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The Trematode Parasites of Lophius piscatorius (Angler Fish) from the Aegean Sea: Ege Denizi'nden Yakalanan Lophius piscatorius'larin (Fener Baligi) Trematod Parazitleri.

ABSTRACT

Objective: There is no study on the trematode parasites of Lophius piscatorius. The aim of this study is to address the lack of knowledge about the parasites of angler fish from the coasts of Turkish seas.

Methods: Frozen individuals of L. piscatorius from the coasts of Izmir were brought to Ataturk University, and their visceral organs were parasitologically investigated. Parasites were fixed with AFA (Acetic acid-Formaline-Alcohol) fixative and permanently mounted with Canada balsam.

Results: Two digenean species were recorded: Prosorhynchoides gracilescens (Bucephalidae), which is commonly found in L. piscatorius, and Aphallus tubarium (Cryptogonimidae), which is rarely harbored in L. piscatorius. Conclusion: Both species comprise the newly discovered parasite fauna of Turkey.

Keywords: Aegean Sea, Bucephalidae, Cryptogonimidae, Lophius piscatorius, Turkey

Received: 24.03.2016

Accepted: 08.12.2016

OZ

Amac: Turkiye'de daha once Lophius piscatorius'un trematod parazitleri arastirilmamistir. Bu calismanin amaci Turkiye kiyilarinda yasayan fener baliklarinin parazit faunasi hakkindaki bilgi eksikligini gidermektir.

Yontemler: Izmir kiyilarinda yakalanmis olan L.piscatorius'lar dondurulmus olarak Ataturk Universitesi'ne getirilmis ve baliklarin ic organlarindaki parazitler arastirilmistir. Tespit edilen parazitler AFA (Asetik asit-Formalin-Alkol) fiksatifiyle tespit edilip, Kanada balsamiyla kalici preparatlari yapilmistir.

Bulgular: Incelenen baliklardan iki digenea turu tespit edilmistir. Bunlar L. piscatorius'ta sikca rastlanan Prosorhynchoides gracilescens (Bucephalidae) ve L.piscatorius'ta nadiren rastlanan Aphallus tubarium (Cryptogonimidae)'dur. Sonuc: Her iki tur de Turkiye parazit faunasi icin yeni kayittir.

Anahtar Kelimeler: Ege Denizi, Bucephalidae, Cryptogonimidae, Lophius piscatorius, Turkiye

Gelis Tarihi: 24.03.2016

Kabul Tarihi: 08.12.2016

INTRODUCTION

Majority of the animals live free and the others live together. The association between animals can be divided into two groups: homogenetic and heterogenetic. The association between individuals of the same species is homogenetic, such as ants and bees, and between those of different species is heterogenetic. Parasitism is a lifestyle of heterogenetic association that is much more complex than that of homogenetic association (1).

In general, the parasitic way of the life is successful and found in nearly every phylum of animals from protists to arthropods and chordates as well as in many plant groups. Humans, for example, can be infected with more than hundred types of parasites. It is almost impossible to find animals not infected by even a single parasite on or within it. Organisms that are not parasites are usually hosts (2).

The marine fish fauna of Turkey consists of 512 species (3). Only 84 marine fish species of Turkey have been parasitologically studied and 161 metazoan parasites were found (4).

Angler fish, a common carnivorous and demersal fish of the Black Sea; Mediterranean Sea; coasts of Europe, Africa, and Northern America; Atlantic Ocean; Arctic Ocean; and Baltic Sea but not the the Pacific and Indian Oceans is one of the important species of the marine fish fauna of Turkey (5). Although there are many papers on parasites, mainly on Protozoa, Monogenea, and Crustacea, of the marine fishes from Turkey, only two studies by Oktener and Trilles (6) and Akmirza (7) mentioned regarding one crustacean and nematod species of L. piscatorius, respectively.

The aim of this paper is to contribute to the research on trematod parasite fauna of marine fishes of Turkey.

