REVIEW ARTICLE


A Review of the Parasites of Deep-Water Fishes from Macaronesian Islands, North-East Atlantic Ocean



Graça Costa1, *, Luísa Costa2, Maria João Santos3, 4, E. Melo-Moreira1
1 Estação de Biologia Marinha do Funchal, Universidade da Madeira, Promenade Orla Marítima do Funchal, 9000-107 Funchal, Portugal
2 Estação de Biologia Marinha do Funchal, Departamento de Ciência da Câmara Municipal do Funchal, Funchal, Portugal
3 Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre 4169-007 Porto, Portugal
4 CIMAR/CIIMAR Centro Interdisciplinar de Investigação Marinha e Ambiental, Av. General Norton de Matos s/n 4450-208 Matosinhos, Portugal


© 2018 Costa et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: https://creativecommons.org/licenses/by/4.0/legalcode. This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

* Address correspondence to the author at the Estação de Biologia Marinha do Funchal, Universidade da Madeira, Promenade Orla Marítima do Funchal, 9000-107 Funchal, Portugal; E-mail: gcosta@uma.pt


Abstract

The deep-water fish fauna of Macaronesian islands is currently estimated at a total of 1029 different fish species, but records of both ecto- and endoparasites are from only about 30 of those species. This fact presents an exciting field of research for scientists interested in fish parasitology, by exploring the structure of parasite communities and their connections with ecological and oceanographic variables. Research on the effect of climatic changes on the parasite faunas, on the occurrence of fish parasites in man and its impact on human health, has not been carried out to date. The present review aims to collate our present knowledge about the parasites of deep-water fishes of Macaronesia, and to suggest directions for future research on the parasites of fishes from the deepwater realm. A checklist of the parasites infecting the deep-water fishes from this region is included.

Keywords: Deep-water fishes, Parasites, Madeira, Azores, Canary Islands, Macaronesian region.



1. INTRODUCTION

The deep-sea habitat encompasses the ocean regions below 200m depth, with temperatures around 40C, subjected to high pressures, low nutrient concentrations and poor or no sunlight. Thus, deep-water fishes are living in low productivity environments in comparison with the epipelagic fishes [1, 2]. Two regions can be identified in this zone: the mesopelagic (200-1000m) and the bathypelagic (1000-4000m) [3]. Of the 33,200 fish species described, it is estimated that 10-15% are inhabitants of the deep-sea [4]. In the North Atlantic alone, 593 fish species are inhabitants of the deep-water habitat [5]. In the Macaronesian region, which includes the island archipelagos of Azores, Madeira, Canary and Cape Verde, the number of deep-water fish species, according to the FishBase database, amounts to 193 fish species in Azores archipelago, 288 in Canary archipelago, 254 in Cape Verde and 294 in Madeira archipelago [4]. Nevertheless, in spite of the richness of species inhabiting this region, only a few are commercially exploited and thus readily available for biodiversity studies. For example, the black scabbard fishes, Aphanopus carbo Lowe, 1839 and A. intermedius Parin, 1983, which have been commercially exploited for some years in Madeira, were subjected to several studies including parasites, growth performance and fisheries management [6-11]. The need to adapt fishing gear to the conditions of the deep-water habitat has been a limiting condition for the exploitation of this ocean region. Overexploitation of the epipelagic fish resources has accelerated interest in the deep-water resources in recent years [5, 12, 13]. Many of the biotic surveys conducted in the deep sea were based on fish captured in the North-west Atlantic, and the northern North-east Atlantic (latitudes above 43oN), which did not include the Macaronesian island archipelagos although a good number of papers did include parasite surveys in Madeira and Azores Archipelagos [8, 9, 14-18]. Madeira archipelago is the richest in species, with about 49.6% of the species registered for the North Atlantic, closely followed by the Canary Archipelago with 48.6% of species. This highlights the importance of the deep-water fishing resources for the fisheries economy of these archipelagos. Notwithstanding this high number of fish species, information on the occurrence of parasites and other biological aspects of deep-water fishes is currently restricted to only 31 fish species, the commercially exploited ones and some other species of no commercial value collected during scientific deep-water fish surveys [16, 19]. Some of the deep-water fish species currently been commercially exploited, in particular from the Azores, Madeira and Canary archipelagos, are: A. carbo, Beryx splendens Lowe, 1834, Centrophorus squamosus Bonnaterre, 1788, Conger conger Linnaeus, 1758, Dalatias licha Bonnaterre, 1788, Epigonus telescopus Risso, 1810, Etmopterus spinax Linnaeus, 1758, Helicolenus dactylopterus Delaroche, 1809, Lepidopus caudatus Euphrasen, 1788, Mora moro Risso, 1810, Pagellus bogaraveo Brünnich, 1768, Polyprion americanus Bloch & Schneider, 1801 [11, 20, 21]. Surveys of the parasites occurring in deep-water fishes from other regions of the North Atlantic have been published [15, 16, 19, 22-27], although due to the inherent difficulties of fishing in deep-waters, which limits the exploitation of fish resources, parasites of deep-water fishes are less known in comparison with parasites of epipelagic and demersal fishes [16]. More papers are being published on the parasites of deep-water fishes in recent years due to the improvement of technical gear for the exploration of deeper waters [25, 27-31], so that the number of parasites infecting deep-water fishes is now estimated at 671 named species or higher taxa, with digeneans being the dominant group of parasites, followed by cestodes, in particular from the orders Trypanorhyncha, Tetraphyllidea and Triaenophoridae [16, 29, 32]. The present work aims at producing an up-to-date review of the diversity of parasites found in the exploited deep-water fishes of Macaronesia, their geographic distribution, transmission and food-web dynamics, as well as their role as indicators of fish population structure and climatic change, and their zoonotic potential. In particular, due to the present climatic change, which facilitates invasion of species from tropical areas [33, 34], it is important to update checklists of parasites and hosts. The importance of parasites as potential human health threats is also discussed [35-37]. Due to the lack of knowledge of the parasites infecting deep-water fishes from Macaronesian islands, it is strongly recommended that researchers engage themselves in basic scientific projects, targeting the study of the parasite diversity in fish species from this realm. This would lead to the description of many parasite species new to science, as well as to better understanding the biology and the feeding habits of the fish, based on the occurrence of the parasites.

