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Ukrainian Journal of Ecology
Ukrainian Journal ofEcology, 2020,10(3), 86-92, doi: 10.15421/2020_172
ORIGINAL ARTICLE
Parasite diversity from two deep-sea fishes Phycis blennoides (Brunnich, 1768) and Phycis phycis (Linne, 1758),
from the western Algerian coasts
M.M. Hassani1, A. Kerfouf2, A. Baaloudj3*, F. Denis4
1 Department of biology, Sciences Faculty, Saida University, 20000, Algeria 2,4Laboratoire d'écodéveloppement des espaces, Université Sidi Bel Abbes, 22000, Algeria 3Laboratoire Biologie, Eau et Environnement (LBEE). Faculté SNV-STU, Université 8 Mai 1945 Guelma
BP.40124000 Guelma, Algeria 4Département Milieux et Peuplements Aquatiques, UMR 7208 'BOREA, Station de Biologie Marine du MNHN,
Place de la Croix, 29182, Concarneau, France
Corresponding author E-mail: bafef@yahoo.fr
Received: 04.08.2020. Accepted: 04.09.2020
This study investigated the diversity of metazoan parasites of 132 greater forkbeards and 91 forkbeards, from the western Algerian coasts, a total of 19 taxa: 15 taxa from Phycis blennoides, 11 taxa from Phycis phycis, allocated to 15 genera in 12 families were recovered, including 7species common to the two hosts. 90% are endoparasites, mostly located in the intestine and the stomach, encapsulate forms were in the liver, whereas crustaceans were found in the gills of the hosts. The Anisakidae Railliet & Henry, (1912) is the most diverse group with two genera: Hysterothylacium Ward & Magath, (1917) and Anisakis Dujardin, (1845) with 5 species. The nematode Hysterothylacium fabri(P= 55%) and the digenean Stephanostomum pristis are the most abundant and the most prevalent parasites from P. phycis (P=94%), while Hysterothylacium aduncum (P=49%) and Lepidapedon guevarai (P=87%) are from P. blennoides. 14 parasites species are present as adult stage, indicated that these fish act as their definitive hosts, while cosmopolite species are present in the larval stage. We also noticed a high ectoparasites infection level from hosts gills Clavella alata (P=45%) in greater forkbeards and Gnathia sp (P=65%) from forkbeards. Phycis blennoides and Phycis phycis are new hosts records for Cucullanus cirratus, Capillaria gracilis, Derogenese varicus and Lectthocldium excisum.
Keywords: Parasites; Gadiform fishes; Deep sea; Western Algerian coasts
Introduction
Inventories of fish parasites are operated for decades in order to have informations on biodiversity in aquatic ecosystems (Poulin and Rohde, 1997; Morand and Gonzales, 1997), moreover in large bathymetries, that still poorly explored because of their inaccessibility (Klimpel et al., 2010).
Fish parasites of the Algerian coasts were first studied by Dollfus (1935), later; Petter and Maillard (1988) described some nematodes from Dollfus collection. Since little works on marine fish parasites have been published besides,they focused on digenea trematodes group from the western Algerian coasts (Abid-Kachour et al., 2013; Marzoug et al., 2012, 2014; Rima et al., 2017; Brahim tazi et al., 2016) and ectoparasites, mainly monogenean and copepods, from the eastern coasts (Boualleg et al., 2011; Kouachi et al., 2014; Ramdane et al., 2013 ), studies on nematodes are even rarer (Hassani and Kerfouf, 2014; Hassani et al., 2015; Ichalal et al., 2015). Phycis blennoides and Phycis Phycis, two congeneric gadiform fish, caught in depths of up to -1000 m, and with great economic value in Algeria were the subject of two studies that focused on Nematodes Anisakidae because of their pathogenicity by Valero et al., (2005) and Farjallah et al., (2006) in Southern Spain and eastern Mediterranean coasts, Tunisia respectively, Dallares et al., (2016) provided a complete description of the parasite community of the greater forkbeard. The aim of this study, is to drew up an inventory of parasites of both fish P. blennoides, and especially P. phycis that parasite fauna remains insufficient in Algerian and Mediterranean coast.