METHODS

A total nine L. piscatorius samples collected by the fishermen from the coasts of the Aegean Sea (Izmir) were brought to the Parasitology Research Laboratory of Ataturk University Science Faculty in April 2014. The alimentary organs, livers, and gallbladders of the fishes were taken out and put into petri dishes filled with 1% saline water after the dissection. The detected parasites were fixed with alcohol-formalin-acetic acid (AFA), dyed with Mayer's carmalum, and mounted with Canada balsam, according to the study by Pritchard and Kruse (8). Identification of the parasites was executed according to studies by Dawes (9), Dawes (10), Yamaguti (11), and Skrjabin (12). Author declared that the study was conducted according to the principles of the World Medical Association Declaration of Helsinki "Ethical Principles for Medical Research Involving Human Subjects" (amended in October 2013).

RESULTS

Family: Cryptogonimidae Ward, 1917

Aphallus tubarium (Rudolphi, 1819) Poche, 1926

Synonyms: Distoma tubarium (Rudolphi, 1819); Distoma fuscescens (Rudolphi, 1819); Distomum (Cryptogonimus) tubarium (Rudolphi, 1819 and Nicoll, 1915); Acanthochasmus inermis (Stossich, 1905); Acanthostomum inermis (Stossich, 1905 and Yamaguti, 1958); Aphallus fuscescens (Rudolphi, 1819 and Yamaguti, 1971).

The body is long and slightly wide at the ventral sucker level. The tegument is spinous. The oral sucker is a little larger than the ventral one. The pharynx is slightly rectangular, and the esophagus is longer than the prepharynx. The intestinal ceca extend to the posterior end of the body. The pretesticular ovary is three-lobed, and the uterus extends to the posterior end of the body. The eggs are small and nonfilamentous. The vitellin glands are globular and located between nearly the middle of the body and the posterior of the hind testis. The anterior testis is smaller than the posterior one (Figure 1) (Table 1).

Family: Bucephalidae

Prosorhynchoides gracilescens (Rudolphi, 1819)

Synonyms: Bucephaloides gracilescens (Rudolphi, 1819); Bucephalopsis gracilescens (Rudolphi, 1819); Prosorhynchus gracilescens (Rudolphi, 1819).

The shape of the body, broader anteriorly, is elongated and oval. The oral sucker is larger than the pharynx. The intestine is simple and sac-like. The genital pore is at the posterior end of the body. The testes are slightly globular, and the cirrus sac is long and located at posterior end of the body. The pretesticular ovary is spherical. The vitellin follicles are few in number, globular, slightly larger, and located at the anterior half of the body. The eggs are operculate, small, and ovoid (Figure 1) (Table 2).

DISCUSSION

The cosmopolitan family Cryptogonimidae Ward, 1917, includes a large number of species from marine and freshwater fishes to snakes and crocodiles (13). The metacercariae of Cryptogonimids encyst in the tissues of fishes The adults are found in the gut sometimes in the other organs of freshwater and marine fishes, occasionally in amphibians and reptiles (14).

A. tubarium was recorded previously in Dentex dentex; L. piscatorius; Sciaena umbra; Gobius ophiocephalus; Sparus pagrus; Syngnathus typhle; Trachurus trachurus; and Umbrina cirrhosa (13, 15-24).

In light of the literature, it is clear that A. tubarium can be found in various fish species of the Atlantic Ocean, Mediterranean Sea, Aegean Sea, and Black Sea, whereas it has not been found in the fish species of Turkish seas.

The tegument of A. tubarium is spinous, but the tegument of the parasite we mounted is not covered with spines because the fish material was frozen and spines are very easily lost in frozen and poorly fixed materials (14). The width of the samples and the measures of the suckers, pharynx, testis, and ovary are smaller and the prepharynx and esophagus are longer than the measures of the A. tubarium described by Bartoli and Bray (13) and Kornychuk and Gaevskaya (22). The variation of the measurements can be due to the host difference. A. tubarium has been recorded from Turkey for the first time.

Bucephalids especially found in the gut and intestine, occasionally in the body cavities and tissues of the teleost fishes, rarely found in amphibians (14, 25). Prosorhynchoides is a cosmopolitan parasite that lives in marine and some freshwater fishes (26). P. gracilescens (Rudolphi, 1819) is a common intestinal parasite of the angler fish L. piscatorius in European marine waters (27).

