

17–18 × 11–13

Velasquez (1959)

B. margaritae Ozaki & Ishibashi, 1934

?

19

8

7

21

14

60

25

30

??

Sakaguchi (1968)

 

1,435

15

9

7

48

29

59

15

24

20–22,5 × 10

Chinchilla et al. (2006)

 

320–815

16–20

15

7

42

?

67–69

17

32

14–28 × 4(?)–19

Marchiori et al. (2010)

 

343–834

17–20

9

7

42

28

58

14

25

19–20 × 8–11

Al-Zubaidy (2011)

B. marinus Vlasenko, 1931

2,000

10

12

7?

33

21

40

28

30

24 × 15

Vlasenko (1931)

B. minimus (Stossich, 1887)

900

72

13

0?

41

44

35

36

41

not given

Stossich (1887)

 

840–1,540

76

11–16

7

57

34

43

24

41

22–24 × 13–14

Maillard (1975, as Labratrema lamirandi)

 

366–1,088

51–70

10–18

?

57

?

?

?

?

18–24 × 10–15

Pina et al. (2009)

B. neoscombropsi Parukhin, 1979

2,300–2,860

17

8–9

7

41

27

50

16

26

20–25 × 17–22

Parukhin (1979)

B. paraheterotentaculatus Velasquez, 1959

1,220–4,070

12–13

2–3

21/3 = 7

40

31

42–71

31

36

15–26 × 11–18

Velasquez (1959)

B. priacanthi Manter, 1940

1,020–1,215

21

12

7

25

13

51–52

24

39

17–19 × 10–12

Manter (1940b)

B. pseudovaricus Velasquez, 1959

980–1,000

24–30

8

weak

36

34

59

24

43

18–22 × 13–14

Velasquez (1959)

B. retractilis Yamaguti, 1952

1,400–1,950

21–23

7

7

18

16

55

35

37

15–16 × 10–12

Yamaguti (1952)

B. scorpaenae Manter, 1940

2,065–2,792

12–15

6–7

7

23

15

46

23

28

19–22 × 13–15

Manter (1940b)

B. sebastichthydis Yamaguti, 1959

3,450

13

10

7

31

25

51

22

23

23–26 × 13–16

Yamaguti (1959)

B. sextentaculatus Yamaguti, 1970

1,800–3,600

8–9

8

6

38

7

63

26

21

16–21 × 11–16

Yamaguti (1970)

B. solitarius Kohn, 1966

1,550

15

7

5

33

21

60

32

28

20–22 × 11–13

Kohn (1966)

B. sphyraenae Yamaguti, 1952

2,500–2,800

12–16

5

7

37

25

58

25

25

18–24 × 12–16

Yamaguti (1952)

 

1,500–2,175

12–15

5–6

7

29

16

46

21

26

13–20 × 10–18

Nahhas et al. (2006)

B. thapari Gupta & Tiwari, 1983

3,470–3,850

25–26

7–8

4

29

29

68

28–30

39

16–18 × 16–18

Gupta & Tiwari (1985)

B. trifurcatus Wang, 1980

2,400–2,480

10

6

7

23

17

55

21

21

19–21 × 14–15

Wang (1980)

B. ulua Yamaguti, 1970

650–1,300

28–43

14–15

7 (rarely 6)

21

19

63

35

47

14–21 × 9–14

Yamaguti (1970)

B. uranoscopi Yamaguti, 1934

4,860

9

3

7

40

41

63

22

19

18 × 22

Yamaguti (1934)

B. urophyci Szidat, 1961

760

13

17

?

28

20

55

25

37

19 × 10

Szidat (1961)

B. varicus Manter, 1940

705–1,458

9–28

6–19

7

20–25

17–31

53

21–49

35–48

17–20 × 9–16

Manter (1940a)

 

618–2,288

15–17

8–14

7

23–38

25–30

48–86

22–31

32–54

21–27 × 13–23

Nagaty (1937, as B. polymorphus)

 

1,787–2,338

21–24

6–8

7

34

17

58

24

29

15–20 × 9–18

Shen (1990)

 

980–2,500

12–20

9–17

7

37

21

56

22

20

17–22 × 11–13.

Al-Zubaidy (2011)

B. xiamenensis Liu, 1994

1,620–2,180

20–22

9–11

7

14

9

46

30

34

18–22 × 12–16

Liu (1994)

B. yamagutii Gupta & Singh, 1985

1,460–1,570

16

8

5

28

29

66

24–25

30

15–18 × 9–11

Gupta & Singh (1985)

aThis species is unrecognisable; the illustrations are poorly reproduced microphotographs

Concluding remarks

It is not clear why we have not been successful in securing useful DNA from this species as it was fixed in the same way as other digeneans recovered from the Bali Workshop that have been successfully sequenced (Cribb et al., 2014; Bray et al., 2016; Yong et al., 2016; Bray et al., 2017). Successful and experienced molecular biologists in the Rostock and the University of Queensland Laboratories have been frustrated in their attempts to extract DNA from these worms. The species described here is morphologically distinct enough to be easily recognised so it was felt worthwhile to describe it and add a further detail to our depauperate knowledge of the marine fish digeneans of Indonesia.

