Parasitofauna Isolated from Fish Off the East Algerian Coast

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Parasitofauna isolated from ﬁsh off the east Algerian coast

Article in Bulletin- European Association of Fish Pathologists · January 2017

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ȱȱȱęȱ ěȱȱȱȱ

ǯȱ ęȬ1*, Z. Ramdane1, N. Kadri2,3, ǯȱ ę4, J-P. Trilles5 and R. AmaraŜ

1Laboratoire de Zoologie Appliquée et d’Ecophysiologie Animale, Faculté des Sciences de la Nature et de la Vie, Université de Bejaia, 06000 Bejaia, Algérie ; 2Laboratoire de Biochimie, Biophysique, Biomathématiques et Scientométrie (L3BS), Faculté des Sciences de la Nature et de la Vie, Université de Bejaia, 06000 Bejaia, Algérie ; 3Département de Biologie, Faculté des Sciences de la Nature et de la Vie et Sciences de la Terre, Université de Bouira, 10000 Bouira, Algérie ; 4Direction Générale des Forêts, Chemin Doudou Mokhtar, B.p. 232, Ben Aknoun, Alger, Algérie ; 5Équipe Adaptation Eco Physiologique et Ontogenèse, Université de Montpellier, CC. 092, Place E. Bataillon, 34095 Montpellier cedex 05, France ; 6·ȱĴȱȱȂǰȱ·ȱǰȱǰȱȱ 8187, LOG, Laboratoire d’Océanologie et de Géosciences, F62930 Wimereux, France

Abstract ȱ ¢ȱŘŖŗŗȱȱ ¢ȱŘŖŗřǰȱȱȱŗŜŚřȱǰȱȱȱȱ ȱ ȱǻƽŗśŚśǼȱȱȱǻƽşŞǼȱ ȱǯȱȱŗŚȱęȱǰȱŗŝȱȱȱ ȱ ǰȱȱ ȱȱȱȱȱ ȱȱǯȱȱȱ ȱȱ rate, some isolated parasite species induce serious necrosis, alterations and atrophies to the muscle, ȱ¢ȱȱȱȱȱȱ¢ȱPyroderma cylindricum (P=9.37%; I=1); Lerneolophus sultanus (P=9.09%; I=1), and Ceratothoa oestroidesȱǻƽŖǯŜŘƖǲȱ ƽŗǼǰȱ¢ǯȱȱȱěȱ ȱ ȱȱȱęȱȱ¢ȱNaeobranchia sygniformis (P=27.27%; I=1). Among the most abundant isolated parasites was the nematode, Anguillicola crassusȱǻƽŚŘǯśřƖǲȱ ƽŜǯŗŗǼȱȱȱ European eel, Anguilla anguillaǰȱ ȱȱȱȱĚ¢ȱȱȱȱ Ȭǯȱ ȱȱ¢ȱȱȱ ȱȱȱęȱǯ

Introduction ǰȱŘŖŖŞǰȱŘŖŗŖǰȱŘŖŗŘǲȱȱȱǯǰ 2007, ȱȱȱȱȱȱ¢ȱ 2009, 2013; Ider et al., 2014; Ichalal et al., 2015). ecosystem (Zander et al., 2002), greatly contrib- ĴȱĴȱȱȱȱȱȱȱ uting to overall aquatic biodiversity. endangered species such as the European eel, Anguilla anguilla ǻǯǰȱŗŝśŞǼȱǻAnguilla; Anguil- ȱȱȱȱȱęȱ Ǽǯȱȱ¡ȱȱȱ¢ȱȱȱ ȱȱȱ¡¢ȱǻȱȱ ȱ¡ȱȱ ȱǻȬ Ǽȱǻȱȱǯǰȱ

* Corresponding author’s email: [email protected] Bull. Eur. Ass. Fish Pathol., 37(4) 2017, 149