Materials and Methods
Fish and collection site
The 132 Phycis. blennoides were harvested near the fishing ports (Benisaf, Oran and Mostaganem) and the 91 Phycis phycis were captured by the fishermen of small trades (Ain el turck and Kristel located in Oran). Sampling sites along the Algerian coast of the Western Mediterranean located at 35°43' N - 0°37' W (the total length of fishes ranged from 16 to 32 cm. Fishes were examined for ecto- and endoparasites according to a standardized protocol from June 2015 to October 2016. Collection and analysis of parasites
All organs were dissected out and examined under a stereomicroscope. This included examination of the content (digestive tubes and appendices and their gonads as well. Stomach, pyloric caecums, intestine) of the parts of the intestinal tract separately. The contents were cleared by successive rinsing in physiological saline water (9%). The intestinal mucosa was scraped and the liver, gallbladder and gonads were squeezed between two Petri dishes and examined. Harvested parasites were fixed and preserved at ethanol (70)
Specimens were stained with iron acetocarmine according to the protocol of Georgiev et al. (1986), dehydrated in a graded ethanol series, cleared in Eugenol and examined as permanent mounts in Canada balsam. All parasites were identified to the lowest taxonomic level possible and counted.
The identification of parasites was carried out using the identification keys of (Anderson, 1992) and (Moravec, 1998) for Nematodes. (Gibson et al., 2002) for the Digenea, (Kabata, and Gusev, 1966) for Crustaceans, (Khalil et al., 1994) for the Cestoda and finally (Amin's, 1987) identification keys for Acanthocephalans.
The ecological terms defined by Bush et al. (1997) have been used in our present study. Prevalence represents the percentage (P%) of host individuals infested with a parasitic species in the sample, divided by the number of host fish examined. Average abundance (AM) refers to the total number of individuals of the particular parasite species divided by the total number of hosts examined in the sample (Figure 1).
Algeria
Figure 1. Geographical location of the studied area. (Kerfouf et al., 2007).
Results
A total of 1984 specimens of helminthes parasites were recovered from both host species, representing 19 species and 14 genera, as listed below (Table 1). (9 Nematoda 1 Acanthocephalan, 6 Digenea, 1 Cestoda and 2 Crustaceans).
Table 1. Metazoan parasite of Phycis blennoides and Phycis phycis from the western Algerian coasts (with citations of other regions).
Parasite species from present study with taxonomic Host P% AM Site Other report Area
position Infection reference
Phylum Platyhelminthes Claus, 1887 PPHY 20% 1,75 Posterior Bartoli, et al., [7]
Class Trematoda Rudolph, 1808 intestine 2005 [12]
Sub-class Digenea Carus, 1863 rectum Akmirza 2013
Super family Allocreadioidea Loos, 1902
Family Opecoelidae Ozaki, 1925
Sub family Plagioporinae Manter, 1947
Genus Bathycreadium Kabata, 1961
1. Bathycreadium elongata Maillard, 1970 (adult
stage)
PBLE 76% 20,8 Stomach Perez Del Olmo [13]
2. Bathycreadium brayi Perez-del-Olmo, 2014 (adult anterior et al., 2014
and juvenile) intestine L CI l.f ¿—\J.LI
Synonymes: Nicolla elongata Maillard, 1970 Dallares et al., [14]
Bathyreadium elongatum Maillard, 1970 2016
Super family Hemiuroidea Looss, 1899 PBLE 0,5% 0,25 Stomach Bartoli, et al., [7]
Family Deroginidae Nccoll, 1910 PPHY 2% 1 2005 [11]
Sub family Derogeninae Nicoll, 1910 Ternengo et al.,
Genus Derogenes Janiszewska, 1953 2009 (as
3.* Derogenes varicus Müller, 1784 (adult stage) Derogenes
latus)
Family Hemiuridae Loos, 1899 PBLE 1% 0,03 Stomach
Sub family Elytrophallinae Skrjabin et Guschanskaja, 1945
Genus Lecithocladium Lühe, 1901 4.*Lecithocladium excisum Rudolphi, 1819 (adult)
Super family Lepocreadioidea Odhner, 1905 PPHY 94% 18,3 Stomach Papoutsoglou [3]