2. DIVERSITY OF PARASITES OF DEEP-WATER FISHES

Although the deep-sea is known as a nutrient poor habitat, with low or no light, which suggests that fishes in this habitat should have depauperate parasite faunas [24, 38-40], a number of parasites belonging to many phyla have been reported from deep-water fishes [16]. In the Macaronesian region, myxosporeans belonging to the genus Ceratomyxa (2 species) and Parvicapsula (1 species) were found in the gall bladders of A. carbo and B. splendens [6, 17, 41, 42]. Haematozoans, of the genus Haemohormidium (Apicomplexa) were found in erythrocytes of Coryphaenoides armatus Hector, 1875 caught at Cape Verde [19]. Although blood smears of 11 deep-water fish species - Alepisaurus ferox Lowe, 1833, Bathypterois grallator Goode & Bean, 1886, Bathysaurus mollis Günther, 1878, Borostomias elucens Brauer, 1906, Chauliodus sloanei Bloch & Schneider, 1801, Conocara salmoneum Gill & Townsend, 1897, C. armatus, Coryphaenoides profundicolus Nybelin, 1957, Histiobranchus bathybius Günther, 1877, and Sigmops elongatus Günther, 1878- were examined, no further haematozoans were found [19]. Monogeneans are represented by at least 5 species, mostly specific to their respective hosts (Table 1). Among the digeneans, lepocreadioids include groups of worms which are common in deep-sea fishes, from the subfamily Lepidapedinae, although members of the subfamily Lepocreadiinae have been found in deep-water fish (e.g. Prodistomum priedei Bray & Merrett, 1998) [28, 31, 43-46]. Hemiuridae, in particular Lecithochirium species, are common in deep-water fish. A total of 18 different digenean taxa were found infecting deep-water fishes from Macaronesia (Table 1).

Table 1. Protozoan and metazoan parasites infecting the deep-water fishes from Macaronesian region, North-east Atlantic.
Parasite Taxon Host
Aphanopus carbo Alepsisaurus ferox Beryx splendens Cataetyx laticeps Centrophorus squamosus Centroscymnus coelolepis Centroscyllium fabricii Centroscymnus cryptacanthus Ceratoscopelus maderensis Coelorinchus karrerae Conger conger Coryphaenoides armatus Coryphaenoides nasutus Dalatias licha Deania calcea D. hystricosa D. profundorum Etmopterus princeps E. pusillus E. spinax Halosauropsis macrochir Helicolenus dactylopterus Heptranchias prelo Lepidopus caudatus Maurolicus muelleri Myctophum punctatum Pagellus bogaraveo Poromitra crassiceps Polyprion americanus Scopelogadus beanii References
Apicomplexa
Haemohormidium sp. Y [19]
Microsporidia
Glugea capverdensis Lom, Gaevskaya & Dykova 1980 Y [103, 104]
Pleistophora duodecimae Lom, Gaevskaya & Dykova 1980 Y [103, 104]
Myxozoa
Ceratomyxa maxima Gaevskaya & Kovaljova, 1980 Y [41]
Ceratomyxa tenuispora Kabata, 1960 Y [6, 42]
Parvicapsula schulmani Kovaljova & Gaevskaya, 1981 Y [105]
Monogenea
Calicobenedenia polyprioni Kritsky & Fennessy, 1999 Y [106]
Lamellodiscus virgula Euzet & Oliver, 1967 Y [57]
Octoplectanocotyla aphanopi Pascoe, 1987 Y [17, 107]
Paradiplectanotrema lepidopi Gerasev, Gaevskaja & Kovaleva, 1987 Y [15]
Digenea
Accacladocoelium petasiporum Odhner, 1928 Y [52]
Adinosoma gaevskaye Zubchenko, 1978 Y [108]
Botulus microporus (Monticelli, 1889) Y [109] personal obs.
Brachyphallus crenatus (Rudolphi, 1802) Y [15]
Degeneria halosauri (Bell, 1887) Campbell, 1977 Y [25]
Derogenes varicus (Muller, 1784) Y [52]
Diphterostomum vividum (Nicoll, 1912) Bray & Gibson, 1986 Y [52, 67]
Gaevskajatrema halosauropsi Bray & Campbell, 1996 Y [25]
Gonocerca phycidis Manter, 1925 [15]
Lecithocladium excisum (Rudolphi, 1819) Lühe, 1901 Y [15]
Lecithochirium furcolabiatum (Jones, 1933) Dawes, 1947 Y [54]
Lecithochirium grandiporum (= L. fusiforme Lühe, 1901) (Rudolphi, 1819) Lühe, 1901 Y [52, 54]
Lecithochirium musculus (Looss, 1907) Nasir & Diaz, 1971 Y Y [17, 54]
Odhnerium sp. Yamaguti, 1934 Y [49]
Pachycreadium carnosum (Rudolphi, 1819) Cortini & Ferretti, 1959 Y [52]
Pycnadenoides senegalensis Fischthal & Thomas, 1972 Y [52]
Steringophorus sp. Odhner, 1905 Y [25]
Cestoda
Aporhynchus sp. Nybelin, 1918 Y Y [40]
Aporhynchus menezesi Noever, Caira, Kuchta & Desjardins, 2010 Y [40, 110]
Aporhynchus norvegicus (Olsson, 1868) Y [40]
Aporhynchus tasmaniensis Beveridge, 1990 Y [111]
Aporhynchus pickeringae Noever, Caira, Kuchta & Desjardins, 2010 Y [40, 110]
Bilocularia hyperapolytica Obersteiner, 1914 Y [40]
Campbelliella heteropoeciloacantha Palm, 2004 Y [17]
Clistobothrium carcharodoni Dailey & Vogelbein, 1990 Y [40]
Clistobothrium montaukensis Ruhnke, 1993 Y Y Y [40]
Crossobothrium dohrnii
(Oerley, 1885) Ruhnke, 1996
Y [47]
Crossobothrium
sp. Linton, 1889
Y [47, 111]
Deanicola
sp. Beveridge, 1990
Y Y [40]
Heteronybelinia yamagutii
(Dollfus, 1960)
Y [8, 17]
Bathygrillotia kovalevae (Palm, 1995) Beveridge & Campbell, 2012 (=Grillotia kovalevae Palm, 1995) Y [53]
Grillotia acanthoscolex
Rees, 1944 (= Grillotia microthrix Dollfus, 1969)
Y [47]
Grillotia meteori Palm & Schröder, 2001 Y [47]
Grillotia
sp. Guiart, 1927
Y Y [40, 48]
Gilquinia
sp. Guiart, 1927
Y Y Y [18, 40]
Monorygma
Diesing, 1863
Y [40]
Nybelinia lingualis
Cuvier, 1817
Y Y [6, 15, 17]
Nybelinia thyrsites
Korotaeva, 1971
Y [17]
Pelichnibothrium speciosum Monticelli, 1889 Y [112], personal obs.
Plesiorhynchus brayi
Palm, 2004
Y [40]
Tentacularia coryphaenae
Bosc, 1802
Y Y Y [6,
17, 18, 47]
Scolex pleuronectis Müller,1788 Y Y [25,
40], personal obs.
Heterosphyriocephalus tergestinus
(
Pintner, 1913) Dallarés, Carrassón & Schaeffner, 2016 (= Sphyriocephalus tergestinus Pintner, 1913)
Y Y Y [6, 15, 54]
Tetraphyllidea Y Y Y [46, 52]
Triloculate Tetraphyllidea Y [18]
Acanthocephala
Bolbosoma vasculosum (
Rudolphi, 1819)
Y Y [7,
15]
Echinorhynchus
sp. Zoega
in Müller, 1776
Y [25]
Rhadinorhynchus pristis
(Rudolphi, 1802)
Y Y Y [15,
52, 54]
Nematoda
A. brevispiculata
Dollfus, 1966
Y [8]
A. nascettii Mattiucci,
Paoletti & Webb, 2009
Y [14]
A. pegreffii
Campana-Rouget & Biocca, 1955
Y Y Y [14, 46, 50, 51]
A. physeteris
(Baylis, 1923)
Y Y Y [8, 49, 51].
A. simplex
(Rudolphi, 1809)
Y Y Y Y Y Y Y [14, 15, 18, 46, 49, 51]
Anisakis sp.
Dujardin, 1845
Y Y Y Y Y [25, 46, 47]
A. typica (Diesing, 1860) Baylis, 1920 Y [51]
A. ziphidarum Paggi,
Nascettii, Webb, Mattiucci, Cianchi & Bullini, 1988
Y Y [14, 51]
Comephoronema macrochiri
Moravec & Klimpel, 2007
Y [25]
Contracaecum
Railliet & Henry, 1912
Y [51]
Cristitectus congeri
Petter, 1970
Y [54]
Hysterothylacium aduncum
(Rudolphi, 1802)
Y [15][
Hysterothylacium
sp. Ward & Magath, 1917
Y Y [25, 50, 51]
Pseudoterranova ceticola
Deardorff & Overstreet, 1981
Y [18]
Crustacea
Aega antillensis
(Schioedte & Meinert, 1879)
Y [56]
Aega deshaysiana
Milne Edwards, 1840
Y [56]
Anelasma
sp. Darwin, 1852
Y [113]
Argulus
sp. Muller, 1785
Y [56]
Caligus elongatus
von Nordmann, 1832
Y [15]
Gnathia
sp. Leach, 1814
Y [56]
Hatschekia pagellibogueravei
Hesse, 1878
Y [56]
Jusheyus shogunus
Deets & Benz, 1987
Y [114]
Rocinela danmoniensis
Leach, 1818
Y [56]
Tautochondria dolichoura
Ho, 1987
Y Y [46]