We are aware of eleven named species of bucephalids in Indonesian waters. These are:
  • Bucephalus damriyasai n. sp. ex blacktip trevally Caranx heberi (Carangidae), off Bali.

  • Bucephalus margaritae Ozaki & Ishibashi, 1934 (as B. retractilis Yamaguti, 1952) ex Caranx sp. (Carangidae), off Sulawesi (Yamaguti, 1952).

  • Bucephalus sphyraenae Yamaguti, 1952 ex Sphyraena sp. (Sphyraenidae), off Sulawesi (Yamaguti, 1952).

  • Prosorhynchoides tenuis (Yamaguti, 1952) ex Indian flathead Platycephalus indicus (L.) (Platycephalidae), off Sulawesi (Yamaguti, 1952).

  • Prosorhynchus chorinemi Yamaguti, 1952 ex doublespotted queenfish Scomberoides lysan (Forsskål) (Carangidae), off Sulawesi (Yamaguti, 1952).

  • Prosorhynchus longicollis Yamaguti, 1953 ex Sphyraena sp. (Sphyraenidae), off Sulawesi (Yamaguti, 1953).

  • Prosorhynchus luzonicus Velasquez, 1959 ex orange-spotted grouper Epinephelus coioides (Hamilton, 1822) (Serranidae), and brown-marbled grouper E. fuscoguttatus (Forsskål), off Sumatra and Java (Palm & Rückert, 2009; Rückert et al., 2009; Rückert et al., 2010; Kleinertz & Palm, 2015).

  • Prosorhynchus platycephali (Yamaguti, 1934) ex fringelip flathead Sunagocia otaitensis (Cuvier) (Platycephalidae), off Java (Bray & Palm, 2009).

  • Rhipidocotyle danai Bray & Palm, 2009 ex black snoek Thyrsitoides marleyi Fowler (Gempylidae), off Java (Bray & Palm, 2009).

  • Rhipidocotyle jayai Bray & Palm, 2009 ex largefin croaker Johnius macropterus (Bleeker) (Sciaenidae), off Java (Bray & Palm, 2009).

  • Rhipidocotyle khalili Nagaty, 1937 ex Sphyraena sp. (Sphyraenidae), off Sulawesi (Yamaguti, 1953).

Two further, as yet unnamed, species are found in Indonesian groupers:
  • Prosorhynchus sp. 1 of Bray & Palm (2009) (syn. Prosorhynchus australis of Rückert et al. (2009) and Palm & Rückert (2009)) from Epinephelus coioides, off Sumatra, E. fuscoguttatus, off Java and the areolate grouper E. areolatus (Forsskål), off Java (Palm & Rückert, 2009; Rückert et al., 2009; Rückert et al., 2010; Palm et al., 2011; Kleinertz et al., 2014; Kleinertz & Palm, 2015).

  • Prosorhynchus sp. 2 of Bray & Palm (2009) (Syn. Prosorhynchus cf. crucibulum (Rudolphi, 1819) of Palm & Rückert (2009)) ex Epinephelus fuscoguttatus, off Java and E. areolatus, off Bali (Rückert et al., 2009; Palm et al., 2011; Kleinertz et al., 2014).

Notes

Acknowledgements

The new species was collected on the 1st Educational Workshop on Marine Fish Parasites in Bali, July 21st–August 2nd, 2013. This study falls under the MOU between the Faculty of Veterinary Sciences, UDAYANA University, Denpasar Bali, and the Professorship of Aquaculture and Sea-ranching, University Rostock, Germany (publication No. 12), to promote fish parasite research in Indonesia.

Funding

This study was supported by the German Federal Ministry for Education and Science (BMBF Grant No. 03F0641D) within the framework of the joint Indonesian-German research programme SPICE III - MABICO (Science for the Protection of Indonesian Coastal Marine Ecosystems).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional, national and international guidelines for the care and use of animals were followed.

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Authors and Affiliations

  • Rodney A. Bray
    • 1
    Email author
  • Harry W. Palm
    • 2
    • 3
  • Stefan Theisen
    • 2
  1. 1.Department of Life SciencesNatural History MuseumLondonUK
  2. 2.Faculty of Agricultural and Environmental Sciences, Aquaculture and Sea-RanchingUniversity of RostockRostockGermany
  3. 3.Faculty of Veterinary SciencesUdayana UniversityBadungIndonesia

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