P. gracilescens was previously recorded in L. piscatorius; Sarda sp. S. sarda Scomber sp.; Gadus morhua and Merlangius merlangus euxinus and Belone belone (9 , 10, 15, 16, 19, 21, 28-37).

P. gracilescens that is generally found in L. piscatorius and occasionally in various fish species of the European coasts of the Atlantic Ocean, Mediterranean Sea, Aegean Sea, and Black Sea has not been discovered in the Turkey seas. The morphometric measures are consistent with those reported by Bartoli et al. (27). P. gracilescens has been recorded for the first time in the parasitic fauna of the marine fishes of Turkey.

CONCLUSION

We investigated nine L. piscatorius samples and noted that 33% of the fishes were not infected with any trematode. Infection rates of both P. gracilescens and A. tubarium are 44% (Table 3). We found neither nematode nor any other parasite groups except digenean parasites in L. piscatorius. In light of the literature, it is obvious that a lot of parasite taxa were found in L. piscatorius of various seas of the world (38-52) (Table 4). Consequently, parasites of the angler fish of Turkish seas must be comprehensively studied.

Ethics Committee Approval: Author declared that the study was conducted according to the principles of the World Medical Association Declaration of Helsinki "Ethical Principles for Medical Research Involving Human Subjects" (amended in October 2013).

Informed Consent: Not required in this study.

Peer-review: Externally peer-reviewed.

Acknowledgements: The author would like to thank Dr. R.A. Bray from the NHM of London for his help on verification of the descriptions.

Conflict of Interest: No conflict of interest was declared by the authors.

Financial Disclosure: The authors declared that this study has received no financial support

Etik Komite Onayi: Yazar calismanin World Medical Association Declaration of Helsinki "Ethical Principles for Medical Research Involving Human Subjects", (amended in October 2013) prensiplerine uygun olarak yapildigini beyan etmistir.

Hasta Onami: Bu calisma icin hasta onamina gerek yoktur. Hakem Degerlendirmesi: Dis Bagimsiz.

Tesekkur: Yazar, Londra Natural History Museum'da gorevli olan Dr. R.A. Bray'a teshislerin dogrulanmasindaki yardimlarindan dolayi tesekkur eder.

Cikar Catismasi: Yazarlar cikar catismasi bildirmemislerdir.

Finansal Destek: Yazarlar bu calisma icin finansal destek almadiklarini beyan etmislerdir.

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Yahya Tepe

Department of Biology, Ataturk University School of Medicine, Erzurum, Turkey

Address for Correspondence / Yazy[thorn]ma Adresi: Yahya Tepe E.mail: tepeyahya@hotmail.com

[c]Copyright 2017 Turkish Society for Parasitology - Available online at www.tparazitolderg.org

[c]Telif hakky 2017 Turkiye Parazitoloji Derne[eth]i - Makale metnine www.tparazitolderg.org web sayfasindan ula[thorn]ylabilir.
Table 1. The measurements of Aphallus tubarium ([mu]m)
[min-max (average)]

                              Lophius piscatorius    Dentex dentex
Aphallus tubarium              Izmir, Aegean Sea   Scandola, Corsica
(Rudolphi, 1819) Poche, 1926    (present study)           (13)

Length                          1990-4001 (2947)     2425-4797 (2894)
Width                            264-528 (381)        341-682 (519)
Oral Sucker Length               105-145 (122)        124-217 (186)
Oral Sucker Width                121-162 (141)        152-250 (201)
Ventral Sucker Length            113-162 (130)        130-234 (187)
Ventral Sucker Width             105-145 (120)        124-234 (191)
Pharynx Length                    73-105 (88)         104-152 (124)
Pharynx Width                     65-81 (74)           76-130 (103)
Prepharynx                       121-242 (178)         39-108 (81)
Esophagus                        267-687 (492)        130-423 (260)
Anterior Testis Length            81-170 (117)        160-293 (213)
Anterior Testis Width             73-202 (122)        149-320 (237)
Posterior Testis Length           73-218 (137)        197-373 (249)
Posterior Testis Width            73-218 (140)        160-320 (243)
Ovary Length                     105-210 (157)        133-229 (191)
Ovary Width                       81-242 (146)        160-320 (250)
Egg Length                        12-20 (17)          20-24 (22)
Egg Width                          8-10 (9)            7-13 (9)