The majority of the cestodes infecting deep-water fishes appear to be larval stages belonging to the order Tetraphyllidea, and adults of the order Trypanorhyncha. Larval trypanorynchs were also found in some deep-water sharks [18, 40, 47, 48]. Acanthocephala are poorly represented in the deep-water habitat, with only 3 species found to date [7, 17, 49]. In contrast, nematodes of the genus Anisakis were found in many of the fish examined, sometimes reaching high prevalences (up to 100%) and intensities of infection [8, 17, 50-52]. Finally, 9 species of Crustacea were found, which, with the exception of one, were generalist parasites. Summarizing, to date 1 haematozoan, 2 microsporidians, 3 myxozoans, 5 monogeneans, 17 digenean, 28 cestodes, 3 acanthocephalans, 12 nematodes and 9 crustaceans, have been found in the 30 different deep-water fishes from the Macaronesian region. Although the parasite fauna of deep-water squaliform sharks appears to be depauperate in comparison to the parasite fauna of deep-water carcharhiniforms [18, 40, 53], it would be worthwhile to conduct more research, including surveys of more host species, to understand better the dynamics of parasite transmission in the deep sea.

3. TRANSMISSION, FOOD-WEB DYNAMICS AND GEOGRAPHIC DISTRIBUTION OF PARASITES

The study of the occurrence of parasites in a particular fish species can give clues about the feeding ecology of the fish, and consequently about the food-web transmission of the parasites. In this respect a survey of parasites of the conger eel, C. conger, from Madeira Archipelago, found that some parasites were more abundant in deeper waters. For example the postlarvae of the trypanorhynch Sphyriocephalus tergestinus Pintner, 1913 and the hemiurid digenean Lecithochirium grandiporum (L. fusiforme Lühe, 1901) (Rudolphi, 1819) Lühe, 1901, occurred in waters below 400m deep, whereas the digenean L. musculus (Looss, 1907) Nasir & Diaz, 1971, was present in conger eels only at depths of 200-300m [54]. In the mesobathyal region, fish and crustaceans are the preferential prey, thus explaining the presence of S. tergestinus in deeper waters. Another study, that examined the parasite diversity of seven different meso- and bathypelagic fish species, from the Mid-Atlantic Ridge (MAR), found significant differences in prevalence with helminth parasites, which were correlated with the feeding habits of the fish hosts [46]. High prevalence with anisakids, in myctophid fishes, was correlated with feeding predominantly on euphausiids and on copepods, common intermediate hosts in the complex life cycle of these parasites. High prevalence with anisakids was also observed in A. carbo from Madeira waters [8, 17] due to feeding on prey items, which act as intermediate and paratenic hosts in the life cycle of the nematodes. Likewise the diversity of parasites infecting the silver scabbard fish, L. caudatus agreed well with its diet on copepods and euphausiids transmitting anisakid nematodes, amphipods transmitting acanthocephalans, and chaetognaths acting as intermediate hosts for hemiurid digeneans [15]. Larval stages of cestodes, of the orders Trypanorhyncha and Tetraphyllidae, were transmitted to the black scabbard fish, by feeding on cephalopods and crustaceans, as well as on mesopelagic fishes [6, 17]. In the deep water realm trypanorhynchs of the families Aporhynchidae, Gilquinidae and larval tetraphyllideans are the most common cestodes infecting fishes and sharks [18, 40, 47, 48]. Nevertheless, trypanorhynchs of the families Tentaculariidae and Sphyriocephalidae, common parasites of epipelagic and mesopelagic fishes, were additionally found in the black-scabbard fish and the conger eel [9, 17, 54]. This reflects the feeding behaviour of the fish hosts, which undergo extensive vertical migrations [11, 54]. Ecological factors such as diet, depth range, temperature, and host behaviour are important as driving forces shaping the community structure of parasites. One other factor in the shaping of parasite communities is the life cycle of the parasite, which is inherently connected to diet. Trypanorhynchs and tetraphyllidean cestodes mature in sharks, many of them deep-water sharks [40, 47, 53]. This explains why these parasites are common in deep-water fishes (28 taxa, Table 1). On the other hand acanthocephalans, many of which mature in whales, were rare in deep-waters. The majority of the digeneans, cestodes and acanthocephalans found in deep-water fishes from the Macaronesia were generalists, with complex life cycles. In contrast, monogeneans and crustaceans, which tend be host specific have less complex life cycles. The relatively few (5) monogenean species and crustacean parasites (10) found in deep-water fishes from Macaronesia may be explained by the fact that, been ectoparasites, they are more vulnerable to being lost or damaged due to fishing procedures, and does not necessarily reflect poor diversity of these parasite groups.

