INTRODUCTION
Cymothoids are a family of ectoparasitic isopods found on body, fins, or inside the buccal or branchial cavities of numerous freshwater and marine fish. They are protandrous hermaphrodite. The settling male will first increase in size and, after mating, will change to the female stage (Mayer, Reference Mayer1879; Montalenti, Reference Montalenti1941, Reference Montalenti1948; Juchault & Legrand, Reference Juchault and Legrand1965; Trilles, Reference Trilles1969, Reference Trilles1994; Stephenson, Reference Stephenson1976; Weinstein & Heck, Reference Weinstein and Heck1977; Kensley, Reference Kensley1978; Raibaut & Trilles, Reference Raibaut and Trilles1993). For a long time, it has been relatively well known that descriptions made exclusively on juvenile or non-ovigerous females are not recommended as they lead to misidentifications.
The cymothoid fauna of the eastern Mediterranean were relatively poorly known and studies have started only recently in Greece (Papapanagiotou et al., Reference Papapanagiotou, Trilles and Photis1999; Papapanagiotou & Trilles, Reference Papapanagiotou and Trilles2001), Turkey (Horton & Okamura, Reference Horton and Okamura2001; Öktener & Trilles, Reference Öktener and Trilles2004; Trilles & Öktener, Reference Trilles and Öktener2004), Lebanon (Monod, Reference Monod and Gruvel1931; Bariche & Trilles, Reference Bariche and Trilles2005, Reference Bariche and Trilles2006; Trilles & Bariche, Reference Trilles and Bariche2006) and Israel (Horton et al., Reference Horton, Diamant and Galil2005).
Out of the eight species reported so far from Lebanon, two were introduced from the Indo-Pacific region. These were Anilocra pilchardi Bariche & Trilles, Reference Bariche and Trilles2006 and Cymothoa indica Schioedte & Meinert, 1884 (Bariche & Trilles, Reference Bariche and Trilles2006; Trilles & Bariche, Reference Trilles and Bariche2006). The eastern Mediterranean has been invaded by exotic species from the Red Sea via the Suez Canal for more than a century in a process generally known as lessepsian migration (Por, Reference Por1978).
Carrying out a large survey on Lebanese cymothoid fauna, we have collected several specimens of Ceratothoa collaris, first identified by Schioedte & Meinert (Reference Schioedte and Meinert1883) from Algeria. This species was previously known from the north-western Atlantic (Senegal to Morocco) and Mediterranean (Morocco to Tunisia) coasts of Africa (Trilles, Reference Trilles1994; Horton, Reference Horton2000). Three morphological forms (forma typica, africana, and globuligera) were distinguished by Monod (Reference Monod1924a, Reference Monodb). However, a meticulous and accurate description of the species was lacking, notably concerning the general features of the female and male, and different appendages and mouth parts.
The present paper reports for the first time the presence of Ceratothoa collaris in the easternmost Mediterranean Sea and redescribes the female and male stages, based on the holotype and other materials collected from north-western African coasts and newly collected specimens from Lebanon. It provides also an updated synonymy, geographical distribution and host specificity of the species.
MATERIALS AND METHODS
Material studied was collected from fresh fish landed along the coast of Lebanon from 2003 to 2005 and was deposited at the Natural History Museum of the American University of Beirut (AUBM). It was compared with additional material including the holotype and numerous other specimens from the Atlantic and Mediterranean coasts of Africa, collected by Monod or Dollfus (Trilles, Reference Trilles1972b; Dollfus & Trilles, Reference Dollfus and Trilles1976), and preserved in the Muséum National d'Histoire Naturelle (MNHN), Paris. Drawings were made using a camera lucida attachment and all measurements were made in millimetres. Fish names were updated according to Froese & Pauly (Reference Froese and Pauly2006).
SYSTEMATICS
Cymothoa oestroides Lucas, Reference Lucas1849: 78, pl. 8, figures 4a–c; Ceratothoa collaris Schioedte & Meinert, Reference Schioedte and Meinert1883: 366–368, table XVI (Cym. XXIII), figures 8–9; Carus, 1885: 433; Rokicki, Reference Rokicki1984: 1–220, figures 1–68; Rokicki, Reference Rokicki1985: 95–122; Trilles, Reference Trilles1986: 617–636; Trilles, Reference Trilles1994: 5–288; Horton, Reference Horton2000: 1041–1052; Bariche & Trilles, Reference Bariche and Trilles2005: 53–60; Meinertia collaris Monod, Reference Monod1924a: 31–34; Monod, Reference Monod1924b: 430–432; Monod, Reference Monod1925: 103–104; Trilles, Reference Trilles1972b: 1231–1268, pl. I–II; Trilles & Raibaut, Reference Trilles and Raibaut1973: 273–281; Capapé & Pantoustier, Reference Capapé and Pantoustier1976: 203; Dollfus & Trilles, Reference Dollfus and Trilles1976: 821–830; Trilles, Reference Trilles1977: 10; Trilles, Reference Trilles1979: 513–526, pl. I–IV; Avdeev, Reference Avdeev1979: 48–54.
