Abstract
There is increasing interest in the common sole, Solea solea (Linnaeus), as an alternative fish species in aquaculture in the Mediterranean region, and parasitic copepods are a potential hazard for farmed finfish. This paper provides taxonomic information on two species of sea lice (family Caligidae) collected from S. solea in eastern Mediterranean waters off the Turkish coast. Caligus brevicaudatus A. Scott, 1901 and Caligus apodus (Brian, 1924) were both found and this is the first report of C. brevicaudatus in Turkish waters. The discovery of C. apodus on S. solea is a new host record. Key diagnostic characters of both species are reported, supported by light and scanning electron microscopy observations. During a 12-month survey a prevalence of 28% was recorded for C. brevicaudatus, whereas for C. apodus peak prevalence was much lower (3%).
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Introduction
The common sole, Solea solea (Linnaeus), is one of the most economically important fish species in the Mediterranean due to its high market value. Since about 30 years ago, this flat fish has been considered one of the most promising species for marine aquaculture (Imsland et al., 2009) and, to the best of our knowledge, at least three fish farming companies have recently started cultivation trials in Turkey. The successful commercialization of sole aquaculture will require improved knowledge of diseases and the development of parasite and disease management strategies.
At least one viral (Viral nervous necrosis) and five bacterial (Blackpatch necrosis, Vibriosis, Tailrot, Furunculosis and Redspot) diseases have thus far been reported during the cultivation trials of common sole (Flütchter, 1979; Baudin-Laurencin, 1986; Bernadet et al., 1990; Starkey et al., 2001; Imsland et al., 2003). In addition, many parasite species including haemoflagellates, ichthyobdellid leeches, trematodes, isopods and copepods have been reported from S. solea across its range (Claus, 1864; Slinn, 1970; Boxshall, 1974; Kirmse, 1987; Palm et al., 1999; Kabata, 2003; Kayis and Ceylan 2011). Among these groups of parasites infecting S. solea, the copepods, with nine species reported, are the most species rich.
Parasitic copepods are known as disease causing agents in marine and brackish-water fish culture (e.g. Cruz-Lacierda et al., 2011). In particular, species belonging to the family Caligidae, the sea lice, cause high mortalities in aquaculture (Johnson et al., 2004) and may also serve as vectors for other disease agents (Nylund et al., 1994). Sea lice also adversely affect growth rate and fecundity of marine fish in culture species, as has recently been emphasised in disease reports worldwide (e.g. Johnson et al., 2004; Lester & Hayward, 2006; Cruz-Lacierda et al., 2011). The aim of this research was to determine which sea lice species naturally infect S. solea in the eastern Mediterranean off the Turkish coast. A one-year parasitological survey was conducted in İskenderun Bay, Turkey. Morphological examination of the collected parasites revealed the presence of two species of caligids: Caligus brevicaudatus Scott, 1901 and Caligus apodus (Brian, 1924) both of which inhabited the upper surface of S. solea. Their characteristic features are briefly described.
Materials and methods
A one-year (December 2011–December 2012) parasitological survey was conducted to determine which parasitic copepods were present on Solea solea (L.) in İskenderun Bay, Turkey. Fish were caught monthly by Sole trammel nets in İskenderun Bay, near Yumurtalık (36°45′30.11″N, 35°43′08.75″E), Karataş (36°30′01.88″N, 35°23′14.60″E) and Konacık (36°21′51.23″N, 35°45′46.74″E). The body surface (upper and lower), gill cavities and gill filaments of the fish were examined. The fish (n = 3,316) ranged in total length from 11 to 23 cm.
Parasitic copepods were collected from the upper body surface of the infested fish and immediately preserved in 70% ethyl alcohol. Specimens were cleared in lactic acid for 2 h prior to examination using an Olympus SZX16 dissecting microscope and Olympus BX51 compound microscope. Intact specimens and individual appendages were photographed with a digital camera on both microscopes. The scientific and common names of fishes follow Froese & Pauly (2013) and the morphological terminology for the copepods follows Huys & Boxshall (1991). All measurements are in millimetres unless otherwise stated.
The protocols for preparing crustaceans for scanning electron microscopy (SEM) outlined by Felgenhauer (1987) were followed. Ethanol-fixed specimens were hydrated to distilled water and post-fixed in 1–2% osmium tetroxide (OsO4) in buffer for 2 h, washed in distilled water, dehydrated through graded acetone series, critical point dried using liquid carbon dioxide as the exchange medium, mounted on aluminium stubs and sputter coated with platinum. Coated specimens were examined on a Zeiss Supra 55 (FE-SEM, Germany) field emission scanning electron microscope at 1–3 kV.