It is believed that mesopelagic and bathypelagic fishes have more impoverished parasite communities than benthic fishes [24, 55]. If we take the parasites of the bathypelagic fish A. carbo as an example, the total number of parasite species found to date is 14 [7-9, 14, 17], whereas the parasite richness of the benthopelagic P. bogaraveo is represented by 22 parasite species [51, 52, 56]. Only 2 parasites infecting A. carbo are specialists, the remaining being generalists infecting a wide range of fish species, not all of them typical of deep-waters only, occurring also in mesopelagic zones. Among the parasites of P. bogaraveo, 3 are specialists and the remaining 19 are generalists. In very dilute environments, as is the case of oceanic islands, the generalist parasite mode of life is preferred as a survival strategy in these nutrient poor environments [55, 57]. Some parasites have a wide geographical distribution, whereas others are restricted to particular zones. Hosts that undergo extensive migrations, vertical and horizontal ones, concur to spread the parasites in wider geographic patterns. The anisakids, A. simplex (s.s.) (Rudolphi, 1809) and A. pegreffii Campana-Rouget & Biocca, 1955, are common in the entire Atlantic Ocean and Mediterranean Sea, the first one also present in the Pacific Ocean, with mainly benthic, demersal and bathypelagic life cycle [14, 58, 59]. Their definitive hosts, whales of the families Physeteridae and Ziphiidae, are present in the Macaronesian deep-water realm [60, 61]. Likewise the geographic distribution of tapeworm parasites infecting deep-water sharks, are a product of the host wide distribution and their trophic levels [62, 63]. Nevertheless the infection rate of deep-water sharks was low in comparison with infection rates of epi-pelagic sharks. For example, 57% of sharks examined in the Condor Seamount, Azores Archipelago, were not infected with cestodes [40]. This finding agrees with results from other researchers elsewhere, advocating that the parasite fauna of deep-water organisms is impoverished [40, 53].

4. ROLE OF PARASITES AS INDICATORS OF ENVIRONMENTAL HEALTH, CLIMATE CHANGE AND FISH POPULATION STRUCTURE

Parasites are important key elements to assess the quality of the water environment, the effects of climate changes, and population structure of fish [64-66]. Santos et al. [17] highlighted the role parasites play in the differentiation of stocks of A. carbo from different regions in the North Atlantic. The hemiurid digenean, L. musculus was only present in the Azores fish samples, and postlarvae of the trypanorhynchs Campbelliella heteropoeciloacantha Palm, 2004, Heteronybelinia sp. Palm 1999, Nybelinia thyrsites Korotaeva, 1971, and Tentacularia coryphaenae Bosc, 1802, only present in Madeiran fish samples. The conclusions of this study suggested the existence of three different stocks of black-scabbard fish, one in mainland Portugal (at Sesimbra), one in Madeiran waters and the third one in the Azores waters. Sequeira et al. [49] used parasites, in particular anisakid nematodes, for discrimination of populations of the bluemouth, H. dactylopterus. Differences were found in the occurrence of anisakid parasite species, with A. pegreffii as main species in the fish samples from mainland Portugal, an unidentified Anisakis species in Madeiran samples, and A. physeteris (Baylis, 1923) in the Azores samples. Another study of the helminth parasites infecting the black-spot seabream, P. bogaraveo from Madeira, Azores and mainland Portugal suggested the presence of different populations in the study areas [52, 67]. The conclusions were mainly based on the presence of hemiurid digeneans in mainland Portuguese Atlantic waters, and their absence in samples collected in the Azores and Madeira archipelagos. The higher diversity of digeneans in mainland Portugal was correlated with high diversity of benthic invertebrates, intermediate hosts for the digeneans, whereas in the island ecosystems, nutrient poorer waters supported an impoverished benthic invertebrate fauna and consequently a poor digenean fauna. Additionally, anisakid nematodes played a fundamental role as indicators of fish population structure, with A. physeteris dominant in the Azores samples, an unidentified Anisakis sp. in Madeira, and A. pegreffii in mainland Portugal [51, 67]. The impact of climatic changes, particularly rising water temperatures, is expected to critically affect the distribution of meso and epi-pelagic fishes and consequently their parasite faunas [68, 69]. In addition, rising surface water temperatures will allow tropical fish species to extend their distribution range further north, carrying with them new parasites which will thus be introduced and may evolve and complete their life cycles [33, 34, 70]. Since many parasites are not host specific, and can use both pelagic and deep-water fishes as paratenic hosts, it is expected that new colonization events by parasite species will be experienced in the near future. What will be the impact of these parasites in their new hosts, in terms of their pathogenicity and their competitive fitness, is something to ponder [69, 71]. New fish species arriving from tropical waters, which have already been reported in Madeira, include the monacanthids Aluterus scriptus Osbeck, 1765 and A. monoceros Linnaeus, 1758 [72], the goldspot goby Gnatholepis thompsoni Jordan, 1904 [73] and the carangid Caranx crysos Mitchill, 1815 [74]. Wirtz et al. [74] suggested that rising water temperatures were the trigger for the occurrence or the increase in frequency of species typical of warmer waters. These new arrivals can facilitate the introduction and transmission of new parasites in this marine habitat. Many parasites are generalists and those coming with these new fish species will probably spread to local fish species, seeking to establish themselves and conquer new life cycle pathways [55]. Although the impact of climatic changes on the biodiversity of the deep sea, have not been addressed with much detail, a few studies done in other deep-water ocean regions, have indeed demonstrated that, the effect of climatic changes on the biodiversity of this sea realm can not be neglected [75-78]. Studies of the effect of climatic changes in parasite diversity of deep-water species in Macaronesia have not been done yet. However, there are well documented baseline studies of parasites in some deep-water fishes, such as A. carbo and P. bogaraveo [14, 17, 51, 52, 56, 79], so follow-up surveys can be done in order to detect new parasites or parasite extinctions with time.