Family Acanthocopidae Lûhe, 1909 anterior 1976 [7]
Genus Stephanostomum Loss, 1899 intestine Bartoli et Bray [8]
5. Stephanostomum pristis Deslongchamps 1824 (adult and 2001 [11]
juvenile) Bartoli, et al.,
2005
Ternengo et al
., 2009
Family Lepocreadiidae Odhner, 1905 PBLE 87% 13 Stomach, Lopez Roman et [2]
Genus Lepidapedon Stafford, 1904 pylorique Maillard 1973 [4]
6.Lepidapedon guevarai Lopez-Roman et Maillard, 1973 caeca Orecchia et [6]
(adult and juvenile) intestine Paggy
Bray et Gibson, [14]
1997
Dallares et al.,
2016 (as L [15]
Lepidapedon.sp)
Perz Del Olmo
et al., 2019
Class Cestoda PBLE 10% 0,5 Intestine Dallares., 2016 [14]
Subclasse Eucestoda Ternengo et al [11]
7.Order Tetraphyllidae Carus 1863 (larvae stage) ., 2009
Phylum Nematoda Rudolphi, 1808 P 12% 0,22 Stomach, Petter et [5]
Class Secernentea Von Linstow, 1905 BLE 55% 3,62 intestine Radujkovic,1989
Order Ascaridida Skrjabin et Shultz, 1940 PPHY liver Akmirza 2013 [13]
Superfamily Ascaridoidea Railliet et Henry, 1915 Ternengo et [11]
Family Anisakidae Railliet et Henry, 1912 al.,2009
Genus Hysterothylacium Ward et Magath, 1917 Valero et al., [9]
8. Hysterothylacium fabri Ward et Magath, 1917 (third 2005 [10]
stage larvae) Farjallah et al.,
Synonymes: Ascaris fabri Rudolphi, 1819; Ascaris biuncinata 2006
Molin, 1858; Ascaris fiformis
Stossich, 1904
9. Hysterothylacium aduncum Rudolphi, 1802 (adult P 49% 1,35 Oesophagus, Valero et al., [9]
stage) BLE 11% 0,12 Stomach, 2005 [10]
PPHY intestine Farjallah et al.,
rectum 2006
10.* Hysterothylacium sp1 (larval stage) PBLE 3% 0,03 Intestine Petter et [5]
Radujkovic,1989
Genus Anisakis Dujardin, 1845 PBLE 7% 0,1 Liver (cysts), Valero et al., [9]
11. Anisakis simplex Rudolphi, 1809 (Third stage larvae) PPHY 6% 0,09 intestine 2005 [10]
Synonymes: Anisakis marina Linné, 1767; Anisakis sp. Berland, stomach Farjallah et al., [14]
1961 2006
Dallares et al.,
2016 (as
Anisakis sp)
12. Anisakis physeteris Baylis, 1923 (third stage larvae) PBLE 11% 0,25 Liver (cysts), Valero et al., [9]
Synonymes: Anisakis sp. larvall Berland, 1961 PPHY 9% 0,09 intestine 2005 [10]
stomach Farjallah et al.,
2006
Superfamily Seuratoidea Hall, 1916 PBLE 32% 0,40 Posterior Dallares et al., [14]
Family Cucullanidae Cobbold, 1864 PPHY 23% 0,65 intestine 2016 (as
Genus Cucullanus Müller 1777 rectum Cucullanus sp)
13.* Cucullanus cirratus Müller, 1777
Synonymes: Cucullanus muticus Müller,1777; Cucullanus marinus Müller, 1779 ;
Cucullanus crrrhatus Pallas, 1781; Cucullanus foveolatus Rudolphi, 1809; Dacnttis gadorum Beneden, 1858; Heterakis foveolata Schneider, 1866; Cucullanus globosus Linton, 1901
Order Spirurida Chitwood, 1933 Super family Dracunculoidea Stiles, 1907 Family Philometridae Baylis et Daubney, 1926 Genus Philometra Costa, 1845
14. Philometra globiceps Rudolphi, 1819 (adult stage) Synonymes: Filaria globiceps Rudolphi, 1819; Philometra retrccaudata Costa, 1845; Ichtyonema globiceps Diesing, 1861
PPHY 6% 0,15 Gonades
Ternengo et [11] al.,2009 [5]
Petter et Radujkovic,1989
PBLE 2% 0,025 Oesophagus Petter, 1970 [1] Super family Habronematoidea Chitwood et Wehr, 1932 Dallarás et al., [l4]
Family Cystidicoiidae Skrjabin, 1946 2016
Genus Collarinema, Sey, 1970
15. Collarinema collaris Petter, 1970 (adult stage)
Synonym: Ascarophis collaris
Class Adenophorea Linstow, 1905 PBLE 26% 1 Posterior Dallarás et al., [14]
Order Enoplida PPHY 17% 0,40 intestine 2016
Super family Trcchuroidea Railliet, 1916 Rectum
Family Capillariidae Railliet, 1915
Genus Capillaria Zeder, 1800
Sub-genus Procapillaria Moravec, 1987
16.* Capillaria gracilis Bellingham, 1840 Travassos, 1915 (adult stage)
Synonymes: Trichosoma gracile Bellingham, 1840; Capillaria kabatai Inglis and Cole, 1963 ; Capillaria merluccii Reimer, 1991
Phylum Acanthocephala Meyer, 1931
Class Palaeacanthocephala Meyer, 1931
Order Echinorhynchida Southwell et Macfie, 1925
Family Echinorhynchidae Cobbold, 1876