Fig. 1. Ceratothoa collaris Schioedte & Meinert, Reference Schioedte and Meinert1883, adult female, dorsal view: (A) ovigerous female, 38 mm, typica form (Holotype, MNHN-Is 40); (B) non-ovigerous female, 30 mm, typica form (AUBM Cr-227); (C) ovigerous female, 32 mm, globuligera form (AUBM Cr-417); and (D) ovigerous female, 35 mm, africana form (MNHN-45). Scale bars: A, 10 mm; B–D, 7 mm.
Fig. 2. Ceratothoa collaris Schioedte & Meinert, Reference Schioedte and Meinert1883, adult female: (A) cephalon, ventral view; (B) antennule; (C) antenna; (D) maxilliped, non-ovigerous female; (E) maxilliped article 3 apex, non-ovigerous female; (F) maxilliped, ovigerous female; (G) maxilliped article 3 apex, ovigerous female; (H) maxillule; (I) maxilla; (J) maxilla apex; and (K) mandible. Scale bars: A, 5 mm; B, C, F, 1 mm; D, E, I, 0.6 mm; J, 0.4 mm; G, H, K, 0.2 mm.
Fig. 3. Ceratothoa collaris Schioedte & Meinert, Reference Schioedte and Meinert1883, adult female: (A) pereopod 1; (B) pereopod 7; (C–G): pleopods 1–5, ventral view; and (H) uropods. Scale bars: A–G, 2 mm; H, 3 mm.
Fig. 4. Ceratothoa collaris Schioedte & Meinert, Reference Schioedte and Meinert1883, adult male: (A) adult male, 15 mm (AUBM Cr-227), dorsal view; (B) antennule; (C) antenna; (D) maxilliped; (E) maxillule; (F) maxilla; (G) mandible; (H) pereopod 1; (I) pereopod 7. Scale bars: A, 2.5 mm; B, C, 0.4 mm; D, E, G, 0.2 mm; F, 0.35 mm; H, I, 1 mm.
Fig. 5. Ceratothoa collaris Schioedte & Meinert, Reference Schioedte and Meinert1883, adult male: (A–E) pleopods 1–5, ventral view except pleopod 2, dorsal view. Scale bars: A–E, 1 mm.
MATERIAL
Female (ovigerous 38 mm), Algeria, Lucas Reference Lucas1849 (Schioedte & Meinert, Reference Schioedte and Meinert1883; Trilles, Reference Trilles1972b), host unknown (holotype, MNHN-Is 40); female (ovigerous 40 mm), Algiers, Algeria, Lucas Reference Lucas1849 (misidentified as Cymothoa oestroides), host unknown (MNHN-Is 41); female (ovigerous 30 mm) and male (15 mm), Antelias, Lebanon, 12 July 2003, on Pagrus sp. (AUBM-Cr 227); male (9.5 mm), Antelias, 18 February 2005, on Pagellus acarne (AUBM-Cr 712); male (15 mm), Maameltein, 2 January 2005, on Pagellus erythrinus (AUBM-Cr 510); female (ovigerous 30 mm), Tripoli, 27 February 2005, on Epinephelus aeneus (AUBM-Cr 984); female (ovigerous 26 mm), Antelias, 18 January 2005, on P. erythrinus (AUBM-Cr 623); female (non-ovigerous 33 mm), Maameltein, 1 January 2005, on P. erythrinus (AUBM-Cr 506); female (ovigerous 32 mm), Antelias, 30 January 2005, on P. erythrinus (AUBM-Cr 743); female (ovigerous 27 mm), Maameltein, 3 January 2005, on P. erythrinus (AUBM-Cr 534); female (non-ovigerous 30 mm), Antelias, 6 September 2004, on P. erythrinus (AUBM-Cr 466); female (ovigerous 32 mm), Antelias, 19 September 2004, on P. erythrinus (AUBM-Cr 491); female (ovigerous 33 mm), Antelias, 3 May 2004, on P. erythrinus (AUBM-Cr 400); female (ovigerous 32 mm), Antelias, 15 May 2004, on P. erythrinus (AUBM-CR 0417); female (ovigerous 30 mm), Maameltein, 24 April 2004, on P. erythrinus (AUBM-CR 0408); male (14 mm), Antelias, April 2004, host unknown (AUBM-CR 0399); male (15 mm), Antelias, 24 April 2004, on P. erythrinus (AUBM-Cr 396); female (ovigerous 30 mm), Antelias, 18 June 2004, on Pagrus caeruleostictus (AUBM-Cr 441); female (ovigerous 25 mm), Antelias, 25 April 2004, on Pagellus erythrinus (AUBM-Cr 401); female (ovigerous 28 mm), Antelias, on Dicentrarchus labrax (AUBM-Cr 263); female (ovigerous 30 mm), Bouar, Kesserwan, 18 April 2004, on Dentex macrophtalmus (AUBM-Cr 356); male (14 mm), Bouar, Kesserwan, 18 April 2004, on D. macrophtalmus (AUBM-Cr 357); female (ovigerous 33 mm), Bouar, Kesserwan, 2 April 2004, on D. macrophtalmus (AUBM-Cr 364); females (2 ovigerous 37 and 31 mm; 1 non-ovigerous 28 mm) and male (16 mm), Antelias, 19 April 2004, on D. macrophtalmus (AUBM-Cr 372).