5. IMPORTANCE OF PARASITES FOR HUMAN HEALTH AND THEIR IMPACT ON FISH QUALITY

Larval anisakid nematodes (L3 stages) are parasites of a wide range of fish species, both pelagic and deep-water, with worldwide distribution, and can lead to inflammation of the gastrointestinal tract of man, following consumption of raw or poorly cooked fish [35, 80-82]. Major clinic symptoms are vomiting and epigastric pain [36, 83-86]. Reports of human infections with anisakid nematodes have been increasing in the last 30 years, probably because of more awareness and cooperation between parasitologists and medical professionals, with quite a number of papers published, including case studies and state of the art reviews [37, 86-90]. Not all anisakid species have exactly the same ability to infect humans and therefore to be of zoonotic potential. From the 9 known species of Anisakis infecting fish and squids, the only Anisakis species cited as occurring in man are A. simplex (s.s.) and A. pegreffii, both belonging to the complex of species called Anisakis simplex (s.l.) [89]. However, a recent comparative study of the behaviour of both species showed that A. simplex (s.s.) supports better the gastric juices, and migrates faster to the fish muscle, when the fish died, than A. pegreffii [90]. This suggests that it is very important to know what anisakid species is infecting fish used for consumption, and see if the parasites belong to A. simplex (s.s.) species, the most dangerous group, or to other potentially less dangerous species. In Europe, several cases of human infections due to A. pegreffii have been reported [89, 91]. According to several authors, nematodes with zoonotic potential include not only the two species, A. pegreffii and A. simplex (s.s.), but in addition A. physeteris and Pseudoterranova decipiens (Krabbe, 1878) Gibson, 1983 [36, 91-97]. Anisakid nematodes are common parasites of several fish species in the Macaronesian region, including deep-water species (e.g.A. carbo, B. splendens, P. bogaraveo) (Table 1) [6, 8, 14, 49-51]. In some fish species, A. simplex (s.s.) was the most frequent nematode species [8, 14, 51], whereas in others A. pegreffii was the most frequent. Many studies which dealt with the occurrence of anisakids in fishes did not include the identification of the species, a procedure that involves the use of molecular tools. Specific identification of species was done for some fish species from the Madeira Archipelago [8, 14, 50, 51], although only for a sub-sample of the anisakids found. The work of Hermida et al. [51, 52] was also an important study on the occurrence of anisakids in P. bogaraveo from mainland Portugal, the Azores and Madeira archipelagos. This fish is host to a number of anisakid species, including the two species of zoonotic potential. A study of the distribution of anisakids in the viscera and musculature of forty black-scabbard fish, A. carbo, concluded that larvae were mainly located in the viscera, but some were found in the belly flaps region, beginning the process of penetrating into the muscle [98]. This highlights the potential danger of keeping fish with viscera after capture. One good measure to prevent migration of larvae from the visceral cavity to the muscles is to proceed with evisceration of fish on board, immediately after capture, a procedure that is taken place in many fishing vessels, whenever conditions permit such procedure. This action however, increases the risk of enhancing prevalence and abundance of parasite larvae in small pelagic fishes, such as mackerels and sardines, due to “anthropogenic short-cut” as discussed by Mattiucci and co-authors [89]. Evisceration on board would provide easy food to dolphins and whales (which are abundant in Macaronesian islands) [60, 61], the definitive hosts of anisakids. In the intestines of these marine mammals, parasites attain maturity and new release of infective larvae to pelagic fishes, such as mackerels and sardines, will be the outcome. Heavily infected mackerels, as well as other small pelagic fishes, will in turn be food for man. Ingestion of infected fish by man, not only presents the danger of gastroenteritis due to attachment of larvae on the stomach mucosa, but in addition, ingestion of infected fish can lead to allergic reactions in man [85, 97, 99-101]. In contrast to fish, sharks were apparently less susceptible to infections with anisakids, or perhaps due to the physiologic conditions of their digestive tract as gastric digestion leads to a semi-liquid chime, as a result of complete breakdown of the ingested prey, parasites were not detected [102]. In a survey of 69 leafscale gulper shark, C. squamosus, only 9 nematodes were recovered, 7 of them were A. simplex, one was Pseudoterranova ceticola Deardorff & Overstreet, 1981, and another one an unidentified anisakid [18]. In the black-scabbard fish, A. carbo, prevalence of Anisakis spp. can reach 100% [8, 14, 17]. High prevalence was also found in the blackspot seabream, P. bogaraveo [51] in Madeira Archipelago. In contrast to the research and data on the zoonotic potential of anisakids in Continental European and Mediterranean countries, there are no data about human infections in the Macaronesian region. The absence of reported cases of anisakiasis in this region can be due to the fact that fish is mainly consumed well cooked. One other reason could be that human cases of anisakiasis have been overlooked by medical professionals.

CONCLUSION

We strongly recommend a better collaboration between fish parasitologists and medical professionals, in order to assess with greater accuracy, the causes of many allergic reactions in man. As the consumption of fish is very popular in this region, the potential for human infections due to Anisakis larvae thus exists.

CONSENT FOR PUBLICATION

Not applicable.

CONFLICT OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

The present review was accomplished with financial support from the ISOPlexis laboratory, University of Madeira, Funchal, Portugal, and with funds allocated to the Animal Pathology Laboratory of CIIMAR, Porto, Portugal. We are indebted to Dr. Ken MacKenzie (University of Aberdeen, Scotland) for reading and improving the English spelling.