Sub- family Echinorhynchinae Cobbold, 1876
Genus Echinorhynchus Zoega in Müller, 1776 (adult stage)
17. Echinorhynchus sp
Synonymes: Metechinorhynchus Petrochenko, 1956
Phylum Arthropodes
Class Maxillopodes, Dahl, 1956
Order Siphonostomatoida Thorell, 1859
Family Lernaeopodidae Olsson 1869
Genus Clavella Oken, 1815
18. Clavella alata Brian, 1906 (Adult satge) Classe Malacostraca Latreille 1806
Sub class Eumalacostraca Grobben 1892 Super order Peracarida Calman 1904 Order IsopodesLatreille 1817 Sub ordre Gnathiidea Leach 1814 Family Gnathiidae Harger 1880 Genus Gnathia Leach, 1813(Adultes)
19. Gnathia sp
PBLE 10% 0,21 Intestine Dallarás et al., [14] pyloric caeca 2016
PBLE 45% 2,4 Gills Dallarás et al., [14]
2016
PPHY 65% 23 Gills Ternengo et [11]
al.,2009
[1] A Coruna, Spain; [2] Alboran sea, Spain; [3] Saronicos, Gulf Athens, Greece; [4] Ligurian sea, Italy; [5] Montenegro; [6] North east atlantic; [7] Natural Reserve of Scandola, the Gulf of Marseilles, France; [8] Natural reserve off Corsica, France; [9] Mediterranean coasts of Andalucia, Southern Spain; [10] eastern Mediterranean coasts, Tunisia; [11] Bonifacio Strait Marine Reserve, Corsica Island, Mediterranean Sea; [12] Coastal Waters of Gokgeada, Turkey; [13] western Mediterranean; [14] Balearic Sea, Spain; [15]western Mediterranean.
PBLE: Phycis blennoides, PPHY:Phycis phycis, P: prevalence; AM: mean abundance.* New host record.
Discussion
A total of 1984 parasites were collected in this study, 1190 from Phycis. blennoides and 794 from Phycis. phycis, in the studied area with total prevalence of 99% and mean abundance of 9 parasites per host fish (Table 1). In Corsica Ternengo et al., (2009), identified 7 taxa from P. phycis, in the Balearic Sea, Dallares et al., (2016) identified 17 from P. blennoides. Nematodes are the parasite taxa with the most common species to the two forkbeards. Cucullanus cirratus and Capillaria gracilis, were reported by Perdiguero- Alonso et al. (2008) in atlantic cod with similar abundance and prevalence and appointed as gadoids specialists' nematodes with great host specificity (Moravec et al., 1997). Ternengo et al., (2009) identified Cucullanus longicollis from P. phycis while Dallares et al., (2016) identified Cucullanus sp from P. blennoides.
The Cystidicolidae Collarinema collaris was identified from P. blennoides by Petter (1970) in A Coruna in Spain, and assigned it to the genus Ascarophis Van Beneden, 1870, it was assigned to Collarinema after scanning electron microscopy of its cephalic ultrastructure (Moravec & Sobecka, 2012).
However, H. aduncum is more prevalent and more abundant in P. blennoides, while H. fabri is more prevalent and more abundant in P. phycis Similar findings have been also reported in other Mediterranean areas (Valero et al., 2005; Farjallah et al ., 2006; Dallares et al., 2016 ). Otherwise, the community of digenea was composed of Derogense varicus, which is the only common digenean to both fishes with low infestation. Ternengo (2009) identified a Derogenidae from P. phycis as D. latus, Manter (1955) pointed out that D. varicus, while a shallow-water parasite in northern latitudes, also occurs in deep water in lower latitudes (Bray, 2020). Stephanostomum pristis and Lepidapedon guevarai are the most prevalent and abundant parasites from P. Phycis and P. blennoides respectively, L. guevarai is the only report of P. blennoides parasite out of the Mediterranean waters in North east atlantic (Bray & Gibson, 1997). Most digenea parasites of deep water fishes are belonging to the genus Lepidapedon (Bray, 2004), it appears that the deep-sea fauna is constituted of a mixture of higher taxa which have radiated in the deep-sea as Lepidapedon,
that is later reinforced by molecular studies, but there is a distinct set of deep-sea digenea that are not found in shallow waters (Perez Del Olmo et al., 2019).