Results
Two species of Caligus were found. Caligus brevicaudatus was originally described by A. Scott (1901) and subsequently redescribed by Kabata (1979) and Choi et al. (1995). Caligus apodus was originally described by Brian (1924) (as Pseudocaligus apodus) and subsequently redescribed by Brian (1935) and Ben Hassine (1983). Here, only the characteristics important for accurate identification are highlighted and illustrated by light and scanning electron micrographs.
Caligus brevicaudatus A. Scott, 1901
Material examined
Collection of the Natural History Museum, London: 32 females collected from mouth of Chelidonichthys lucerna (Linnaeus) (as Trigla lucerna) in Luce Bay, 1912 and submitted by T. & A. Scott (BMNH Reg. Nos 1913.9.18.77-86).
Newly collected material: Twenty-nine ovigerous females collected from the upper surface of Solea solea (L.) caught in İskenderun Bay, Turkey were examined. Five female C. brevicaudatus are deposited at the Natural History Museum, London (BMNH 2013.68-72); the remaining parasites are in the personal collection of the first author.
Prevalence: 28% (928 of 3,316 hosts parasitised) over the 12-month period of study.
Description (Figs. 1–2)
Adult female. Total body length 3.82 (3.48–4.1) (n = 10); cephalothorax longer than wide, 2.01 × 1.7; genital complex (Fig. 1B) subrectangular, longer than wide, 1.45 × 1.36, about 5.8 times longer than 1-segmented abdomen (Fig. 1C), 0.25 × 0.35 mm. Genital complex with distinctive ornamentation of about 8 compound sensillae aligned along lateral margins of genital complex (Fig. 1B, inset); abdomen ornamented with sensillae and with patch of spinules on central part of ventral surface (Fig. 1C, insets). Cephalothorax 1.7, approximately 1.18 times longer than combined length of genital complex and abdomen. Caudal rami (Fig. 1D) each with 6 pinnate setae plus fringe of pinnules along inner margin; outermost seta about twice as long as adjacent seta (Fig. 1D, inset).
Sternal furca with slightly diverging tines, with blunt tips, and square box (Fig. 1E). Maxilliped (Fig. 1F) comprising robust protopod (corpus) with smooth medial margin; distal subchela armed with short, tapering claw carrying single seta more than half length of claw (Fig. 1F, inset). Swimming leg 1 (Fig. 2A) biramous; with 2-segmented exopod and vestigial, lobate endopod. Protopod (Fig. 2A, inset) armed with plumose seta on anterodistal corner and plumose seta on posteromedial margin, ornamented with patch of spinules on ventral surface near base. Distal exopodal segment (Fig. 2B) with 4 terminal elements about equal in length, outermost element (spine 1) finely serrated on inner margin (Fig. 2B, inset), middle two elements (spines 2 and 3) each bearing single accessory process, and ornamented with fine serrations along inner and outer margins, innermost element (seta 4) at inner distal angle, unarmed; posterior margin with 3 long plumose setae. Leg 4 uniramous, comprising protopod plus 2-segmented exopod. Protopod armed with long outer plumose seta and ornamented with multi-sensillate papilla. Exopod (Fig. 2C) slender; first exopodal segment bearing finely serrated outer distal spine, terminal segment with 3 finely serrated, unequal apical setae (Fig. 2C, inset). Spine (Roman numerals) and seta (Arabic numerals) formula of legs 1–4 as follows:
Exopod | Endopod | |
---|---|---|
Leg 1 | I-0; III, I, 3 | vestigial |
Leg 2 | I-1; I-1; II, I, 5 | 0–1; 0–2; 6 |
Leg 3 | I-0; I-1; III, 4 | 0–1; 6 |
Leg 4 | I-0; III | absent |
Leg 5 (Fig. 2D) comprising single seta on isolated papilla (Fig. 2D, inset) plus papilla with 2 setae, about equal in length, located on posterolateral margin of genital complex. Bifid sensillae present on body surface in vicinity of leg 5 papillae.
Remarks
Caligus brevicaudatus was first reported as parasitic on Eutrigla gurnardus (Linnaeus) from Liverpool Bay by A. Scott (1901). It was subsequently also reported from Chelidonichthys lucerna (Linnaeus) in British waters (Scott & Scott, 1913; Scott, 1929). Caligus brevicaudatus has also been reported from other parts of the world, including the Baltic Sea, Table Bay (South Africa), the Barents Sea (Russia), the Gulf of Naples (Italy), Kamak Bay (Korea), the Gulf of Tunisia (Tunisia), the North Sea and from off the Portuguese Coast (van Oorde-de Lint & Schuurmans Stekhoven 1936; Barnard, 1955; Markevich, 1956; Reichenbach-Klinke, 1956; Rohde, 1980; Choi et al., 1995; Benmansour & Ben Hassine, 1997; Palm et al., 1999; Marques et al., 2006, 2009). Although C. brevicaudatus has most commonly been reported from gurnards (family Triglidae), it has also been found on two flatfish species: Paralichthys olivaceus (Temminck & Schlegel) and S. solea (see Choi et al., 1995; Marques et al., 2009).