REFERENCES

[1] Haedrich RL. Deep-water fishes: Evolution and adaptation in the earth’s largest living spaces. J Fish Biol 1996; 49: 40-53.
[2] Merrett NR, Haedrich RL. Deep-sea demersal fish and fisheries 1997; 282.
[3] Castro P, Huber ME. Marine Biology 1997; 450.
[4] Froese R, Pauly D. Fish Base 2016. Available from: http://www.fishbase.org
[5] Bergstad OA. North Atlantic demersal deep-water fish distribution and biology: Present knowledge and challenges for the future. J Fish Biol 2013; 83(6): 1489-507.
[6] Costa G, Eiras JC, Chubb J, MacKenzie K, Berland B. Parasites of the black scabbard fish, Aphanopus carbo Lowe, 1839 from Madeira. Bull Eur Assoc Fish Pathol 1996; 16: 13-5.
[7] Costa G, Chubb JC, Veltkamp CJ. Cystacanths of Bolbosoma vasculosum in the black scabbard fish Aphanopus carbo, oceanic horse mackerel Trachurus picturatus and common dolphin Delphinus delphis from Madeira, Portugal. J Helminthol 2000; 74(2): 113-20.
[8] Costa G, Pontes T, Mattiucci S, D’Amélio S. The occurrence and infection dynamics of Anisakis larvae in the black-scabbard fish, Aphanopus carbo, chub mackerel, Scomber japonicus, and oceanic horse mackerel, Trachurus picturatus from Madeira, Portugal. J Helminthol 2003; 77(2): 163-6.
[9] Costa G, Veltkamp CJ, Chubb JC. Larval trypanorhynchs (Platyhelminthes: Fucestoda: Trypanorhyncha) from black-scabbard fish, Aphanopus carbo and oceanic horse mackerel, Trachurus picturatus in Madeira (Portugal). Parasite 2003; 10(4): 325-31.
[10] Morales-Nin B, Sena-Carvalho D. Age and growth of the black scabbard fish Aphanopus carbo off Madeira. Fish Res 1996; 25: 239-51.
[11] Farias I, Morales-Nin B, Lorance P, Figueiredo I. Black scabbard fish, Aphanopus carbo in the northeast Atlantic: Distribution and hypothetical migratory cycle. Aquat Liv Res 2013; 26: 333-42.
[12] Gordon JDM, Bergstad OA, Figueiredo I, Menezes G. Deep-water fisheries of the Northeast Atlantic: I. Description and current trends. J Northwest Atl Fish Sci 2003; 31: 137-50.
[13] Bergstad OA, Menezes GMM, Høires ÅS, Gordon JDM, Galbraith JK. Patterns of distribution of deepwater demersal fishes of the North Atlantic mid-ocean ridge, continental slopes, islands and seamounts. Deep Sea Res Part I Oceanogr Res Pap 2012; 61: 74-83.
[14] Pontes T, D’Amelio S, Costa G, Paggi L. Molecular characterization of larval anisakid nematodes from marine fishes of Madeira by a PCR-based approach, with evidence for a new species. J Parasitol 2005; 91(6): 1430-4.
[15] Klimpel S, Rückert S, Piatkowski U, Palm HW, Hanel R. Diet and metazoan parasites of silver scabbard fish Lepidopus caudatus from the Great Meteor Seamount (North Atlantic). Mar Ecol Prog Ser 2006; 315: 249-57.
[16] Klimpel S, Busch MW, Kellermanns E, Kleinertz S, Palm HW. Metazoan Deep-Sea Fish Parasites. Acta Biologica Benrodis Supplementband II. Solingen, Germany: Verlag Natur & Wissenschaft 2009, 384.
[17] Santos MJ, Saraiva A, Cruz C, et al. Use of parasites as biological tags in stock identification of the black scabbard fish, Aphanopus carbo Lowe, 1839 (Osteichthyes: Trichiuridae) from Portuguese waters. Sci Mar 2009; 73(S2): 55-62.
[18] Costa G, Chada T, Melo-Moreira E, Cavallero S, D’Amelio S. Endohelminth parasites of the leafscale gulper shark, Centrophorus squamosus (Bonnaterre, 1788) (Squaliformes: Centrophoridae) off Madeira Archipelago. Acta Parasitol 2014; 59(2): 316-22.
[19] Davies AJ, Hosein S, Merrett NR. Haematozoans from deep water fishes trawled off the Cape Verde Islands and over the Porcupine Seabight, with a revision of species within the genus Desseria (Adeleorina: Haemogregarinidae). Folia Parasitol (Praha) 2012; 59(1): 1-11.
[20] Uiblein F, Bordes F, Castillo R. Diversity, abundance and depth distribution of demersal deep-water fishes off Lanzarote and Fuerteventura, Canary Islands. J Fish Biol 1996; 49: 75-90.
[21] Vieira AR, Figueiredo I, Figueiredo C, Menezes GM. Age and growth of two deep-water fish species in the Azores Archipelago: Mora moro (Risso, 1810) and Epigonus telescopus (Risso, 1810). Deep Sea Res Part II: Topical Studies in Oceanography 2013; 98 (Part A): 148-59.
[22] Noble ER, Orias JD. Parasitism in the bathypelagic fish, Melanostigma pammelas. Int J Parasitol 1975; 5(1): 89-93.
[23] Orias JD, Noble ER, Alderson GD. Parasitism in some east Atlantic bathypelagic fishes with a description of Lecithophyllum irelandeum sp. n. (Trematoda). J Parasitol 1978; 64(1): 49-51.
[24] Campbell RA, Haedrich RI, Munroe TA. Parasitism and ecological relationships among deep-sea benthic fishes. Mar Biol 1980; 57: 301-13.
[25] Klimpel S, Palm HW, Busch MW, Kellermans E. Fish parasites in the bathyal zone: The halosaur Halosauropsis macrochir (Günther, 1878) from the Mid-Atlantic Ridge. Deep Sea Res Part II Top Stud Oceanogr 2008; 55: 229-35.
[26] Palm HW, Klimpel S. Metazoan fish parasites of Macrourus berglax Lacepède, 1801 and other macrourids of the North Atlantic: Invasion of the deep sea from the continental shelf. Deep Sea Res Part II Top Stud Oceanogr 2008; 55: 236-42.
[27] Isbert W, Montero FE, Carrassón M, González-Solís D. Dichelyne (Cucullanellus) romani n. sp. (Nematoda: Cucullanidae) in notacanthid fishes from the Northeast Atlantic and Western Mediterranean. Syst Parasitol 2015; 91(1): 35-47.
[28] Bray RA. The bathymetric distribution of the digenean parasites of deep-sea fishes. Folia Parasitol (Praha) 2004; 51(2-3): 268-74.
[29] Kuchta R, Scholz T. Bathycestus brayi n. gen. and n. sp. (Cestoda: Pseudophyllidea) from the deep-sea fish Notacanthus bonaparte in the northeastern Atlantic. J Parasitol 2004; 90(2): 316-21.
[30] Bray RA, Kuchta R. Digeneans from deep-sea marine teleosts off the Outer Hebrides, Scotland, including the description of Brachyenteron helicoleni sp. nov. (Zoogonidae). Acta Parasitol 2006; 51: 169-75.
[31] Bray RA, Waeschenbach A, Cribb TH, Weedall GD, Dyal P, Littlewood DTJ. The phylogeny of the Lepocreadioidea (Platyhelminthes, Digenea) inferred from nuclear and mitochondrial genes: Implications for their systematics and evolution. Acta Parasitol 2009; 54: 310-29.
[32] Kuchta R, Scholz T. Australicola pectinatus n. gen. and n. sp. (Cestoda: Pseudophyllidea) from the deep-sea fish Beryx splendens from Tasmania. J Parasitol 2006; 92(1): 126-9.
[33] Palm HW. Parasitism in some east Atlantic bathypelagic fishes with a description of Lecithophyllum irelandeum sp. n. (Trematoda). J Parasitol 1978; 64: 49-51.
[34] Poulin R, Townsend CR, Tompkins DM, Kelly DW, Paterson RA. Biological invasions and the dynamics of endemic diseases in freshwater ecosystems. Freshw Biol 2011; 56: 676-88.
[35] Audicana MT, Ansotegui IJ, de Corres LF, Kennedy MW. Anisakis simplex: Dangerous-dead and alive? Trends Parasitol 2002; 18(1): 20-5.