ŘŖŖşǼȱ ȱȱȱȱȱMyxi- ȱǻǼȱǻřǰȱƽŗŚşȱǼȱȱȱȱ dium giardi ǻ·¸ǰȱŗşŖŜǼȱǻMyxidiumǲȱ¢¡- ȱŗŜŚřȱęȱȱȱǻȱŘŖŗŗȱȱ diidae),ȱȱȱȱ¢ȱȱǻǼȱ ŘŖŗřǼǯȱȱęȱ ȱȱȱȱ (Boudjadi et al., ŘŖŖşǼȱȱȱȱ ǰȱ ȱ ȱęȱȱȱ ȱȱȱ ȱ by Anguillicola crassus (Kuwahara, Niimi and ¢ȱȱȱȱęȱ Hagaki, 1974) (Anguillicola; Dracunculidae). ȱȱȱęȱȱȱǯȱȱęȱ ȱȱȱ ȱȱȱȱ ȱȱȱȱ¢ȱ ȱȱȱęȱ ęȱęȱǯȱȱ ȱȱȱ ȱ¡ȱȱȱȱȱȱȱ a transparent, labelled plastic bag (date, study ęǰȱȱȱ ȱȱȱȱ area, etc.) and transported immediately (in less environments, and try to assess their potential ȱŚȱȱȬęǼȱȱȱ¢ȱȱȱǯȱ ȱěȱȱȱǯ ȱȱ ȱęȱȱȱȱ the nearest 1 mm using an ichtyometer, and Material and Methods total weight (Wt) was determined to the nearest ȱ¢ȱ ȱȱȱȱěȱ- Ŗǯŗȱȱȱȱȱǯȱȱ¡ȱ ȱ ȱȱȱȱȱȱȱǻȱŗǼǲȱ ȱ¢ȱȱȱȱ £ěȱęȱȱǻŗǰȱƽȱşŞȱǼǰȱ ȱ ǯȱȱ¢ǰȱęǰȱȱ¢ǰȱȱ ȱȱǻŘǰȱƽŗřşŜȱǼȱȱȱ ǰȱȱȱ Ȭȱ ȱ¡-

Figure 1. Study area and sampling stations, 1:ȱ£ěȱęȱǲȱ2:ȱ ȱȱǲȱ3: Soummam River. 150, Bull. Eur. Ass. Fish Pathol., 37(4) 2017

ȱȱȱȱȱȱȱȱ- Caligus ligusticus ǻǰȱŗşŖŜǼȱǻCaligus; Caligi- secting stereomicroscope. Collected parasites dae); Gotocotyla acanthus (Parona et Perugia, ȱę¡ȱȱŝŖƖȱȱȱȱęǯȱ ŗŞşŜǼ (Gotocotyla; Gotocotylidae). The European Parasitological parameters (Prevalence (P %) eel, Anguilla anguillaȱȱȱȱȱ ƽȱȱȱȱȱȦȱȱȱȱ ȱ ȱȱȱȱȱ£ȱIchtyoph- ¡ȱȱƼȱŗŖŖǲȱȱ ¢ȱǻ Ǽȱƽȱȱ ȱęȱǻǰȱŗŞŝŜǼȱǻIchtyophtirius; ȱȱȱȱȱȦȱȱȱ Hymenostomatida). One nematode Anguil- ȱȱǲȱȱȱȱǻǼȱ licola crassusȱȱȱȱȱ ƽȱȱȱȱȱȱȱȦȱȱ ȱȱȱȱęȱȱȱȱ ȱȱ ȱȱ¡ȱǼȱ ȱȱ Bejaia, although have been already reported ȱȱȱȱǯȱǻŗşşŝǼǰȱȱȱȱ ȱȱȱǱȱMicro- which are summarised in Table 1. cotyle mugilisȱǻǰȱŗŞŝŞǼȱǻMicrocotyle; Micro- ¢Ǽȱȱȱȱǻȱ ęȱȱ ȱȱȱȱěȱȱȱ ǯǰȱŗşşŞǼǰȱPagellicotyle mormyriȱǻ£ǰȱŗŞŝŞǼȱ ȱȱǰȱ¢ȱȱȱȱȱA. crassus (Pagellicotyleǲȱ¢Ǽȱȱ ȱȱ¢ǰȱ and Peroderma cylindricum ǻ ǰȱŗŞŜśǼȱǻPero- ȱǻǰȱŗşŜřǼȱȱȱǻǰŗşşśǼǰȱ derma; Pennellidae), a histological study was Atriaster heterodus ǻȱȱǰȱŗşŜşǼȱ ǯȱ ȱȱǻ Ȭȱȱ (Atriasterǲȱ¢Ǽȱȱ (Lebedev Ǽȱ ȱę¡ȱȱŗŖƖȱěȱ- ȱǰȱŗşŜşǼȱȱȱǻ£ȱȱ aldehyde solution, dehydrated in increasing Maillard, 1973), Polylabris tubicirrus (Paperna ethanol concentrations (70 to 95%), cleared in ȱ ǰȱŗşŜŚǼȱǻPolylabris; Microcotylidae) in ¡¢ȱȱĜȬǯȱ ȱ- ȱǻȱȱ ǰȱŗşŜŚǼǰȱȱǻ£ȱ ȱȱřΐȱȱǻȱȱȱ and Maillard,1973), Spain (Lopez-Roman, 1973) ȱȱȱǼȱ ȱȱ ȱȱȱȱȱǻ- using Leica RM2125 RTS rotary microtome. ȱȱ£ǰȱŗşŞşǼǰȱG. acanthus in Tunisia Sections were mounted on glass microscope ǻǰȱŗşşśǼȱȱA. crassus in Egypt (Koops ǰȱȱ ȱ¢Ȃȱ¡¢Ȭǰȱ ȱ ǰȱŗşŞşǼǰȱȱǻȱ ȱȱǯǰȱ ȱ ȱȱȱȱ¡ȱ ŗşşŜǼȱȱȱǻȱȱǯǰȱŗşşşǼǯȱ- by Leica DM1000 LED microscope. ȱȱȱ ȱȱȱ£ȱȱ ȱȱȱȱȱěȱȱȱ Results and Discussion the Mediterranean Sea. Diversity and infection rates of isolated parasites ȱȱȱ ȱęȱ Ceratothoa ȱęȱȱȱȱȱȱ oestroidesȱǻǰȱŗŞŘŜǼȱǻCeratothoa; Cymothoi- ęǯȱȱȱȱ ȱȱ dae) in the European pilchard Sardina pilchardus ęȱȱȱȱȱęǰȱ- (Walbaum, 1792) (Sardina; Clupeidae) and Nero- ȱŗŜȱ£ȱȱŗȱ£ȱ¡ǯȱ cila maculata ǻȱ ǰȱŗŞŚŖǼȱǻNerocila; Among the collected parasite species, three are Cymothoidae) in the tub gurnard Trigla lucerna new geographical records; Clavellisa emargi- ǻǯǰȱŗŝśŞǼȱǻTrigla; Triglidae).ȱȱ ȱęȱ nataȱǻ ¢ǰȱŗŞřŝǼ (Clavellisa; Lerneopodidae); ȱȱȱȱȱȱȱ Bull. Eur. Ass. Fish Pathol., 37(4) 2017, 151