The morphological characteristics of our adult females were similar to those of C. brevicaudatus, as described by A. Scott (1901), Kabata (1979) and Choi et al. (1995). In particular, the similarities included: (i) the subrectangular shape of the genital complex; (ii) the presence of about eight sensillae along the lateral margins of the genital complex; and (iii) the short 1-segmented abdomen. In addition, the ornamentation and setation of legs 1 and 4 were identical in fine detail. We also report two previously unrecognised characters which are of taxonomic value. First, there is a patch of spinules on the central part of the ventral surface of abdomen (see Fig. 1C, insets); and secondly, there is a patch of fine spinules on the ventral surface of the basal part of leg 1 (Fig. 2A, inset).
Our Turkish specimens have a smaller mean body length of 3.82 mm when compared with the previous measurements reported from Korea (4.06 mm) and Britain (5.30 mm), respectively (Choi et al., 1995; A. Scott, 1901). Detailed comparison between the Turkish specimens and the specimens identified and presented by T. & A. Scott, stored in the collection of the Natural History Museum, London (BMNH Reg. Nos. 1913.9.18.77-86), revealed close similarities in all morphological features and in body proportions. However, the re-measured mean total body length of Scott’s females was 4.48 mm (4.13–4.76) (n = 10), about 1.2 times longer than the Turkish females. In the absence of any significant differences in limb structure, setation and ornamentation, we infer that the size differences represent geographical variation. Such a size difference between the British and Mediterranean specimens may be correlated with temperature differences.
In the redescription of C. brevicaudatus from Korea (Choi et al., 1995) the outermost two setae of the caudal rami were illustrated as equal in length but in the Turkish material, our SEM images showed these two outermost setae as very unequal in length (Fig. 1D, inset). Again, in the absence of other differences, we interpret this as representing regional variation.
Caligus apodus (Brian, 1924)
Syns Pseudocaligus apodus Brian, 1924; Pseudolepeophtheirus mediterraneus Paperna, 1964
Material examined
Two syntype females, MNHN-Cp-267, collected by A. Brian on 3 January 1923 (Brian, 1924). The data on the label in the vial are “sur Mugil cephalus, 3-1-23”.
One syntype female, MNHN-Cp-269, collected by A. Brian on 13 August 1923 (Brian, 1924). The data on the label in the vial are “squalide 402, surpeaudorsale, 13 août 1923”.
Five females and three males from upper surface of Solea solea (L.) caught in İskenderun Bay, Turkey were examined. Two females and one male C. apodus are stored at the Natural History Museum, London (BMNH 2013.73-75); the remaining parasites are in the personal collection of the first author.
Prevalence: 3% (99 of 3,316 hosts parasitised) over the 12-month period of study.
Description (Figs. 3-6)
Adult female. Total body length 4.30 (4.22–4.38) (n = 5), with suborbicular cephalothorax and slightly longer than wide, 2.06 × 2.03. Fourth pedigerous somite (Fig. 3B) wider than long, 0.23 × 0.41, and without trace of fourth leg; surface ornamented with 2 sensillate papillae in mid-margin plus spiniform structure posterolaterally (Fig. 3C). Genital complex (Fig. 3D) as long as wide, 0.94 × 0.94, tapering gradually anteriorly and with rounded posterolateral corners. Abdomen 1-segmented, 0.89 × 0.38, about four times longer than caudal rami. Caudal rami longer than wide, 0.22 × 0.13. Cephalothorax 2.06 long, slightly longer than combined length of genital complex and abdomen, 1.83 mm. Tines of sternal furca slightly incurved, spatulate, with rounded tips (Fig. 3E). Swimming leg 1 biramous, with 2-segmented exopod and vestigial endopod. Protopod armed with lateral plumose seta and short medial seta (both derived from basis) and ornamented with patch of fine spinules (Fig. 4A). Lobate endopod (Fig. 4B) with single tiny spine-like vestige at tip (Fig. 4B, inset). First exopodal segment fringed with row of setules on inner margin, and bearing small spine at outer distal corner. Terminal exopodal segment (Fig. 4C) with 3 unequal plumose setae on inner margin, plus 4 spiniform elements about equal in length along distal margin. Outermost element (spine 1) and middle 2 elements (spines 2 and 3) finely serrated along margins, element (seta 4) at inner distal angle, unarmed. Spine (Roman numerals) and seta (Arabic numerals) formula of legs 1–4 as follows:
Exopod | Endopod | |
---|---|---|
Leg 1 | I-0; III, I, 3 | vestigial |
Leg 2 | I-1; I-1; II, I, 5 | 0–1; 0–2; 6 |
Leg 3 | I-0; I-1; III, 4 | 0–1; 6 |
Leg 4 | vestigial | absent |
Leg 5 (Fig. 4D) comprising single papilla with 3 plumose setae; sensillate papillae present on body surface in vicinity of leg.
