Parasitic copepods from Egyptian Red Sea fishes: Bomolochidae Claus, 1875

Two species of parasitic copepods from the genus Bomolochus von Nordmann, 1832 (Cyclopoida: Bomolochidae) are redescribed in detail, based on material collected from the gills of Red Sea fishes. Host material was caught at El-tor, near Sharm El-Sheikh, and in the Gulf of Suez, Egypt. Both sexes of Bomolochus bellones Burmeister, 1835 were collected from the gills of a needlefish Tylosurus choram (Rüppell) caught in the Gulf of Suez. This is a new host record. The female is well characterised so only the male is described. Adult females of Bomolochus minus Lin & Ho, 2005 were obtained from the branchial cavities and gills of mojarra Gerresoyena (Forsskål). This species was known only from its original description in Taiwan, and this report constitutes a new host record and a significant range extension. Both parasite species are new records for Egyptian Red Sea waters.


Introduction
The family Bomolochidae Claus, 1875 currently comprises about 141 species of parasites which commonly inhabit the branchial chamber and gills of their marine fish hosts (Boxshall & Halsey, 2004). The type genus, Bomolochus von Nordmann, 1832, is the second largest in the family and the review of Ho & Lin (2009) recognised 20 species as valid. Two species are reported here, Bomolochus bellones Burmeister, 1835 and B. minus Lin & Ho, 2005. Bomolochus bellones was originally discovered off Helgoland, Germany by Burmeister (1835) as a parasite on Belone belone (L.) (as Esox bellone L.), and was subsequently reported from north-western European waters and the Mediterranean (see Vervoort, 1962;Kabata, 1979). However, it was Cressey & Collette (1970) who first documented the worldwide range of this parasite: they collected hundreds of specimens of B. bellones from the gill chambers and oral valves of 16 species of needlefishes (family Belonidae) collected from numerous localities across the North and South Atlantic, the Indian Ocean, and the North and South Pacific (including off Australia). They were the first to report B. bellones from the Red Sea, on Ablennes hians (Valenciennes), but they did not find this parasite on Tylosurus choram (Rüppell). Burmeister's original description (Burmeister, 1835) was rather rudimentary, but the adult female of B. bellones has subsequently been redescribed by numerous authors including Vervoort (1962), Cressey & Collette (1970), Kabata (1979) and Ho et al. (1983). The female is well characterised. However, the only description available of the male is that of Hartmann (1870) who provided a single illustration of an undissected male in ventral view. In the present work, the male B. bellones is described in detail, based on material obtained from Tylosurus choram caught in the Gulf of Suez.
The only previous report of B. minus is the original description based on material from five different host fishes landed in Taiwan (Lin & Ho, 2005). This species is very closely related to the poorly described species, B. indicus Kaliyamurthy, Singh & Singh, 1988 and may even be a junior synonym. The females from Egyptian waters are redescribed here to add to the body of morphological knowledge that will provide the evidence which will allow such questions of possible synonymy to be addressed.