The family Opecoelidae Ozaki, 1925 is represented by one species in each host, Bathycreadium brayi from the anterior portion of digestive tract of P. blennoides, was identified by Perez Del Olmo et al., (2014) in western Mediterranean and reported by Dallares et al. (2016), it is sometimes confused with Bathycreadium biscayense Bray, 1973 which is narrower with a longer esophagus (Perez-Del-Olmo et al., 2014). Bathycreadium elongata from the posterior portion of digestive tract of P. phycis was reported from the natural reserve of Scandola in the gulf of Marseilles in France (Bartoli et al., 2005) and from the coastal waters of Gokgeada in Turkey ( Akmirza 2013).
The only Cestoda from the order of Tetraphyllidae and the acanthocephalan belonging to the genus Echinorhynchus were present only in P. blennoides, also reported in western Mediterranean (Dallares et al., 2016) with higher levels of infection than in our samples. We found different ectoparasite species in the gills of each host: Gnathia sp in P. phycis and C. alata in P. blennoides, that been reported too from Balearic sea with similar ecological indices.
In the other hand, Paterson & Gray (1997) estimated that taxonomic compositions of the parasite communities are generally similar when the hosts are phylogenetically related. This could be one of the direct consequences of a shared inheritance, Le Pommelet et al., (1997) found no significant differences in the composition of the parasitic communities of red stripped mullet and red mullet from the Gulf of Lion and the Corsican coast, despite their different habitats, while Abid-Kachour et al., (2019) noticed that the two congener sparid fishes Pagellus erythrinus (Linnaeus, 1758) and Pagellus acarne (Risso, 1827), from the western Mediterranean coast of Algeria hosts different digenea parasites structure. In this study phylogeny seems not to be a factor structuring the parasite community, Hysterothylacium sp1; Collarinema collaris; Lepidapedon guevarai and Bathycreamium. brayi have been reported only in P. blennoides, as well as P. giobiceps, Lecithocladium excisum; Stephanostomum pristis and Bathycreamium elongata that were present only in P. phycis, this hosts one less digenean species than P. blennoides.
According Sorbe (1977), Macpherson (1978) and Morte et al., (2002), P. blennoides is a nectobenthic, predatory and euryphagous fish, its wide range of prey consists mainly of crustaceans, with a predominance of decapods, teleost fish represent a small proportion of the total ingested prey. While, P. phycis is carnivorous that feed mainly on mobile prey, unlike P. blennoides, his diet consists largely of fish with a small part of decapods (Papaconstantinou & Caragitsou, 1989; Morato et al., 1999). Since most common parasites to both forkbeards are in larval stages, indeed, many studies have reported the approximation of host fish based solely on their sub-communities of adult parasites, considering that the larvae are more generalist and that their presence in the host is often random (Morand et al., 2000).
The digenea Podocotyle sp and Steringotrema sp, in addition of the nematoda: Capillostrongyloides morae and Raphidascaris sp, the Isopode Cymothoidae sp as well as the Cestoda Grillotia erinaceus were reported from P. blennoides from Balearic sea (Dallares et al. 2016), the digenean D. varicus, the nematodes Hysterothylacium sp1 and A. physeteris were found herein. These differences may be related to the difference in habitat and therefore availability of prey. P. blennoides has different diet associated with bathymetric migration involving different composition macro invertebrate communities along the continental slope; diet influences the composition of the community of endoparasites because the majority of them are transmitted by the ingestion of infected preys (Price & Clancy, 1983; Morand et al., 2000). Thus, Dallares et al., (2016) estimate that P. blennoides is one of the most parasited species in the family of Phycidae, despite its deep-water habitat, where parasite diversity tends to decrease the further one gets away from the continental slope, as direct consequence of the decline of populations of benthic invertebrates that can serve as intermediate hosts to parasites (Klimpel et al., 2010; Bray, 2020). Despite some differences in taxonomic composition of parasites communities, numerical descriptors are mostly similar to those of Valero et al. (2005), Farjallah et al. (2006) and Dallares et al. (2016), in Andalusia, Tunisia and Balearic sea respectively, this can be explained by the relative constancy of the abiotic factors in the Mediterranean deep sea (salinity, oligothrophy, oxygenation and temperature) (Hopkins, 1984) that could influencing the composition of intermediate hosts.
Conclusion
Very little is known about deep-sea digenea and moreover nematodes, herein, the taxonomic and numerical descriptors (parasitological indexes) of parasitic community of forkbeards differs despite their close phylogeny, because hosts often have ecological differences in habitat, geographical distribution or diet, these factors act as filters that can affect and modify the structure and dynamics of parasitic infracommunities (Holmes and Price, 1980), the latter being ultimately the result of compromises between host phylogeny and ecological processes during the evolutionary history of each species of parasite, this trait remains one of the most important variable of parasite distribution.