Male (Fig. 5A). Total body length 3.19 (3.17–3.21) (n = 3), with suborbicular cephalothorax slightly longer than wide, 1.59 × 1.32. Fourth pedigerous somite (Fig. 5B) wider than long, 0.17 × 0.35, carrying paired vestige of fourth legs posterolaterally (Fig. 5C). Genital complex (Fig. 5D) wider than long, 0.57 × 0.64, bearing two protrusions on posterior margin; abdomen 0.54 × 0.32, 1-segmented. Cephalothorax about 1.43 times longer than combined length of genital complex and abdomen. Caudal rami longer than wide, 0.20 × 0.13. Antenna (Fig. 5F) 3-segmented; middle segment bearing 2 broad adhesion pads; distal segment terminating in 3 overlapping cuticular flaps, each with rounded free margin, armed with 2 unequal slender setae. Maxilliped (Fig. 6A) with robust corpus produced into conspicuous bifid-pointed process on myxal margin; shaft claw more than half length of corpus, armed with seta at base of claw (Fig. 6A, inset). Tines of sternal furca (Fig. 5E) almost parallel, slightly longer (0.14) than rectangular box (0.12), rounded at tip. Leg 4 reduced, indistinctly 3-segmented, located posterolaterally on somite (Fig. 5C). Middle segment bearing 1 pinnate spine at outer distal corner, terminal segment with 3 unequal spiniform elements at apex (Fig. 5C, inset), lateral margins of outer and middle spines finely serrated, serrations very small; innermost element shortest and unarmed. Leg 5 (Fig. 6B) represented by single papilla on posterolateral margin of genital complex bearing single spiniform, posteriorly-curved process; body surface ornamented with patches of spinules in vicinity of papilla (Fig. 6B, inset). Leg 6 (Fig. 6C) comprising papilla carrying 3 plumose setae located on posterolateral corner of genital complex, ornamented with dorsolateral patch of spinules on surface (Fig. 6C, inset).
Remarks
Caligus apodus was first described by Brian (1924) as Pseudocaligus apodus and was recorded on Mugil cephalus (Linnaeus) and Galeorhinus galeus (Linnaeus) (as Eugaleus galeus) caught off the coast of Mauritania (Brian, 1924). No type was designated but the description was based on a female of length “environs 5 mm” which is the length given in the text for the four specimens from M. cephalus (L.). We conclude that the type-host is M. cephalus (L.). The report from an elasmobranch host is atypical and we consider it most likely to represent contamination within the net by host transfer while the fish were being landed. The type-series as listed by Brian (1924) comprised five females and no males.
Subsequently this parasite was reported on different members of the Mugilidae from around the coast of Africa, from different parts of the Mediterranean, and from further afield (Rose & Vaissiere, 1953; Rangnekar, 1955; Capart, 1959; Paperna, 1964; Paperna & Lahav, 1971, 1974; Raibaut et al., 1971; Paperna, 1975; Raibaut & Ben Hassine, 1977; Braun, 1981; Paperna & Overstreet, 1981; Radujkovic, 1982; Altunel, 1983; Ben Hassine, 1983; Arru et al., 1988; Ragias et al., 2004). Paperna (1964) described Pseudolepeophtheirus mediterraneus Paperna, 1964 on the basis of material from Liza ramada (Risso) (as Mugil capito), but Paperna & Lahav (1974) subsequently recognised this species to be a synonym of P. apodus, as was later confirmed by Raibaut & Ben Hassine (1977). The synonymy of Pseudocaligus A. Scott, 1901 and Caligus O.F. Müller, 1785 is reviewed in the discussion below.
Pseudocaligus apodus Brian, 1924, was placed in the genus Pseudocaligus A. Scott, 1901 due to the complete absence of the fourth leg in the female. However, Ben Hassine (1983) redescribed P. apodus based on specimens collected from grey mullets caught off Tunisia and noted the presence of vestigial fourth legs in both females and males. In contrast to Ben Hassine (1983), we did not observe even a trace of the fourth leg in our females (Fig. 3B). In addition, our females are distinguishable from the Tunisian material in the possession of a sternal furca which has its tines slightly inwardly curved (vs slightly divergent); the swimming leg 1 has a vestigial endopod bearing only one tiny but noticeable spiniform process on its apex (vs one small spiniform process plus two minute denticle-like structures) and is ornamented with a patch of spinules on the protopod (vs none); and leg 5 comprises a single papilla carrying three plumose setae (vs a setate papilla plus an anterior spine).