Materials and methods
Host fish were purchased from local markets and examined for the presence of parasitic copepods. Copepods were removed from the host and preserved in 70% ethanol. The copepods were dissected and mounted in lactophenol as temporary slide preparations and examined on an Olympus microscope. Measurements were made using an ocular micrometer and drawings were made with the aid of drawing tube. Morphological terminology follows Huys & Boxshall (1991). Host names were validated against FishBase (Froese & Pauly, 2015).
Antennule (Fig. 1C) 7-segmented; proximal 4 segments only slightly more robust than distal 3 cylindrical segments. First segment with 5 robust pilose setae, none modified; second segment with 14 setae (6 robust pilose setae, 5 naked setae and 3 short plumose setae); third segment with 1 naked seta and 3 robust pilose setae; fourth segment with 1 naked seta and 2 robust pilose setae. Cylindrical distal segments with setal formula 4, 2?1ae and 7?1ae respectively; distal element on fifth segment longer than in female. Antenna ( Fig. 1D) uniramous, 3-segmented; comprising long proximal segment (coxobasis) bearing single long seta, short middle (= first endopodal) segment armed with small naked seta, and highly ornamented apical segment. Apical segment produced into blunt distal process ornamented with marginal row of blunt spinules continuous with row present along margin of apical segment, ventral surface of segment with multiple rows of hooked spinules. Apical segment armed distally with 4 curved claws, 3 naked setae and pectinate process bearing tiny naked seta.
Leg 4 ( Fig. 2D) biramous with 3-segmented exopod and 2-segmented endopod; outer margin spines on exopod segments finely bilaterally spinulate, each spine bearing subterminal flagellum. Inner seta on proximal endopodal segment about twice as long as ramus, extending almost to tip of long seta on distal segment; distal endopodal segment with inner apical spine longer than outer; apical seta about 1.5 times longer than ramus. Ornamentation of long setules present on outer margins of endopodal segments. Leg 4 coxa with spinules at outer distal angle.
Males of Bomolochus are found and reported less frequently than females. Currently males are known for just seven of the 20 valid species of Bomolochus: B. bellones, B. ensiculus (Cressey, in Cressey & Collette, 1970), B. globiceps (Vervoort & Ramirez, 1968), B. megaceros Heller, 1865, B. psettobius (Vervoort, 1962), B. soleae Claus, 1864 and B. xenomelanirisi Carvalho, 1955. In addition, Vervoort (1969) described an unidentified male as Bomolochus sp., although this specimen may well have been immature (Vervoort, 1969). The only description of male B. bellones is that of Hartmann (1870) which is supported by a single illustration of an undissected male, providing an inadequate level of detail. The detailed description presented here permits comparison with congeneric males.
Adult males of Bomolochus spp. are all smaller than their respective females. Sexual dimorphism is exhibited in urosomal segmentation (the formation of the genital somite and the number of free abdominal somites), in the antennule (the lack of the modified hook-like seta on the proximal segment in the male), the robust subchelate maxilliped of the male, the 2-segmented endopod of leg 4 in the male (3segmented in the female), and the presence of only two setal elements on the free exopodal segment of leg 5 in the male (compared to four setal elements in the female). The spine and setal formula for the exopods of legs 3 and 4 is also sexually dimorphic: adult males lack an outer spine on the second exopodal segment of both legs, whereas a spine is present in the females. There are additional differences in ornamentation: the male has extensive spinulation on the ventral surface of the first free abdominal and anal somites, on the caudal rami, and on the interpodal sclerites of legs 1 to 4. This enhanced spinular ornamentation presumably assists the male in holding the female during mating.
Leg 2 ( Fig. 5A-C) with 3-segmented rami; coxa with short inner coxal seta and ornamented with patch of setules at outer distal angle; basis with outer basal seta. All exopodal segments ornamented with patches of flattened scale-like spinules; all outer spines provided with subterminal flagellum; outer spine on first exopodal segment bilaterally spinulate, but outer margins of spines on second and third segments denticulate (Fig. 5A, B). Outer and inner margins of first exopodal segment ornamented with long setules. Endopodal segments very broad and flattened; outer margins of first and second segments ornamented with long setules and distal row of spinules, third segment with outer row of setules. Interpodal sclerite ornamented with row of long spinules.
Leg 3 (Fig. 5D) with 3-segmented rami; coxa and basis with short inner coxal seta and outer basal seta, respectively. Coxa lacking ornamentation at outer distal angle. Exopodal segments armed and ornamented as for leg 2. Endopodal segments less broad and less flattened than in leg 2; ornamentation as for leg 2. Interpodal plate ornamented with row of long spinules.  Leg 4 ( Fig. 5E) with 3-segmented rami; coxa lacking inner seta and ornamented with patch of spinules at outer distal angle; basis with outer basal seta. All exopodal segments ornamented with patches of flattened scalelike spinules; all outer spines denticulate and provided with subterminal flagellum (Fig. 5E). Outer margins of first and second endopodal segments ornamented with long setules and distal row of spinules. Inner seta on first endopodal segment short, extending nearly to middle of second segment. Inner seta on second endopodal segment extending to about 75% length of third segment; small spinules present at base of seta. Third segment with spinules present adjacent to base of outer and inner apical spines. Interpodal sclerite ornamented with row of long spinules.
Leg 5 (Fig. 5G) 2-segmented; protopodal segment small, ornamented with patch of spinules and armed with outer seta; free segment (exopod) armed with subterminal spine extending almost to end of segment, but not extending beyond distal margin (Fig. 5G, H), outer and inner terminal spines, plus naked seta in middle of distal margin; inner distal spine longer than outer (Fig. 5I). Exopod ornamented with patch of spinules extending along outer lateral margin, plus 2 distal patches.
Leg 6 ( Fig. 3A) represented by 3 short setae located in egg sac attachment area on genital double-somite.