One hundred and twelve specimens (81 females and 31 males) held in the MNHN and collected along the coasts of Africa. Detailed lists are recorded in Trilles (Reference Trilles1972b) and Dollfus & Trilles (Reference Dollfus and Trilles1976).
DESCRIPTION OF FEMALE (FIGURES 1A–D, 2A–K & 3A–H)
The general morphology of non-ovigerous females is rather different from the ovigerous ones.
The ovigerous female is stout, with dorsum moderately vaulted, about two times as long as wide, widest at pereonites 4–5 or 5–6, ratio width pereonite 1/width pereonite 6 = 1/1.4; non-ovigerous female is more slender, with a pereon vaguely triangular in shape, widest at pereonite 6, ratio width pereonite 1/width pereonite = 1/1.7.
Cephalon 1.25–1.5 as wide as long, nearly triangular, anterior margin acute in dorsal view, moderately immersed in pereonite 1; eyes distinct but often partly hidden by antennae.
Pereonite 1 moderately produced on antero-lateral sides; antero-lateral angles extended to posterior margins of eyes, auriform with internal surface partly conspicuous, or with a globular protuberance, or narrow and moderately acute (respectively forma typica, globuligera and africana according to Monod (Reference Monod1924a, Reference Monodb)). Pereonite 1 longest; pereonites 2–4 slightly shorter according to the condition of the female (ovigerous or non-ovigerous) and nearly equal in length; pereonites 5–7 distinctly shorter, progressively more rounded and concave posteriorly. Coxal plates of pereonites 3–7 visible in dorsal view.
All pleonites visible, becoming wider towards posterior side, sub-equal in length; pleonites 1–2 distinctly less wide than others; pleonite 1 the least wide; pleonite 5 wider than preceding pleonites with a sinuate distal margin. Width of pleotelson slightly variable; pleotelson more or less wide than pereon, distinctly wider than long (average 2.05–2.6 as wide as long; mean 2.35), widest at base, distal margin always bisinuate but with irregular features.
Antennule slightly stouter and shorter to antenna; both with seven articles, extending generally to or beyond posterior margin of eyes; first four articles of antennule and antenna wider than others. Mandible palp without setae or spines, third article distinctly smaller than others; maxillule with three terminal spines; maxilla lateral lobe with 23 spines and medial lobe with 8–10 spines and very small setae; maxilliped of ovigerous female with oostegial lobe bordered with plumose setae and a palp with eight apical recurved spines on article 3; ten apical recurved spines on article 3 of non-ovigerous female.
Pereopods gradually increasing in size, all without spines or setae; 1–6 almost similar to each other; pereopod 7 distinct with a carina very expanded on basis and a distinctive lobe produced on merus. Pleopods simple, not distinctly visible in dorsal view; peduncles without retinacula; endopods often crumpled in alcohol but without accessory folds. Uropods often varying in shape, usually more or less extended along the pleotelson, rarely beyond; rami unequal in length, apices acute, exopod usually shorter than endopod.