                              Syngnathus typhle
Aphallus tubarium                 Black Sea
(Rudolphi, 1819) Poche, 1926         (22)

Length                            2553-3243
Width                              552
Oral Sucker Length                 152-179
Oral Sucker Width                  193-221
Ventral Sucker Length              152
Ventral Sucker Width               166
Pharynx Length                      97
Pharynx Width                      110
Prepharynx                    Data not reported
Esophagus                     Data not reported
Anterior Testis Length             317-386
Anterior Testis Width              290-317
Posterior Testis Length            345-400
Posterior Testis Width             290-386
Ovary Length                       207-276
Ovary Width                        207-386
Egg Length                          19-22
Egg Width                            8-11

Table 2. Some morphometric measures of Prosorhynchoides gracilescens
([mu]m) [min-max (average)]

                                       Lophius piscatorius
Aphallus tubarium             Izmir, Aegean Sea  Gulf of Marseille
(Rudolphi, 1819) Poche, 1926   (present study)         (27)

Length                         2397-4692 (3323)  2180-5024 (3328)
Width                           467-995 (739)     537-900 (702)
Oral Sucker Length              203-406 (292)     356-425 (385)
Oral Sucker Width                41-508 (294)     286-419 (353)
Pharynx Length                  102-183 (153)     120-190 (146)
Pharynx Width                   122-183 (159)     147-235 (179)
Intestinal Cecum Length         345-630 (470)     254-483 (334)
Intestinal Cecum Width          142-284 (232)     160-330 (224)
Anterior Testis Length          223-366 (276)     254-380 (312)
Anterior Testis Width           162-264 (211)     191-305 (238)
Posterior Testis Length         223-366 (282)     224-380 (288)
Posterior Testis Width          162-264 (210)     159-330 (224)
Ovary Length                    122-244 (191)     178-273 (212)
Ovary Width                     122-223 (166)     133-210 (179)
Cirrus-Sac Length               731-1198 (905)    584-1232 (942)
Cirrus-Sac Width                122-223 (166)     143-235 (186)
Egg Length                       20-24 (23)        19-22 (20,8)
Egg Width                        14-18 (16)        15-17 (16.3)

                              Lophius piscatorius
Aphallus tubarium               Off England
(Rudolphi, 1819) Poche, 1926        (27)

Length                        1643-2830 (2149)
Width                          355-553 (430)
Oral Sucker Length             191-279 (244)
Oral Sucker Width              191-267 (232)
Pharynx Length                 106-138 (121)
Pharynx Width                  118-165 (138)
Intestinal Cecum Length        154-358 (284)
Intestinal Cecum Width         114-182 (150)
Anterior Testis Length         199-288 (230)
Anterior Testis Width          133-189 (154)
Posterior Testis Length        169-266 (211)
Posterior Testis Width          77-179 (143)
Ovary Length                   122-224 (169)
Ovary Width                     95-197 (123)
Cirrus-Sac Length              500-635 (574)
Cirrus-Sac Width                93-154 (117)
Egg Length                      19-22 (21.1)
Egg Width                       14-17 (16.1)

Table 3. Parasite numbers of Lophius piscatorius

Host Number        1  2  3  4  5  6  7  8  9  TPN   %  FREE

Aphallus tubarium  -  -  7  9  2  -  -  9  -  27   44  33
Prosorhynchoides   -  -  -  2  -  3  7  2  -  14   44
grasilescens