Remarks
Only four nominal species of Bomolochus share the unusual scale-like ornamentation on the exopods of swimming legs 2 to 4, namely, B. decapteri Yamaguti, 1936, B. indicus Kaliyamurthy, Singh & Singh, 1988, B. minus and B. unicirrus Brian, 1902. The adult females of two of these species, B. decapteri and B. unicirrus, are characterised by the possession of patches of spinules on the ventral surface of both the anal somite and the caudal rami (cf. Yamaguti, 1936: figure 50;Ho & Rokicki, 1987: figure 1c). Bomolochus minus lacks such patches: indeed, the specific epithet ''minus'' specifically alludes to the absence of this ornamentation (Lin & Ho, 2005). Kaliyamurthy et al. (1988) do not mention any such patches of ornamentation on the anal somite or caudal rami, and while the overall quality of their description of B. indicus is low, it does mention the scale-like ornamentation (referred to as ''pustules'') on the exopods of legs 2 to 4, indicating that the authors were paying attention to such fine details. So we presume these spinule patches are absent in B. indicus also. Bomolochus indicus and B. minus are morphologically very similar, the body length given for the former (1.6 mm) lies within the range (1.52 to 2.00 mm) given for the latter, and both occur on the same host, Gerres filamentosus Cuvier (see Kaliyamurthy et al., 1988;Lin & Ho, 2005). The former also occurred on a second gerreid, Gerres limbatus Cuvier (as Gerres lucidus), while the latter also occurred on four sciaenids, Johnius belengerii (Cuvier), J. amblycephalus (Bleeker), Pennahia pawak (Lin), and Chrysochir aureus (Richardson). Despite sharing a common suite of characters and co-occurring on the gerreid host, G. filamentosus, these two species were not compared by Lin & Ho (2005) when they established their new species from Taiwan.
The key to species of Bomolochus created by Ho & Lin (2009) separates B. indicus and B. minus on the basis of the length of the modified, hook-like fourth seta on the proximal segment of the antennule of the female relative to the length of the adjacent fifth seta. In B. indicus the fourth seta protrudes well beyond the tip of the fifth seta, whilst in B. minus it does not. The interpretation of this character can be difficult as relative lengths can appear to vary according to the angle of observation: for example, in Lin & Ho's description (Lin & Ho, 2005) the dorsal view of the adult female of B. minus shows the fourth seta as markedly longer than the fifth, but in the ventral view of the antennule, they appear similar in length. In the Egyptian material the fourth seta is somewhat intermediate in length: in Fig. 3F the enlargement of the third, fourth and fifth setae, the hook-like fourth seta is shown extending a small distance beyond the tip of the fifth seta. On the basis of this character we identify the Egyptian material from Gerres oyena as B. minus, but we recommend that the B. indicus is fully redescribed to modern standards because we consider it possible that these two Bomolochus species are conspecific.

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