DESCRIPTION OF MALE (FIGURES 4A–I & 5A–E)
Body oval, stocky, 2.4 times as long as wide, bilaterally symmetrical; dorsum vaulted nearly as in female. Cephalon triangular, slightly immersed in pereonite 1, anterior margin smoothly acuminated in dorsal view. Eyes distinct and more visible than female particularly because not hidden by antennae.
Pereon widest at pereonite 5; as in female, pereonite 1 longer than any others; 2–5 sub-equal and 6–7 decreasing in length. Coxae conspicuous in dorsal view.
Pleonites 2–5 sub-equal in length and width; pleonite 1 partly concealed by pereonite 7, narrower than any others. Pleotelson wider than long (average 2.2 times as wide as long), widest at base and posterior margin broadly rounded.
Antennule extending to middle of eye, composed of seven articles, slightly stouter than antenna, article 1 widest and distal margin with an isolated seta, others decreasing in width progressively; antenna extending to posterior margin of cephalon, comprising seven articles decreasing in width progressively, article 4 with sometimes a plumose seta on the postero-distal margin. Last article of mandible palp with four serrate setae on distal margin; maxillule with four terminal spines; maxilla lateral lobe with nine recurved spines and medial lobe with six; maxilliped with four apical recurved spines on article 3.
Pereopods gradually increasing in length, all without spines; pereopod 7 slightly distinct with a carina on basis and a lobe on merus but less expanded than in female. Pleopods rather similar to female except pleopod 2 with appendix masculinum well developed on endopod and pleopods 3–4 with few retinaculae on peduncle. Uropods extending beyond posterior margin of pleotelson; rami usually sub-equal, apices acute.
COLOUR
Female and male, alive or in alcohol, present a pale tan with few sparse chromatophores.
SIZES
Ovigerous females: 20–40 mm; non-ovigerous females: 18–40 mm; males: 9.5–16 mm.
SITE OF INFECTION
Females are usually in the buccal cavity; males are more erratic and can be found in mouth, branchial chamber and rarely on body.
TYPE LOCALITY
Algeria (Schioedte & Meinert, Reference Schioedte and Meinert1883).
TYPE HOST
Not specified on the label enclosed with the holotype. Lucas (Reference Lucas1849) reported that this species live on various fish.
HOSTS
Lebanese specimens were collected mainly on Pagellus erythrinus, less frequently on other Sparidae such as Dentex macrophthalmus, Pagellus acarne, P. caeruleostictus, Pagrus sp., and rarely on Dicentrarchus labrax (Moronidae) and Epinephelus aeneus (Serranidae). Previous records are from Africa (Trilles, Reference Trilles1994; Horton, Reference Horton2000) and were reported on Sparidae: Dentex dentex, D. maroccanus (Trilles & Raibaut, Reference Trilles and Raibaut1973), D. gibbosus (syn. D. filosus; Monod, Reference Monod1924a, Reference Monodb, Reference Monod1925; Trilles, Reference Trilles1972b; Trilles & Raibaut, Reference Trilles and Raibaut1973), D. macrophthalmus (Rokicki, Reference Rokicki1984); Pagellus acarne (Trilles, Reference Trilles1972b; Dollfus & Trilles, Reference Dollfus and Trilles1976), P. bogaraveo (Dollfus & Trilles, Reference Dollfus and Trilles1976), P. erythrinus (Monod, Reference Monod1924a, Reference Monodb, Reference Monod1925; Dollfus & Trilles, Reference Dollfus and Trilles1976), Diplodus sargus (syn. Sargus sargus; Dollfus & Trilles, Reference Dollfus and Trilles1976); Centracanthidae: Spicara sp., Smaris sp. (Trilles & Raibaut, Reference Trilles and Raibaut1973) and Spicara smaris (syn. Smaris vulgaris; Trilles, Reference Trilles1979); Sciaenidae: Corvina cameronensis (Trilles, Reference Trilles1977); and two Elasmobranchs: Raja miraletus (Rajidae) (Trilles & Raibaut, Reference Trilles and Raibaut1973) and Torpedo marmorata (Torpedinidae) (Capapé & Pantoustier, Reference Capapé and Pantoustier1976).
REMARKS
Cymothoa collaris was first collected by Lucas in the Mediterranean (Algeria, Alger) but misidentified as C. oestroides (Lucas, Reference Lucas1849). Schioedte & Meinert (Reference Schioedte and Meinert1883) later briefly described this species from a single specimen (ovigerous female) collected by Lucas.