[36] Cavallero S, Ligas A, Bruschi F, D’Amelio S. Molecular identification of Anisakis spp. from fishes collected in the Tyrrhenian Sea (NW Mediterranean). Vet Parasitol 2012; 187(3-4): 563-6.
[37] Cipriani P, Acerra V, Bellisario B, et al. Larval migration of the zoonotic parasite Anisakis pegreffii (Nematoda: Anisakidae) in European anchovy, Engraulis encrasicolus: Implications to seafood safety. Food Control 2016; 59: 148-57.
[38] Campbell RA. Deep water parasites. Ann Parasitol Hum Comp 1990; 65(Suppl. 1): 65-8.
[39] Klimpel S, Palm HW, Seehagen A. Metazoan parasites and food composition of juvenile Etmopterus spinax (L., 1758) (Dalatiidae, Squaliformes) from the Norwegian Deep. Parasitol Res 2003; 89(4): 245-51.
[40] Caira JN, Pickering M. Cestodes from deep-water squaliform sharks in the Azores. Deep Sea Res Part II Top Stud Oceanogr 2013; 98: 170-7.
[41] Gaevskaya AV, Kovaleva AA. New species of giant myxosporidia from bathypelagic Atlantic fish. Zool Zhurnal 1980; 59: 942-4.
[42] Casal G, Costa G, Azevedo C. Ultrastructural description of Ceratomyxa tenuispora (Myxozoa), a parasite of the marine fish Aphanopus carbo (Trichiuridae), from the Atlantic coast of Madeira Island (Portugal). Folia Parasitol (Praha) 2007; 54(3): 165-71.
[43] Bray RA. Annotated checklist of digenean parasites of Macrouridae (Teleostei, Gadiformes). Acta Parasitol 1995; 40: 168-92.
[44] Bray RA, Gibson DI. The Lepocreadiidae (Digenea) of fishes from the north-east Atlantic: A review of the genus Lepidapedon Stafford, 1904. Syst Parasitol 1995; 31: 81-132.
[45] Bray RA, Merrett NR. Prodistomum priedei n. sp. (Digenea: Lepocreadiidae) from the deepwater cardinal fish Epigonus telescopus (Perciformes: Epigonidae) in the northern Atlantic Ocean. Syst Parasitol 1998; 41: 71-7.
[46] Klimpel S, Busch MW, Sutton T, Palm HW. Meso- and bathy-pelagic fish parasites at the Mid-Atlantic Ridge (MAR): Low host specificity and restricted parasite diversity. Deep Sea Res Part I Oceanogr Res Pap 2010; 57: 596-603.
[47] Palm HW, Schröder P. Cestode parasites from the elasmobranchs Heptranchias perlo and Deania from the Great Meteor Bank, central East Atlantic. Aquat Living Resour 2001; 14: 137-44.
[48] Costa G, Khadem M, Dellinger T, Biscoito M, Melo-Moreira E. Larval cestodes infecting the deep-water fish, Cataetyx laticeps (Pisces: Bythitidae) from Madeira Archipelago, Atlantic Ocean. Acta Parasitol 2016; 61(1): 187-90.
[49] Sequeira V, Gordo LS, Neves A, Paiva RB, Cabral HN, Marques JF. Macroparasites as biological tags for stock identification of the bluemouth, Helicolenus dactylopterus (Delaroche, 1809) in Portuguese waters. Fish Res 2010; 106: 321-8.
[50] Costa G, Madeira A, Pontes T, D’Amelio S. Anisakid nematodes of the blackspot seabream, Pagellus bogaraveo, from Madeira waters, Portugal. Acta Parasitol 2004; 49: 156-61.
[51] Hermida M, Mota R, Pacheco CC, et al. Infection levels and diversity of anisakid nematodes in blackspot seabream, Pagellus bogaraveo, from Portuguese waters. Parasitol Res 2012; 110(5): 1919-28.
[52] Hermida M, Cruz C, Saraiva A. Gastrointestinal helminth communities of the blackspot seabream Pagellus bogaraveo (Teleostei: Sparidae) from Portuguese north-east Atlantic waters. J Helminthol 2014; 88(2): 129-38.
[53] Palm HW. The Trypanorhyncha Diesing 1863; 710.
[54] Costa G, Santos MJ, Costa L, Biscoito M, de Carvalho MA, Melo-Moreira E. Helminth parasites from the stomach of conger eel, Conger conger, from Madeira Island, Atlantic Ocean. J Parasitol 2009; 95(4): 1013-5.
[55] Marcogliese DJ. Food webs and parasite transmission. Parasitology 2002; 124: S83-99.
[56] Hermida M, Cruz C, Saraiva A. Ectoparasites of the blackspot seabream Pagellus bogaraveo (Teleostei: Sparidae) from Portuguese waters of the north-east Atlantic. J Mar Biol Assoc U K 2012; 93: 503-10.
[57] Poulin R, Morand S. Parasite Biodiversity 2004; 216.
[58] Mattiucci S, Nascetti G, Clanchi R, et al. Genetic and ecological data on the Anisakis simplex complex, with evidence for a new species (Nematoda, Ascaridoidea, Anisakidae). J Parasitol 1997; 83(3): 401-16.
[59] Mattiucci S, Nascetti G. Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: An update. Parasite 2006; 13(2): 99-113.
[60] Jefferson TA, Leatherwood S, Webber MA. Marine Mammals of the World 1994; 320.
[61] Mathias ML. An annotated list of the mammals recorded from Madeira Island. Bol Mus Munic Funchal 1988; 40: 111-37.
[62] Cortés E. Standardized diet compositions and trophic levels of sharks. ICES J Mar Sci 1999; 56: 707-17.
[63] Compagno L, Dando M, Fowler S. A field guide to the sharks of the world 2005; 368.
[64] MacKenzie K, Williams HH, Williams B, McVicar AH, Siddall R. Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Adv Parasitol 1995; 35: 85-144.
[65] Marcogliese DJ. Parasites of the superorganism: Are they indicators of ecosystem health? Int J Parasitol 2005; 35(7): 705-16.
[66] MacKenzie K, Hemmingsen W. Parasites as biological tags in marine fisheries research: European Atlantic waters. Parasitology 2015; 142(1): 54-67.
[67] Hermida M, Cruz C, Saraiva A. Parasites as biological tags for stock identification of blackspot seabream, Pagellus bogaraveo (Telesotei: Sparidae) in Portuguese northeast Atlantic waters. Sci Mar 2013; 77: 607-15.
[68] Mouritsen KN, Poulin R. Parasitism, climate oscillations and the structure of natural communities. Oikos 2002; 97: 462-8.
[69] Lafferty KD. Calling for an ecological approach to studying climate change and infectious diseases. Ecology 2009; 90(4): 932-3.
[70] Goedknegt MA, Welsh JE, Drent J, Thieltges DW. Climate change and parasite transmission: How temperature affects parasite infectivity via predation on infective stages. Ecosphere 2015; 6(6): 1-9.
[71] Dunn AM, Hatcher MJ. Parasites and biological invasions: Parallels, interactions, and control. Trends Parasitol 2015; 31(5): 189-99.
[72] Freitas M, Biscoito M. First record of Aluterus scriptus and Aluterus monoceros (Pisces: Tetraodontiformes:Monacanthidae) from the archipelagos of Madeira and Selvagens (NE Atlantic). Bocagiana 2002; 206: 1-7.
[73] Araújo R, Freitas M. First record of the Goldspot goby Gnatholepis thompsoni Jordan 1904 (Pisces: Gobidae) in Madeira Island (NE Atlantic Ocean). Bocagiana 2002; 209: 1-4.
[74] Wirtz P, Fricke R, Biscoito MJ. The coastal fishes of Madeira Island- new records and an annotated check-list. Zootaxa 2008; 1715: 1-26.
[75] Marris E. Nature News 2004. Available from: https://www.nature.com/search?q=Marris+E.+Nature+News+2004
[76] Ruhl HA, Smith KL Jr. Shifts in deep-sea community structure linked to climate and food supply. Science 2004; 305(5683): 513-5.
[77] Brierley AS, Kingsford MJ. Impacts of climate change on marine organisms and ecosystems. Curr Biol 2009; 19(14): R602-14.