Aknowlegments
We wish to thank Dr. ZINAI Amina for her comments and suggestions on the manuscript. We are grateful to all persons who contributed to the field and lab analysis. We thank the MERS and the DGRSDT for supporting and funding this work.
References
Abid-Kachour, S., Mouffok, S., Boutiba, Z. (2013). Description of a new species of Sphincteristomum from Sparid fishes of the Algerian coast (Western Mediterranean). Journal of Environnement protections sciences 04 (10),1129-1136. Abid-Kachour, S., Rouane Hacene, O., Mouffok, S., Bouderbala, M. (2019). Digenean parasites in two congeneric sparid fish and of commercial importance, Pagellus erythrinus (Linnaeus, 1758) and Pagellus acarne (Risso, 1827), from the western Mediterranean coast of Algeria. Biodiversity Journal 10 (2), 151-158.
Akmirza, A. (2013). Parasitic Nematodes of Fish in the Coastal Waters of Gokçeada. The Turkish journal of Parasitology 37, 199-202.
Amin, OM. (1987). Key to the families and subfamilies of Acanthocephala, with the erection of a new class (Polyacanthocephala) and a new order (Polyacanthorhynchida), Journal of Parasitology, 73(6), 1216-1219. Anderson, RC. (1992). Nematode Parasites of Vertebrates, Their Developmentand Transmission. Walligford, CABI publishing. 340 p.
Bartoli, P., Bray, R. (2001). Contribution to the knowledge of species of the genus Stephanostomum Loss, 1899 (Digenea, Acanthocolpidae) from Teleosts of the Western Mediterranean, with the description of S. gaidropsari n. sp.
Systematic Parasitology 49, 159-188.Bartoli, P., Gibson, D.I., Bray, R.A. (2005). Digenean species diversity in teleost fish from a nature reserve off Corsica, France (Western Mediterranean), and a comparison with other Mediterranean regions, Journal of Natural History, 39:1, 47-70.
Boualleg, C., Kaouachi, N., Seridi, M., Ternengo, S., Bensouilah, M. (2011). Copepod parasites of gills of 14 teleost fish species caught in the gulf of Annaba (Algeria). African Journal of Microbiology Research 5 (25) 4253-4259. Brahim Tazi, AN., Meddour, A., Nadjadi, Z., Boutiba, Z. (2016). First Records of Helminth Parasites of Dicentrarchus labrax in the Western Coast of Algeria. Journal of Applied and Environmental Biological Sciences 6(1), 46-51. Bray, RA. (2004). The bathymetric distribution of the Digenean parasites of deep-sea fishes. Folia Parasitologia 51, 268-274.
Bray, RA., Gibson, DI. (1997). The Lepocreadiidae Odhner, 1905 (Digenea) of fishes from the north-east Atlantic, summary paper, with keys and checklists. Systematic Parasitology 36, 223-228. Bray, RA. (2020). Digenean parasites of deep-sea teleosts, a progress report. International Journal for Parasitology, Parasites and Wildlife. Journal preproof.
Dallarás, S., Moyà-Alcover, CM., Padros, F., Cartes, JE., Sole, M., Castañeda, C., Carrasson, M. (2016). The parasite community of Phycis blennoides (Brünnich, 1768) from the Balearic Sea in relation to diet, biochemical markers, histopathology and environmental variables. Deep Sea Research 118, 84-100. Dollfus, RP. (1935). Sur quelques parasites de Poissons récoltés à Castiglione (Algérie). Bulletin de la société nationale d'Agriculture 2, 199-279.
Farjallah, S., Ben Slimane, B., Blel, H., Amor, N. (2006). Anisakid parasites of two forkbeards (Phycis blennoides and Phycis phycis) from the eastern Mediterranean coasts in Tunisia. Parasitology Research 100(1), 11-17. Georgiev, VB., Boyko, B., Genov, T. (1986). In toto staining method for cestodes with iron acetocarmine. Helminthologia23,279-281.
Gibson, DI., Jones, A., Bray, RA. (2002). Keys to the Trematoda. Volume I. Walligford, CABI publishing.The Natural History Museum, UK.512p
Hassani, MM., Kerfouf, A. (2014). Diversity of Nematodes parasites of the greater forkbeard Phycis blennoides in the western Mediterranean Sea. International Journal of Scientific Basic and Applied Research 18 (2), 97-103.
Hassani, MM., Kerfouf, A., Boutiba, Z. (2015). Checklist of helminthes parasites of Striped Red Mullet, Mullus surmuletus (Linnaeus, 1758) (Perciform, Mullidae), caught in the Bay of Kristel, Algeria (western Mediterranean). Check list 11(1),1-3.