We also observed differences between our males and the description of the male given by Ben Hassine (1983). These include: the maxilliped claw bears only a single seta at its base (vs one seta plus a minute second seta anteriorly), the tips of the two myxal processes lack any ornamentation (vs ornamented with tiny denticles); the distal segment of the antenna consists of three overlapping cuticular flaps with rounded free margins (vs sharply pointed tips) and is armed with two slender basal setae (vs one slender basal seta plus two equal small denticles); the postantennal process bears two multi-sensillate papillae plus one similar multi-sensillate single papilla (vs plus three) located on body surface adjacent to postantennal process; leg 5 comprises a papilla carrying a single, posteriorly-curved spiniform process on the posterolateral margin of the genital complex (vs a single papilla carrying three plumose setae at the posterolateral corner of the genital complex); and leg 6 comprises a papilla sited at the posterolateral corner of the genital complex and carrying three plumose setae (vs with two small knob-like processes on the posterior margin of the genital complex).
The presence or absence of a vestigial fourth leg in females of P. apodus was the major discrepancy observed between the Turkish and Tunisian material. In the original description Brian (1924) emphasised the complete absence of the fourth legs in females. We re-examined the type-material of Pseudocaligus apodus Brian, 1924 stored in the Muséum national d’Histoire naturelle in Paris. There were two lots: MNHN-Cp-267, which contained two ovigerous adult females, one of which was distorted in preservation and could not be readily observed, and MNHN-Cp-269, which contained a single adult female. No males were present in the type-series. Close examination of the female syntypes revealed that one of the two females had no trace of the fourth leg while the second female carried a minute, rod-like trace of a possible fourth leg on one side only of the pedigerous somite. Both females were ornamented with two sensillate papillae plus a spiniform structure located near the posterolateral corner of the fourth pedigerous somite, identical to that reported here for females from Turkish waters (Fig. 3C). In addition, other morphological features of adult females from Turkey were similar both in shape and morphometrics to the re-examined syntypes. However, the Turkish females differed slightly in having a smaller body length from those reported from Mugil cephalus (L.) by Brian (1924) (4.30 vs 5.00 mm).
The general morphology and body proportions of Turkish males of P. apodus were also similar to Brian’s (1935) description, based on material from M. cephalus (L.) and Mugil sp. from Italy, although the total body length of our male is slightly shorter than Brian’s (1935) (3.19 vs 4.00 mm). The vestigial fourth leg of our males carried three unequal, spiniform terminal elements at the apex while Brian (1935) described his males as carrying two spiniform terminal elements. We were unable to confirm the validity of this difference, in the absence of male syntypes.
Discussion
Kabata (1965) expressed strong reservations concerning the validity of using the state of the fourth legs as a generic-level character, diagnostic for the genera Pseudocaligus and Pseudolepeophtheirus Markevich, 1940. He considered that Pseudocaligus and Pseudolepeophtheirus should probably be synonymised with their respective related genera, Caligus and Lepeophtheirus von Nordmann, 1832. Ben Hassine (1983) also noted the lack of any significant differences between Caligus and Pseudocaligus. She placed P. apodus in the genus Caligus and used the combination Caligus apodus. Finally, Kabata’s suggestions (Kabata, 1965, 1979) concerning the relegation of the genera Pseudocaligus to synonymy with the genus Caligus were revisited by Dojiri & Ho (2013) who formally recognised Pseudocaligus as a junior synonym of Caligus; however, they did not deal with the nomenclatural problems arising from that decision.
As a consequence of the genus-level synonymy, Pseudocaligus brevipedis (Bassett-Smith, 1896) and P. parvus (Bassett-Smith, 1898) revert to their original combinations of Caligus brevipedis Bassett-Smith, 1896 and C. parvus Bassett-Smith, 1898, respectively. Pseudocaligus apodus Brian, 1924 becomes Caligus apodus (Brian, 1924), as already proposed by Ben Hassine (1983). Three more species become new combinations: Pseudocaligus subparvus Hameed, 1977 becomes Caligus subparvus (Hameed, 1977), Pseudocaligus laminatus Rangnekar, 1955 becomes Caligus laminatus (Rangnekar, 1955), and Pseudocaligus uniartus Ho, Kim, Cruz-Lacierda & Nagasawa, 2004 becomes Caligus uniartus (Ho, Kim, Cruz-Lacierda & Nagasawa, 2004). However, three species of Pseudocaligus become secondary homonyms as a result of the generic level synonymy between Pseudocaligus and Caligus (see Dojiri & Ho, 2013): Pseudocaligus fistulariae Pillai, 1961 and Caligus fistulariae Yamaguti, 1936, Pseudocaligus fugu Yamaguti, 1936 and Caligus fugu Yamaguti & Yamasu, 1959, and Pseudocaligus indicus Hameed, 1977 and Caligus indicus Pillai, 1967.