[78] Löhmus M, Björklund M. Climate change. What will it do to fish-parasite interactions? Biol J Linn Soc Lond 2015; 116: 397-411.
[79] Nadler SA, D’Amelio S, Dailey MD, Paggi L, Siu S, Sakanari JA. Molecular phylogenetics and diagnosis of Anisakis, Pseudoterranova, and Contracaecum from northern Pacific marine mammals. J Parasitol 2005; 91(6): 1413-29.
[80] Audicana MT, Kennedy MW. Anisakis simplex: From obscure infectious worm to inducer of immune hypersensitivity. Clin Microbiol Rev 2008; 21(2): 360-79.
[81] Kuhn T, Hailer F, Palm HW, Klimpel S. Global assessment of molecularly identified Anisakis Dujardin, 1845 (Nematoda: Anisakidae) in their teleost intermediate hosts. Folia Parasitol (Praha) 2013; 60(2): 123-34.
[82] Daschner A, Pascual CY. Anisakis simplex: Sensitization and clinical allergy. Curr Opin Allergy Clin Immunol 2005; 5(3): 281-5.
[83] Abattouy N, Valero A, Benajiba MH, Lozano J, Martín-Sánchez J. Anisakis simplex s.l. parasitization in mackerel (Scomber japonicus) caught in the North of Morocco-prevalence and analysis of risk factors. Int J Food Microbiol 2011; 150(2-3): 136-9.
[84] Daschner A, Rodero M, DE Frutos C, et al. Different serum cytokine levels in chronic vs. acute Anisakis simplex sensitization-associated urticaria. Parasite Immunol 2011; 33(6): 357-62.
[85] D’Amelio S, Cavallero S, Bussi M, et al. Anisakis.Molecular detection of human parasitic pathogens 2013; 485-97.
[86] Suzuki J, Murata R, Hosaka M, Araki J. Risk factors for human Anisakis infection and association between the geographic origins of Scomber japonicus and anisakid nematodes. Int J Food Microbiol 2010; 137(1): 88-93.
[87] Mattiucci S, D’Amelio S. Anisakiasis. In: Bruschi F, Ed. Helminth infections and their impact on global public health 2014; 325-65.
[88] Bao M, Pierce GJ, Pascual S, et al. Assessing the risk of an emerging zoonosis of worldwide concern: Anisakiasis. Sci Rep 2017; 7: 43699.
[89] Mattiucci S, Cipriani P, Paoletti M, Levsen A, Nascetti G. Reviewing biodiversity and epidemiological aspects of anisakid nematodes from the North-east Atlantic Ocean. J Helminthol 2017; 91(4): 422-39.
[90] Arizono N, Miura T, Yamada M, Tegoshi T, Onishi K. Human infection with Pseudoterranova azarasi roundworm. Emerg Infect Dis 2011; 17(3): 555-6.
[91] Mladineo I, Popović M, Drmić-Hofman I, Poljak V. A case report of Anisakis pegreffii (Nematoda, Anisakidae) identified from archival paraffin sections of a Croatian patient. BMC Infect Dis 2016; 16: 42.
[92] Asato R, Wakuda M, Sueyoshi T. A case of human infection with Anisakis physeteris larvae in Okinawa, Japan. Kisechugaku Zasshi 1991; 40: 181-3.
[93] D’Amelio S, Mathiopoulos KD, Brandonisio O, Lucarelli G, Doronzo F, Paggi L. Diagnosis of a case of gastric anisakidosis by PCR-based restriction fragment length polymorphism analysis. Parassitologia 1999; 41(4): 591-3.
[94] Umehara A, Kawakami Y, Araki J, Uchida A. Molecular identification of the etiological agent of the human anisakiasis in Japan. Parasitol Int 2007; 56(3): 211-5.
[95] Fumarola L, Monno R, Ierardi E, et al. Anisakis pegreffi etiological agent of gastric infections in two Italian women. Foodborne Pathog Dis 2009; 6(9): 1157-9.
[96] Mattiucci S, Paoletti M, Borrini F, et al. First molecular identification of the zoonotic parasite Anisakis pegreffii (Nematoda: Anisakidae) in a paraffin-embedded granuloma taken from a case of human intestinal anisakiasis in Italy. BMC Infect Dis 2011; 11: 82.
[97] Mattiucci S, Fazii P, De Rosa A, et al. Anisakiasis and gastroallergic reactions associated with Anisakis pegreffii infection, Italy. Emerg Infect Dis 2013; 19(3): 496-9.
[98] Silva MIF. Anisakis sp (Nematoda: Ascaridida: Anisakidae) do peixe-espada preto, Aphanopus carbo: Estudo morfológico dos estádios larvares L3, distribuição e seu efeito histopatológico no hospedeiro 2005; 50.
[99] Angot V, Brasseur P. Les larves d’anisakidés et leur incidence sur la qualité des poisons et produits de poisson. Rev MédVét 1995; 146: 791-804.
[100] Karl H, Levsen A. Occurrence and distribution of anisakid nematodes in Grey gurnard (Eutrigla gurnardus L.) from the North Sea. Food Control 2011; 22: 1634-8.
[101] Levsen A, Karl H. Anisakis simplex (s.l.) in Grey gurnard (Eutrigla gurnardus) from the North Sea: Food safety considerations in relation to fishing ground and distribution in the flesh. Food Control 2014; 36: 15-9.
[102] Leigh CS, Papastamatiou Y, German DP. The nutritional physiology of sharks. Rev Fish Biol Fish 2017; 27: 561-85.
[103] Lom J, Gayevskaya AV, Dyková I. Two microsporidian parasites found in marine fishes in the Atlantic Ocean. Folia Parasitol (Praha) 1980; 27(3): 197-202.
[104] Lom J. A catalogue of described genera and species of microsporidians parasitic in fish. Syst Parasitol 2002; 53(2): 81-99.
[105] Kovaleva A, Gaevskaya AV. On new findings of Myxosporidia of the genus Parvicapsula in the Atlantic fishes. Zool Zhurnal 1981; 60: 771-3.
[106] Kritsky DC, Fennessy CJ. Calicobenedenia Polyprioni n. gen., n. sp. (Monogenoidea: Capsalidae) from the external surfaces of wreckfish, Polyprion americanus (Teleostei: Polyprionidae), in the north Atlantic. J Parasitol 1999; 85(2): 192-5.
[107] Pascoe PL. Monogenean parasites of deep-sea fishes from the Rockall trough (N.E. Atlantic), including a new species. J Mar Biol Assoc U K 1987; 67: 603-22.
[108] Zubchenko AV. New species of trematodes from fishes in the North Atlantic. Parazitologia 1978; 12(2): 116-20.
[109] Gibson DI, Bray RA. The Azygiidae, Hirudinellidae, Ptychogonimidae, Sclerodistomidae and Syncoeliidae (Digenea) of fishes from the northeast Atlantic. Bull Br Mus Nat Hist Zool 1977; 32: 167-245.
[110] Noever C, Caira JN, Kuchta R, Desjardins L. Two new species of Aporhynchus (Cestoda: Trypanorhyncha) from deep water lanternsharks (Squaliformes: Etmopteridae) in the Azores, Portugal. J Parasitol 2010; 96(6): 1176-84.
[111] Palm HW, Waeschenbach A, Olson PD, Littlewood DTJ. Molecular phylogeny and evolution of the Trypanorhyncha Diesing, 1863 (Platyhelminthes: Cestoda). Mol Phylogenet Evol 2009; 52(2): 351-67.
[112] Scholz T, Euzet L, Moravec F. Taxonomic status of Pelichnibothrium speciosum Monticelli, 1889 (Cestoda: Tetraphyllidea), a mysterious parasite of Alepisaurus ferox Lowe (Teleostei: Alepisauridae) and Prionace glauca (L.) (Euselachii: Carcharinidae). Syst Parasitol 1998; 41: 1-8.
[113] Yano K, Musick JA. The effect of the mesoparasitic barnacle Anelasma on the development of reproductive organs of deep-sea squaloid sharks, Centroscyllium and Etmopterus. Environ Biol Fishes 2000; 59: 329-39.
[114] Benz GW, Fennessy CJ, Vogelbein WK. New host and ocean records and remarks on the morphology and behavior of Jusheyus shogunus (Copepoda: Siphonostomatoida: Eudactylinidae. J Parasitol 1999; 85(5): 809-14.