Table 1.ȱȱȱȱȱȱȱ¡ǯ

Lm Parasites Parasites Host Sites N (Min - Fs P% Am I groups species Max) 17.31 Sparus aurata 1 Şř (4.20 - // /000 ǻǯǰȱŗŝśŞǼ 31.50) Lernaeolophus sultanus Pr 9.09 0.09 1 ǻ ǰȱŗŞŜśǼ 27.75 Sparus aurata 211 (20.90 - Crustacea Naobranchia ǻǯǰȱŗŝśŞǼ 33.50) cygniformis Br 27.27 0.27 1 ǻ ǰȱŗŞŜřǼ Gnathia sp. Br, Bc 45.45 ŗŝǯŞŗ 39.2 Dicentrarchus ŗşǯŜś labrax 115 / / / 0 0 0 (7 - 32.10) ǻǯǰȱŗŝśŞǼ Lernanthropus kroyeri Br 33.33 0.33 1 Dicentrarchus řŘǯŘŜȱ (van Beneden, labrax 211 (30.30 - Crustacea ŗŞśŗǼ ǻǯǰȱŗŝśŞǼ 34) Caligus minimus ǻĴǰȱŗŞŘŗǼ Br 33.33 0.33 1

Caligus ligus- Sarpa salpa ȱŘŜǯř 230 Crustacea ticus Bc 3.33 0.033 1 ǻǯǰȱŗŝśŞǼ ǻŗŞȱȮȱřŘǼ ǻǰȱŗşŖŜǼȱȘȘ Peroderma cylin- ŗřǯŘŜ dricum Mus 9.37 0.09 1 Sardina pilchar- ǻ ǰȱŗŞŜśǼ dus 2 ŗŜŖ Crustacea (Walbaum, 1792) Ceratothoa oes- (10 - 20) troides Bc ŖǯŜŘ ŖǯŖŖŜ 1 ǻǰȱŗŞŘŜǼȱȘ Nerocila mac- Trigla lucerna 19.75 ulata 210 Crustacea ȱ 10 0.1 1 ǻǯǰȱŗŝśŞǼ ǻŗŜȱȮȱŘśǼȱ (Milne Ed- ǰȱŗŞŚŖǼȘ Lithognathus Pagellicotyle ŗŜǯŜŗ mormyrus 2 330 Monogenea mormyri Br 3.33 0.03 1 (14 – 22) ǻǯǰȱŗŝśŞǼ ǻ£ǰȱŗŞŝŞǼ Atriaster hetero- ŗŞǯşśȱ Boops boops dus 2 ŜŜŚ (10 - Monogenea Br ŜǯŖŘ 0.14 2.37 ǻǯǰȱŗŝśŞǼ (Lebedev et 27.50) ǰȱŗşŜşǼ 152, Bull. Eur. Ass. Fish Pathol., 37(4) 2017