In the first of these examples, Caligus fistulariae Yamaguti, 1936 has priority and so a substitute name is required for Pseudocaligus fistulariae Pillai, 1961 on transfer. According to Article 60.2 of the International Code for Zoological Nomenclature if a rejected junior homonym has available valid synonyms, then the oldest of these becomes the valid name of the taxon. In this case Pseudocaligus tenuicauda Shiino, 1964, which was placed in the synonymy of Pseudocaligus fistulariae by Pillai (1985), is the oldest available valid name. The new combination Caligus tenuicauda (Shiino, 1964) thus becomes the valid name for the junior secondary homonym Pseudocaligus fistulariae Pillai, 1961.
In the case of the secondary homonymy resulting from the transfer of Pseudocaligus fugu Yamaguti, 1936 to Caligus, it is Caligus fugu Yamaguti & Yamasu, 1959 that becomes the junior homonym. In the recent revision of the Caligus productus group by Boxshall & El-Rashidy (2009) Caligus lagocephali Pillai, 1961 was treated as a subjective synonym of Caligus fugu Yamaguti & Yamasu, 1959. Since Caligus fugu Yamaguti & Yamasu, 1959 is the junior secondary homonym, the oldest available valid name for this taxon is Caligus lagocephali Pillai, 1961 as pointed out to us by Freeman & Ogawa (pers. comm.).
In the third case of homonymy, Caligus indicus Pillai, 1967 retains priority as the senior homonym, even though it has been treated as a subjective synonym of Caligus cossacki Bassett-Smith, 1898. Pseudocaligus indicus Hameed, 1977 becomes the junior secondary homonym upon transfer and requires a replacement name. We propose the substitute name Caligus keralensis nom. nov. as it was reported from Kerala, India.
References
Altunel, F. N. (1983). [Parasitism in Mugil spp.] Ege University, Faculty of Science Journal, Series B, Supplement. 364-378 (in Turkish).
Arru, E., Leoni, A., & Garippa, G. (1988). Contributo alla conoscenza della parassitofauna dei pesci delle acque costiere ed interne della Sardegna. Parassitologia, 30, (suppl. 1), 14–16.
Barnard, K. H. (1955). South African Parasitic Copepoda. Annals of the South African Museum, 41, 223–312.
Baudin-Laurencin, F. (1986). Sensitivity of the sole (Solea solea) to vibriosis. In: Vivares, C. P., Bonami, J. R. & Jaspers, E. (Eds.), Pathology in Marine Aquaculture. Special Publication no. 9. Bredene, Belgium: European Aquaculture Society, pp. 345–350.
Ben Hassine, O. K. (1983). Les Copépodes parasites de Poissons Mugilidae en Mediterranée occidentale (côtes françaises et tunisiennes). Univ. Montpellier II, These d’Etat, 452 pp.
Benmansour, B., & Ben Hassine, O. K. (1997). Première mention en Tunisie de certains Caligidae et Lernaeopodidae (Copepoda) parasites de poisons Téléostéens. Ichtyophysiological Acta, 20, 157–175.
Bernadet, J. F., Campbell, A. C., & Buswell, J. A. (1990). Flexibacter maritimus is the agent of "black patch necrosis" in Dover sole in Scotland. Diseases of Aquatic Organisms, 8, 233–237.
Boxshall, G. A. (1974). Infections with parasitic copepods in North Sea marine fishes. Journal of the Marine Biological Association of the United Kingdom, 54, 355–372.
Boxshall, G. A., & El-Rashidy, H. H. (2009). A review of the Caligus productus species group with a new species, new synonymies and supplementary descriptions. Zootaxa, 2271, 1–26.
Braun, M. (1981). Contribution à l’étude biologique des zones à salinité variable du littoral méditerranéen français: Copépodes parasites de Mugilidés. Thèse 3e cycle, U.S. T.L. Montpellier, France, 88 pp.
Brian, A. (1924). Arthropoda (1ére partie) Copepoda. Copépodes commensaux et parasites des côtes mauritaniennes. Parasitologia Mauritanica. Bulletin du Comité d’Études Historiques et Scientifiques de l’Afrique Occidentale Française, 364–427.
Brian, A. (1935). Caligus parassiti dei pesci del Meditterraneo (copepodi). Annali del Museo Civico di Storia Naturale ‘Giacomo Doria’, 57, 152–211.
Capart, A. (1959). Copépodes parasites. Expédition Océanographique Belge dans les Eaux Côtières Africaines de l’Atlantique Sud (1948–1949): Résultats Scientifiques. Institut Royal des Sciences Naturelles de Belgique: Bruxelles, Belgium, 3, 55–126.
Choi, H. S., Hong, S. Y., & Lee, J. M. (1995). Two species of Caligus (Siphonostomatoida, Copepoda) parasitic on marine cultured fishes from Kamak Bay in Korea. Bulletin of National Fisheries Research and Development Agency (Korea), 49, 157–165.