TPN: total parasite number; %: prevalence; FREE: the rate of uninfected
fishes

Table 4. The parasites of Lophius piscatorius from various localities

PARASITE                   LOCALITY            AUTHOR
DIGENEA

Aphallus tubarium          France              (39)
                           Greece              (19)
Prosorhynchoides borealis  Northeast Atlantic  (27)
P. gracilescens            England             (9), (10), (29), (31),
                                               (32), (33)
                           France              (39), (27)
                           Germany             (15), (28), (40)
                           Icelandic Waters    (35), (41), (42)
                           Irish Sea           (34),
                           Italy               (16), (30)
                           North Sea           (36)
                           Ukraine             (21)
                           West Africa         (43)
Prosorhynchus aculeatus    France              (39)
P. crucibulum              England             (10), (33)
Derogenes latus            France              (39)
D. varicus                 England             (10), (32), (33)
                           Icelandic Waters    (35)
Dinosoma sp.               France              (39)
D. lophiomi                Western             (44)
                           Mediterranean
Distomum cesticillus       Germany             (40)
                           Italy               (30)
Di. hystrix                Germany             (40)
Ectenurus lepidus          England             (10)
Gonocerca crassa           USA                 (45)
Hemiurus communis          England             (10), (32), (33)
Lecithaster gibbosus       Icelandic Waters    (35)
Lecithochirium fusiforme   France              (39)
L. grandiporum             Western             (46)
                           Mediterranean
L. musculus                France              (39)
L. physcon                 England             (10)
L. rufoviride              England             (10), (32), (33)
L. excisum                 England             (10)
Metadena brotulae          USA                 (10)
Otodistomum sp.            Icelandic Waters    (35)

Table 4. The parasites of Lophius piscatorius from various localities
(continued)

PARASITE                    LOCALITY          AUTHOR
DIGENEA

O. veliporum (larvae)       England           (10)
Stephanostomum sp.          Icelandic Waters  (35)
S. baccatum (larvae)        England           (10)
S. caducum                  England           (10)
S. cesticillum              England           (10)
                            Egypt             (47)
                            France            (39)
                            Italy             (20)
                            Western
                            Mediterranean     (48)
Steringophorus furciger     Icelandic Waters  (35)
                            England           (10)
Sterrhurus floridensis      USA               (45)
S. fusiforme                England           (10), (33)
S. grandiporus              England           (10)
S. musculus                 England           (10)
Synaptobothrium             England           (10), (32)
caudiporum                  France            (39)
Zoogonoides viviparus       Icelandic Waters  (35)
CESTODA
Bothrioceplialus lophii     Germany           (40)
Grillotia sp.               Icelandic Waters  (35)
Rhynchobothrium             Germany           (40)
crassiceps
R. palcaceum                Germany           (40)
R. tennicolle               Germany           (40)
R. erinaceus                Germany           (40)
Scolex polymorphus          Germany           (40)
S. lophii piscatorii        Germany           (40)
Tetraphyllid plerocercoids  Icelandic Waters  (35)
Tetrarhynchus lophii        Germany           (40)
piscatorii
NEMATODA
Agamonema capsularia        Germany           (40)
A. commune                  Germany           (40)
A. lophii piscatorii        Germany           (40)
Anisakis simplex            Icelandic Waters  (35)
Ascaris angulata            Germany           (40)
A. incvescens               Germany           (40)
A. rigida                   Germany           (40)
Contracaecum clavatum       England           (33)
                            Italy             (20)
Capillaria sp.              Icelandic Waters  (35)
Dikentrocephalus crinalis   Germany           (40)

Table 4. The parasites of Lophius piscatorius from various localities
(continued)

PARASITE                   LOCALITY          AUTHOR
DIGENEA

Hysterothylacium sp.       Icelandic Waters  (35)
H. aduncum                 Icelandic Waters  (35)
                           Turkey            (7)
H. rigidum                 England           (33)
                           Icelandic Waters  (35)
Cucullanus hians           England           (33)
Spinitectus sp.            Icelandic Waters  (35)
Phocascaris sp.            Icelandic Waters  (35)
Pseudoterranova decipiens  Icelandic Waters  (35)
ACANTHOCEPHALA
Echinorhynchus acus        Germany           (40)
E. casculosus              Germany           (40)
E. gadi                    Icelandic Waters  (35)
E. globosus                USA               (49)
E. propinquus              Italy             (17)
ANNELIDA-HIRUDINEA
Calliobdella lophii        England           (50)
                           Norway To
                           Mediterranean     (51)
ARTHROPODA-CRUSTACEA
Bomolochus attenuates      Panama            (52)
Chondracanthus lophii      Turkey            (6)
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Author:Tepe, Yahya
Publication:Turkish Journal of Parasitology
Article Type:Report
Date:Mar 1, 2017
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