Table 1 Continuedǯȱȱȱȱȱȱȱ¡ǯ

Lm Parasites Parasites Host Sites N (Min - Fs P% Am I groups species Max) Atriaster heterodus Br ŗśǯŜŘ ŖǯŗŜ 1 (Lebedev et Diplodus vulgaris ŗŞ ǰȱŗşŜşǼ ǻ ě¢ȱȬ 2 ŜŚ Monogenea (14 – 29) ǰȱŗŞŗŝǼ Polylabris tubicirrus Br ŚǯŜş ŖǯŖŞ ŗǯŜŝ (Paperna et ǰȱŗşŜŚǼ Atriaster heterodus Br ŗŖǯŜŝ 0.11 1 (Lebedev et Diplodus cervinus ŘŜǯŜŝȱ ǰȱŗşŜşǼ 275 Monogenea ǻ ǰȱŗŞřŞǼ (10 - 55) Polylabris tubicirrus Br 4 0.07 ŗǯŜŝ (Paperna et ǰȱŗşŜŚǼ Gotocotyla acan- Diplodus annu- 12.44 thus laris 237 Monogenea Br ŗŜǯŘŘ 0.02 1.33 (10 - 17) (Parona et Peru- ǻǯǰȱŗŝśŞǼ ǰȱŗŞşŜǼȱȘȘ Gotocotyla acan- Lichia glauca ŘŞ thus 23 Monogenea Br 33.33 1.33 4 ǻǯǰȱŗŝśŞǼ ǻŘřȱȮȱřŜǼȱ (Parona et Peru- ǰȱŗŞşŜǼȱȘȘ Microcotyle Mugil cephalus 27.49 350 Monogenea mugilis Br 10 0.121.2 ǻǯǰȱŗŝśŞǼ (15 - 40) ǻǰȱŗŞŝŞǼ Anguillicola crassus Nematoda (Kuwahara, Sb 42.53 ŘǯŜ Ŝǯŗŗ řŜŗǯşş Anguilla anguilla Niimi and 3 Şŝ (197 - ǻǯǰȱŗŝśŞǼ Hagaki, 1974) ŞŘŘǼ Ichtyophtirius Protozoa ęȱ(Fou- 2.3 0.02 1 ǰȱŗŞŝŜǼ Alosa fallax alge- Clavellisa emar- 17.04 riensis (Regan, 312 Crustacea ginata (Kroyer, Br 25 0.25 1 (14 - 21) ŗşŖŜǼ ŗŞřŝǼȱȘȘ

ȘǱȱ ȱȱȱȱǲȱȘȘǱȱ ȱȱȱȱǲȱǱȱȱȱ¡ȱęǲȱǱȱȱ ǰȱȬ¡Ǳȱȱȱ¡ǲȱȱǻƖǼǱȱǲȱǱȱȱǲȱ Ǳȱȱ ¢ǲȱ Ǳȱ¡ȱǲȱǱȱȱ¢ǲȱǱȱȱǲȱǱȱȱǲȱǱȱȱęǲȱǱȱȱęǲȱǱȱ Ȭ bladder ; Mus: Muscle; 1Ǳȱ££ȱęȱǲȱ2Ǳȱ ȱȱǲȱ3: Soummam River. Bull. Eur. Ass. Fish Pathol., 37(4) 2017, 153