Claus, C. (1864). Beiträgezur Kenntnis der Schmarotzer krebse. The Genus Bomolochus and its relatives. Zeitschrift für Wissenschaftliche Zoologie, 14, 365–383.
Cruz-Lacierda, E. R., Pagador, G. E., Yamamoto, A., & Nagasawa, K. (2011). Parasitic caligid copepods of farmed marine fishes in the Philippines. In: Bondad-Reantaso, M. G., Jones, J. B., Corsin, F. & Aoki, T. (Eds.), Diseases in Asian Aquaculture VII Selangor, Malaysia: Fish Health Section, Asian Fisheries Society, pp. 53–62.
Dojiri, M., & Ho, J.-S. (2013). Systematics of the Caligidae, copepods parasitic on marine fishes. Crustaceana Monographs, 18, 1–448.
Felgenhauer, B. E. (1987). Techniques for preparing crustaceans for scanning electron microscopy. Journal of Crustacean Biology, 7, 71–76.
Flütchter, J. (1979). Identification and treatment of diseases in the common sole (Solea solea L.). Aquaculture, 16, 271–274.
Froese, R., & Pauly, D. (Eds.) (2013). Fish Base. World Wide Web electronic publication. www.fishbase.org [10 May 2013].
Huys, R., & Boxshall, G. A. (1991). Copepod evolution. London: The Ray Society. 468 pp.
Imsland, A. K., Foss, A., Conceicao, L. E. C., Dinis, M. T., Delbare, D., Schram, E., et al. (2003). A review of the culture potential of Solea solea and S. senegalensis. Reviews in Fish Biology and Fisheries, 13, 379–407.
Imsland, A. K., Foss, A., & White, P. (2009). Sole show culture potential in Europe. Global Aquaculture Advocate, 5, 39–40.
Johnson, S. C., Treasurer, J. W., Bravo, S., Nagasawa, K., & Kabata, Z. (2004). A review of the impact of parasitic copepods on marine aquaculture. Zoological Science, 43, 229–243.
Kabata, Z. (1965). Copepoda parasitic on Australian fishes, IV. Genus Caligus (Caligidae). Annals and Magazine of Natural History, 13, 211–226.
Kabata, Z. (1979). Parasitic Copepoda of British Fishes. London: The Ray Society, 468 pp.
Kabata, Z. (2003). Copepods parasitic on fishes. In: Crothers, J. & Hayward, P. J. (Eds), Synopses of the British Fauna. Shrewsbury: Field Studies Council, 264 pp.
Kayis, S., & Ceylan, Y. (2011). First report of Nerocilaorbigyni (Crustacea, Isopoda, Cymothoidae) on Solea solea (Teleostei, Soleidae) from Turkish Sea. Turkish Journal of Fisheries and Aquatic Sciences, 11, 169–171.
Kirmse, P. (1987). Important parasites of dover sole (Solea solea L.) kept under mariculture conditions. Parasitology Research, 73, 466–471.
Lester, R. J. G., & Hayward, C. J. (2006). Phylum Arthropoda. In: Woo, P. T. K. (Ed.), Fish Diseases and Disorders, Vol. 1. Protozoan and Metazoan Infections (2nd edn.). Oxford: CABI Publishing, pp. 463–562.
Markevich, A. P. (1940). Neue Arten parasitischer Copepoden. Dopovidi Akademiyi Nauk Ukrayins’koiy RSR, Kiev, 11, 11–21 (In Russian).
Markevich, A. P. (1956). [Parasitic Copepods on the Fishes of USSR]. Kiev: Izdatel’stvo Akademii Nauk Ukrainskoi SSR, 259 pp (In Russian).
Marques, J. F., Teixeira, C. M., & Cabral, H. N. (2006). Differentiation of commercially important flatfish populations along the Portuguese coast: evidence from morphology and parasitology. Fisheries Research, 81, 293–305.
Marques, J. F., Santos, M. J., & Cabral, H. N. (2009). Zoogeographical patterns of flatfish (Pleuronectiformes) parasites in the Northeast Atlantic and the importance of the Portuguese coast as a transitional area. Scientia Marina, 73, 461–471.
Nylund, A., Hovlund, T., Hodneland, K., Nilsen, F., & Lervik, P. (1994). Mechanisms of transmission of infectious salmon anaemia (ISA). Diseases of Aquatic Organisms, 19, 95–100.
Palm, H. W., Klimpel, S., & Bucher, C. (1999). Checklist of metazoan fish parasites of German coastal waters. Berichte aus dem Institut für Meeres kundean der Christian-Albrechts-Universität Kiel, no. 307.
Paperna, I. (1964). Parasitic Crustacea (Copepoda and Branchiura) from inland water fishes of Israel. Israel Journal of Zoology, 13, 58–68.
Paperna, I. (1975). Parasites and disease of the grey mullet (Mugilidae) with special reference to the seas of the near east. Aquaculture, 5, 65–80.