Hoberg, EP., Adams, A. (2000). Phylogeny, history and biodiversity, understanding faunal structure and biogeography in the marine realm. Bulletin of Scandinave Society of Parasitology 10,19-37.
Holmes, JC., Price, PW. (1980). Parasites communities, the roles of phylogeny and ecology. Systematic Zoology 29, 203-213.
Hopkins, TS. (1984). Physics of the Sea. Western Mediterranean. Pergamon Press. Barcelona. 125p.
Ichalal, K., Ramdane, Z., Ider, D., Kacher, M., Iguerouada, M, Trilles, JP. (2015). Nematodes parasitizing Trachurus trachurus (L.) and Boops boops (L.) from Algeria. Parasitology Research 114, 11.
Khalil, L F., Jones, A., Bray, RA. (1994). Keys to the Cestoda Parasites of Vertebrates. Walligford, CABI publishing. 751 p.
Klimpel, S., Busch, MW., Sutton, T., Palm, HW. (2010). Meso- and bathy-pelagic fish parasites at the Mid-Atlantic Ridge (MAR), low host specificity and restricted parasite diversity. Deep Sea Research 57, 596-603.
Kouachi, N., Quilichini, Y., Djebbari, N., Boualleg, C., Ternengo, S., Gouasmia, G., Barour, C., Bensouilah, M. (2014). Detecting monogenean indicator species from teleost fishes off the eastern Algerian coastline using the IndVal method. Cahier de biologie marine 55, 295-304.
Le Pommelet, E., Bartoli, P., Silan, P. (1997). Biodiversité des digènes et autres helminthes intestinaux des Rougets, Synthèse pour Mullus surmuletus (Linné, 1758) et M. barbatus (L. 1758) dans le bassin méditerranéen. Annales de Sciences Naturelles Zoologie 18(4), 177-181.
Lopez-Roman, R., Maillard, C. (1973). Lepidapedon (Lepidapedon) guevarai n. sp. (Digenea Lepocreadiidae) parasito de Phycis blennoides (Brünnich) (Gadidae). Revista lberica de Parasitologia 33, 617-624.
Macpherson, E. (1978). Régimen alimentario de Phycis blennoides (Brûnnich) y Antonogadus megalokynodon (Kolombatovic) (pisces, gadidae) en el Mediteraneo occidental. Investig Pesq 42(2), 455-466.
Manter, H.W., (1955). Some digenetic trematodes from fishes of New Zealand. Trans. Royal Society of New Zeland, 82, 475-568.
Merzoug, D., Boutiba, Z., Gibson, DI., Perez-Del-Omo, A., Kostadinova, A. (2012). Descriptions of Digeneans from Sardina pilchardus (Walbaum) (Clupeidae) off the Algerian coast of the western Mediterranean, with a complete list of its helminthes parasites. Systematic Parasitology 17-34.
Merzoug, D., Rima, M, Boutiba, Z., Georgieva, S. (2014). A new species of Saturnius Manter, 1969 (Digenea:
Hemiuridae) from Mediterranean mullet (Teleostei: Mugilidae). Systematic Parasitology 87(2), 127-34
Morand, S., Gonzalez, EA. (1997). Is parasitism a missing ingredient in model ecosystems. Ecological Model 95,61-74.
Morand, S., Cribb, TH., Kulbicki, M., Rigby, MC., Chauvet, C., Dufour, V., Faliex, E., Galzin, R., Lo, CM., Lo-Yat, A.,
Pichelin, S., Sasal, P. (2000). Endoparasite species richness of New Caledonian butterfly fishes, host density and diet
matter. Parasitology 121, 65-73.
Morato, T., Solà, E., Grós, MP., Meneze,s G. (1999). Diets of forkbeard (Phycis phycis) and conger eel (Conger conger) off the Azores during spring of 1996 and 1997. Life Marine Sciences 17, 51-64.
Moravec, F. (1998). Nematodes of freshwater fishes of the neotropical regions. Academia and Kluwer Academic Publishers. Prague and Dordrecht. Boston, London. 395 p.
Moravec, F., Kohn, A., Fernandes, BMM. (1997). New observations on Seuratoid nematodes parasitic in fishes of the Parana river, Brazil. Folia Parasitologia 44, 209-223.
Moravec, F., Sobecka, E. (2012). Collarinema eutriglae n. sp (Nematoda, Cystidicolidae), a new gastric parasite of the scorpaeniform fish Eutrigla gurnardus (Osteichthyes, Triglidae) in the North Sea, with remarks on the systematic status
of Collarinema Systematic Parasitology 81(1), 71-77.