ǯȱȱ¡ȱȱȱ ȱȱȱȱȱ the mean intensity reached 45.45% and 39.2 ȱȱȱȱȱǰȱ ȱ ȱȱȱǰȱ¢ǯȱȱ ȱȱȱȱȱȱ- ȱǰȱȱȱ ȱ¢ȱ ǯȱ ȱǰȱ ȱS. aurata and D. labrax ȱȱȱ¡ȱřřǯřřƖȱǻLernanthropus ȱȱ¢ȱȱȱȱȱ kroyeri, Caligus minimus and G. acanthus), with as Lernaeolophus sultanusȱǻ ǰȱŗŞŜśǼȱǻLernae- ȱ¡ȱȱȱȱA. crassus in the olophus; Pennellidae), Naobranchia cygniformis ȬȱȱA. anguillaȱǻƽŚŘǯśřƖǲȱ ƽŜǯŗŗȱ ǻ ǰȱŗŞŜřǼȱǻNaobranchia; Lernaeopodidae), ȱȱȱǼȱȱȱǰȱ Gnathia sp., Lernanthropus kroyeri (van Beneden, £ȱȱGnathiaȱǯȱȱȱȱȱȱ ŗŞśŗǼȱǻLernanthropus; Lernanthropidae), Caligus ¢ȱȱȱ ȱȱȱǰȱSparus minimusȱǻĴǰȱŗŞŘŗǼȱǻCaligus; Caligidae). aurata ǻǯǰȱŗŝśŞǼȱǻSparus; Sparidae) (P=45.45%; ƽřşǯŘȱȱȱȱǼǯȱ- ȱěȱȱȱ ȱȱȱȱȱȱȱ ȱȱȱȱęȱȱ ȱǯȱȬȱęȱȱ ¡ȱ ȱȬęǲȱȱȱȱ ȱĚȱȱȱ£ěǰȱS. aurata and organs were the gills and the oral cavity (Table the European sea bass, Dicentrarchus labrax ŗǼǰȱ ȱȱȱȱȱȱ ǻǯǰȱŗŝśŞǼȱǻDicentrarchus; Moronidae) did not has not been assessed in this study. Parasites ȱȱȱȱȱ ȱ ȱ ȱȱ ȱȱȱȬę¢ǰȱ ȱȱȱȱ ȱǯȱ ȱ¡ǰȱ¡ȱȱ¢¡ȱǻȱ This might be related to one or a combination ŘǼǯȱ¡ȱ ȱȱȱę¢ȱȱȱ- ȱȱ ȱǱȱȱȱȱ ȱ- ȱ ȱȱȱěǰȱ ȱ ȱęȱǻȱȱȱȱǼǰȱ observed both at macroscopic and microscopic indeed, the cages were well spaced and placed ǯȱ ǰȱȱȱCeratothoa oestroides generally in suitable depths (40 m), with gen- ȱȱěȱȱȱȱȱȱ erally moderate currents; Ȧȱȱ¡ȱ ȱȱȱȱȱȱȱȱȱ ¢ȱȱ ȱȱȱęȱ¢ȱȱ ȱǻȱŘǰȱȱŘǼǯȱȱȱěȱ ȱ these cages did not promote the development previously described by Ramdane et al. (2009). ȱǯȱ ǰȱȱȱ ȱ¢ȱȱ Our results corroborate those reported by that ȱ¢ȱȱęȱȱǻ£ěȱǼȱ ȱȱLernaeolophus sultanus and Naobranchia could be easily altered over the coming years cygniformisȱȱȱ¡ȱȱȱȱ ¢ȱęȱ¡ǰȱȱȱȱęȱǰȱȱ ȱȱȱȱȱȱȱȱȱ ǰȱȱ¡¢ǰȱǯǰȱȱ arches (Table 2, Figure 2 B to C). an important issue without regular monitoring. ȱȱ ȱęȱȱĴȱ¢ȱȱ- ȱȱȱPeroderma cylindricum caused ability at aquaculture sites, enhanced interaction ȱȱǰȱȱȱ¢ȱĚȱ in that case might contribute to the development ¢ȱȱȱȱȱȱȱ ȱȱȱȱęǯ ȱȱȱȱȱǻȱ 2; Figure 2D; Figure 3 A to B). Zamouri-Langar ȱǰȱȱȱȱęȱ (1995) noticed that P. cylindricum weakened the 154, Bull. Eur. Ass. Fish Pathol., 37(4) 2017

Table 2.ȱę¢ȱȱȱěȱȱȱȱȱ¡ǯ

SpecięcityȦ Collected parasites species SpecięcityȦhost Impact of parasites on their hosts Fixing site Lernaeolophus sultanus ¢¡ ȱȱȱ Strict Naobranchia cygniformis ¡ ȱȱȱę