Paperna, I., & Lahav, M. (1971). New records and further data on fish parasites in Israel. Badmidgeh, 23, 43–52.
Paperna, I., & Lahav, M. (1974). Mortality among grey mullets in a seawater pond due to caligid parasitic copepod epizootic. Bamidgeh, 26, 12–15.
Paperna, I., & Overstreet, R. M. (1981). Parasites and diseases of mullets (Mugilidae). In: Oren, O.H. (Ed.), Aquaculture of grey mullets. Cambridge: Cambridge University Press, pp. 411–493.
Pillai, N. K. (1961). Copepods parasitic on South Indian fishes Part 1 Caligidae. Bulletin of the Central Research Institute, 8, 87–130.
Radujkovic, B. (1982). Parasito faune de Muges de l’Adriatique (Chelon labrosus Risso., Liza aurata Risso et Liza saliens Risso) et son influence sur la condition des hôtes. XXVIIP Congrès CIESMM, Cannes, 2–11.
Ragias, V., Tontis, D., & Athanassopoulou, F. (2004). Incidence of an intense Caligus minimus Otto 1821, C. pageti Russel, 1925, C. mugilis Brian, 1935 and C. apodus Brian, 1924 infection in lagoon cultured sea bass (Dicentrarchus labrax L.) in Greece. Aquaculture, 242, 727–733.
Raibaut, A., & Ben Hassine, O. K. (1977). Les copépodes parasites des muges en Méditeranée. Bulletin du Muséum d’Histoire Naturelle de Paris. sér. 3 Zool., 329, 833–848.
Raibaut, A., Ben Hassine, O. K., & Maamouri, K. (1971). Copepodes parasites des poissons de Tunisie (premiére série). Bulletin de l’Institut des Pêches Maritimes du Maroc Salammbo, 2, 169–197.
Rangnekar, M. P. (1955). Pseudocaligus laminatus sp. nov. and Diphyllogaster aliuncus sp. nov. (Copepoda) parasitic on Bombay fishes. Journal of the University of Bombay, 23, 44–52.
Reichenbach-Klinke, H. H. (1956). Vorläufige Mitteilung über die Parasiten der Fisch des Golfes von Neapel. Pubblicazioni Della Stazione Zoologica di Napoli, 30, 115–126.
Rohde, K. (1980). Comparative Studies on Microhabitat Utilization by Ectoparasites of some Marine Fishes from the North Sea and Papua New Guinea. Zoologischer Anzeiger, 204, 27–63.
Rose, M., & Vaissiere, R. (1953). Catalogue preliminaire des copepodes de 1’Afrique du Nerd. Le Bulletin de la Société d’histoire naturelle d’Afrique du Nord, 44, 83–99.
Scott, A. (1901). Some additions to the fauna of Liverpool Bay, collected May 1st, 1900, to April 30th, 1901. Proceedings and Transactions of the Liverpool Biological Society, 15, 342–353.
Scott, A. (1929). The copepod parasites of Irish Sea fishes. Proceeding and Transactions of the Liverpool Biological Society, 43, 81–119.
Scott, T., & Scott, A. (1913). The British parasitic Copepoda. Volumes I and II. London: Ray Society, 252 pp.
Slinn, J. D. (1970). An infestation of adult Lernaeocera (Copepoda) on wild sole, Solea solea, kept under hatchery conditions. Journal of the Marine Biological Association of the United Kingdom, 50, 787–800.
Starkey, W. G., Ireland, J. H., Muir, K. F., Jenkins, M. E., Roy, W. J., Richards, R. H., & Ferguson, H. W. (2001). Nodavirus infection in Atlantic cod and Dover sole in the UK. Veterinary Research, 146, 179–181.
van Oorde-de Lint, G. M., & Schuurmans Stekhoven, J. H. (1936). Copepoda Parasitica. Tierwelt der Nord-und Ostsee, 31, 73–197.
Acknowledgements
We would like to thank Dr. Danielle Defaye (MNHN, Paris) for allowing one of us (GAB) to examine the type material of Pseudocaligus apodus stored in the collections in Paris. We also would like to thank Prof. Suphan Karaytuğ from Mersin University, Turkey for his support during our scanning electron microscope studies. We are also grateful to Professor Kazuo Ogawa and Dr Mark Freeman for sharing their earlier conclusions concerning the homonymy of Caligus fugu. This research was funded by the Çukurova University academic research projects unit (Project No. SUF2010BAP4).
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Özak, A.A., Demirkale, İ., Boxshall, G.A. et al. Parasitic copepods of the common sole, Solea solea (L.), from the Eastern Mediterranean coast of Turkey. Syst Parasitol 86, 173–185 (2013). https://doi.org/10.1007/s11230-013-9441-8
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DOI: https://doi.org/10.1007/s11230-013-9441-8