Three different forms, Meinertia collaris forma typica, M. collaris forma africana and M. collaris forma globuligera were originally distinguished by Monod (Reference Monod1924a, Reference Monodb) according to some morphological differences of the cephalon and antennae but without any other descriptions of the species' main features. In this study, we have observed no distinctive morphological variations between the specimens collected off Lebanon and those found in Africa. Indeed, similar variations of the first pereonite (typica, africana, and globuligera forms according to Monod, Reference Monod1924a, Reference Monodb) are seen in both African and Lebanese samples. In the same way, variations in the body shape connected to the sexual and reproductive stages, or in the width and shape of the pleotelson and uropods, were common throughout the geographical range (Africa and Lebanon) of the species. Similar variations can be seen in other species such as Ceratothoa steindachneri (Horton, Reference Horton2000). It is clear that such variations are common in a wide range of cymothoids and can be found on cephalon but also elsewhere.
Lucas (Reference Lucas1849) considered Cymothoa collaris as a ubiquitous cymothoid, characterized by an euryxenic specificity and thus able to infect several species of fish. However, it appears that this species has a clear preference for Sparidae, more particularly P. erythrinus, which was the most common parasitized fish in Lebanon and Africa.
DISTRIBUTION
Eastern Atlantic: Arguin Bank, Port Etienne, Mauritania; Joal, Senegal (Monod, Reference Monod1924a, Reference Monodb, Reference Monod1925; Trilles, Reference Trilles1972b, Reference Trilles1977, Reference Trilles1979; Rokicki, Reference Rokicki1984). Mediterranean: Algiers, Castiglione (now Bou-Ismail), Oran, Algeria (Lucas, Reference Lucas1849; Schioedte & Meinert, Reference Schioedte and Meinert1883; Carus, Reference Carus1885; Monod, Reference Monod1924a, Reference Monodb; Trilles, Reference Trilles1972b, Reference Trilles1979; Dollfus & Trilles, Reference Dollfus and Trilles1976); Gulf of Tunis, Kelibia, Tabarka, La Galite, Tunisia (Trilles & Raibaut, Reference Trilles and Raibaut1973; Capapé & Pantoustier, Reference Capapé and Pantoustier1976); Agadir (Baie de Ouaouzeguedelt), Casablanca, Safi, Morocco (Monod, Reference Monod1924a, Reference Monodb, Reference Monod1925; Trilles, Reference Trilles1972b; Dollfus & Trilles, Reference Dollfus and Trilles1976). The geographical range of the species is now extended to the Levantine basin as numerous specimens were collected from Beirut, Kesserwan, and Tripoli along the Lebanese coast.
To date, this species has been commonly reported from the North Atlantic coast of Africa and seemed uncommon in the Mediterranean. Monod (Reference Monod1924a) wrote: ‘La découverte, en grande abondance, de cette espèce sur la côte occidentale d'Afrique, prouve que c'est là son habitat normal et que sa présence en Méditerranée est exceptionnelle’ [The high number of specimens from this species along the western coasts of Africa, attest that this is its normal habitat and its presence in the Mediterranean is exceptional]. Moreover, this species was never collected from north-western Mediterranean countries despite recent studies (e.g. Montalenti, Reference Montalenti1948; Trilles, Reference Trilles1972a, Reference Trilles1994; Trilles et al., Reference Trilles, Radujkovic and Romestand1989; Rodriguez-Sánchez et al., Reference Rodriguez-Sánchez, Serna and Junoy2001; Junoy & Castelló, Reference Junoy and Castelló2003). Although the species normal distribution might have included the entire southern coast of the Mediterranean Sea and the Levant, no specimens were ever collected from Libya, Egypt or Israel. This might be explained by less scientific attention in the area but also by a recent range expansion of the species, since many tropical Atlantic organisms have contributed many new elements to the Mediterranean biota (Galil et al., Reference Galil, Froglia, Noël and Briand2002; Golani et al., Reference Golani, Orsi-Relini, Massutí, Quignard and Briand2002; Zenetos et al., Reference Zenetos, Gofas, Russo, Templado and Briand2003).
ACKNOWLEDGEMENTS
We are grateful to the University Research Board (URB) of the American University of Beirut for funding this research (DDF 111030/588112), to Dr Gérard Lefranc (University of Montpellier 2, France) for transporting Lebanese material between our two laboratories, to Dr Danielle Defaye (National Museum of Natural History, Paris, France) for providing type and additional specimens. Thanks also to Mr Joseph Chahwan and the Lebanese fishermen for their help in collecting samples.