ȱȱȱęǰȱǰȱ Gnathia sp. ¢¡ Large buccal cavity

Lernanthropus kroyeri ¡ ȱȱȱę Clavellisa emarginata ¡ Unobserved Caligus minimus ȱȱȱȱ¢ Caligus ligusticus ¡ Unobserved Peroderma cylindricum Muscle and kidney deterioration Ceratothoa oestroides ȱȱȱ ¡ Nerocila maculata ȱȱȱȱȱȱę Strict ȱȱ Ȭȱȱ Anguillicola crassus ¢¡ Ě¢ȱ Microcotyle mugilis ¡ Pagellicotyle mormyri Atriaster heterodus Unobserved Polylabris tubicirrus ¡ Gotocotyla acanthus ¢ȱę ¢¡ Large Hemorrhage

parasitised European pilchard, making them lose and digestive tract, reveals potential pathogenic their swimming-balance. ȱ¡ǯȱȱȱȱȱ done on the protozoan parasites, especially ȱȱȱȱȱȱ ¢¡£ǰȱǰȱǯǰȱ ȱȱ¡ȱ Anguillicola crassus ȱȱȱȱȱ ȱȱěȱȱȱǯ swim-bladder (Table 2; Figure 4A) and caused ȱȱȱȱěȱ¢ǰȱ ȱȱ Acknowledgements ȱȱĚȱȱęȱǻȱŘǲȱ ȱ ¢ȱȱȱęȱȱȱȱ Figure 2E; Figure 4 A to B). Larvae, L3 and L4 ęȱȱȱȱȱ ȱȱ however, were located in the wall, resulting ǯȱȱȱȱȱȱȱȱ ȱȱȱȱȱǻȱŚȱȱȱǼǯȱ ¢ȱȱǻ¢ȱȱǼȱȱ Similar results were reported by Molnar et al. ȱȱȱȱ¢ȱ ȱȱ ǻŗşşřǼȱȱȱȱǯȱǻŘŖŖŘǼǯȱ ȱȱȱ¢ȱ ȱȱ- script; we believe that their positive comments ȱȱǰȱȱ¢ȱȱ substantially improved this article. Bull. Eur. Ass. Fish Pathol., 37(4) 2017, 155

Figure 2. A: Ceratothoa oestroides ȱȱȬȱǻǼȱȱȱȱȱȱȱ¢ȱ ǻǼȱȱȱȱBoops boops; B to C:ȱȱȱȱȱ¢ȱȱB. boopsȱȱ¢ȱȱȱ copepod, Lernaeolophus soltanus ¢ȱȱȬȱę¡ȱ¡ǲȱD: Pyroderma cylindricum penetrating into European pilchard Sardina pilchardus body; E:ȱȱ ȬȱȱȱȱAnguilla anguilla by parasitising Anguillicola crassus.

Figure 3. ȱȱȱȱȱȱȱȱSardina pilchardus; A: ȱȱ unparasitised European pilchard showing normal skin layers, (Ep) epidermis, (Ss) stratum spongiosum, (Sc) stratum compactum, (M) skeletal muscle; B:ȱȱȱPeroderma cylindricumȱȱȱȱȱȱǰȱ ȱȱȱȱȱǻȱ Ǽȱȱȱ¢ȱȱȱȱȱǱȱǻI) Intestine, (O) Ovary, (Cg) Cemental gland. ŗśŜǰȱǯȱǯȱǯȱȱǯǰȱřŝǻŚǼȱŘŖŗŝ

Figure 4. ȱȱȱ ȬȱȱȱȱȱAnguilla anguilla, A: Anguillicola crassus parasitising the swim-bladder lumen, (Cu) cuticle, (W) womb, (O) ovaries, (I) intestine; B:ȱ Ȭȱȱȱ ȱȱ ȱȱ¢ȱ¢ǱȱǻTE) tunica externa, (SM) submucosa, (M) muscularis mucosae, (E) epithelium, (Bv) blood vessel, (L) lumen; C:ȱ Ȭȱȱȱȱ ȱȱȱ¢ȱǻSM, M, EǼȱȱȱȱȱǻȱ ǼǲȱD:ȱȱȱAnguillicola crassus ȱǻǼȱȱȱ¢ǰȱ EǱȱȱȱAnguillicola crassus entrapped in the rete mirabile ȱȱ Ȭǯ Bull. Eur. Ass. Fish Pathol., 37(4) 2017, 157

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