Morte, MS., Redon, MJ., Sanz-Brau, A. (2002). Diet of Phycis blennoides (Gadidae) in relation to fish size and season in the western Mediterranean (Spain). Marine Ecology 23(2), 141-155.
Orecchia, P., Paggi, L. (1978). Aspetti di sistematica e di ecologia degli elminti parassiti di pesci marini studiati presso Ustituto di Parassitologia Roma. Parassitologia 20, 73-89.
Papaconstantinou, C., Caragitsou, E. (1989). Feeding interactions between two sympatric species Pagrus pagrus and Phycis phycis around Kastellorizo island (Dodecanese, Greece). Fishery Research 7, 329-342.
Papoutsoglou, SE. (1976). Metazoan parasites of fishes from Saronicos Gulf Athens- Greece. Thalassographica 1, 69102.
Paterson, AM., Gray, RD. (1997). Host-parasite cospeciation host switching, and missing the boat. In Host-parasite Evolution, General Principles and Avian Models. Edition Clayton. D.H. et Moore. J. University Press. Oxford, UK. 250p. Perdiguero-Alonso, D., Monteo, F., Antonio, R., Kostadinova, A. (2008). Composition and structure of the parasite faunas of cod, Gadus morhua L. (Teleostei, Gadidae), in the North East Atlantic. Parasites and Vectors. 1(23), 1-18. Pérez-del-Olmo, A., Dallarés, S., Carrasson, M., Kostadinova, A. (2014). A new species of Bathycreadium Kabata, 1961 (Digenea, Opecoelidae) from Phycis blennoides (Brünnich) (Gadiformes, Phycidae) in the western Mediterranean. Systematic Parasitology 88(3), 233-44.
Petter, AJ., Maillard, C. (1988). Larves d'ascarides parasites de poissons en Méditerranée Occidentale. Bulletins du Muséum d'Histoire Naturelle 10, 347-369.
Petter, A.J. (1970). Une espèce nouvelle d'Ascarophis (Nematoda, Cystidicolinae) Parasite de Phycis blennoides (Brunnich) Gadidé. Revue des Travaux de l'Institut de Pêche Maritime 34(2), 221-225.
Petter, A.J., Radujkovic, B.M. (1989). Parasites des poissons marins du Montenegro: Nématodes. Acta Adriatica. 30:195-236. Poulin, R., Rohde, K. (1997). Comparing the richness of metazoan ectoparasite communities of marine fishes, controlling for host phylogeny. Oecologia, 110,278-283.
Price, PW., Clancy, KM. (1983). Patterns in number of helminth parasite species in freshwater Fishes. Journal of Parasitology 69, 449-454.
Ramdane, Z., Trilles, JP., Mahe, K., Amara, R. (2013). Metazoan ectoparasites of two teleost fish, Boops boops (L.) and Mullus barbatus (L.) from Algerian coast, diversity, parasitological index and impact of parasitism. Cybium 37, 5966.
Rima, M., Marzoug, D., Pérez-del-Olmo, A., Kostadinova, A., Bouderbala, M., Georgieva, S. (2017). New molecular and morphological data for opecoelid digeneans in two Mediterranean sparid fishes with descriptions of Macvicaria gibsoni n. sp. and M. crassigula (Linton, 1910) (sensu stricto). Systematic Parasitology 94, 739-763.
Sey, O., (1970). Parasitic helminthes occurring in Adriatic fishes (Nematodes, Acanthocephala). Acta Adriatica 13 (3), 1-16.
Sorbe, JC. (1977). Régime alimentaire de Phycis blennoides (Brunnich, 1768) dans le sud du golfe de Gascogne. Revue des Travaux de l'Institut de Pêche Maritime 41(3), 271-281.
Ternengo, S., Levron, C., Mouillot, D., Marchand, B. (2009). Site influence in parasite distribution from fishes of the Bonifacio Strait Marine Reserve (Corsica Island, Mediterranean Sea). Parasitology Research 104(6),1279- 1287. Valero, A., Paniagua, MI., Hierro, I., Diaz, V., Valderrama, MJ., Benitez, R., Adroher, FJ. (2005). Anisakid parasites of two forkbeards (Phycis blennoides and Phycis phycis) from the Mediterranean coasts of Andalucia (Southern Spain). Parasitology International 55 (5), 1-5.
Citation:
Hassani, M.M., Kerfouf, A., Baaloudj, A., Denis, F. (2020). Deep see fishes Phycis blennoides (Brunnich, 1768) and Phycis phycis (Linne, 1758) parasite diversity. Ukrainian Journal of Ecology, 10(4), 86-92.
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