Knowledge of marine fish trematodes of Atlantic and Eastern Pacific Oceans

A brief summary of the early history of the study of Atlantic Ocean marine fish digeneans is followed by a discussion of the occurrence and distribution of these worms in the Atlantic Ocean and adjacent Eastern Pacific Ocean, using the Provinces of the ‘Marine Ecoregions’ delimited by Spalding et al. (Bioscience 57:573–583, 2007). The discussion is based on a database of 9,880 records of 1,274 species in 430 genera and 45 families. 8,633 of these records are from the Atlantic Ocean, including 1,125 species in 384 genera and 45 families. About 1,000 species are endemic to the Atlantic Ocean Basin. The most species-rich families in the Atlantic Ocean are the Opecoelidae Ozaki, 1925, Hemiuridae Looss, 1899 and Bucephalidae Poche, 1907, and the most wide-spread the Opecoelidae, Hemiuridae, Acanthocolpidae Lühe, 1906, Lepocreadiidae Odhner, 1905 and Lecithasteridae Odhner, 1905. A total of 109 species are shared by the Atlantic Ocean and the Eastern Pacific, made up of cosmopolitan, circum-boreal, trans-Panama Isthmus and Magellanic species. The lack of genetic evaluation of identifications is emphasised and the scope for much more work is stressed.

The study of the marine digenean fauna in the South Atlantic developed later. The first report in our database from the southwestern Atlantic is that of Monorcheides popovicii Szidat, 1950 from off Tierra del Fuego (Szidat, 1950) and those from the southeastern Atlantic are six monorchiids from off the coast of Ghana (Thomas, 1959).

Database and methods
A database in the form of an Excel spreadsheet has been developed for the marine fish trematodes of the Atlantic Ocean. This is based predominantly on the work of one of us (THC) and his students, who have used the literature to write over 25,000 lines. The Atlantic and Eastern Pacific Ocean records from this database have been extracted and some further records have been added (by RAB and PED). The locality records have been coded according to Provinces of the 'Marine Ecoregions' delimited by Spalding et al. (2007) (see Table 1, Fig. 1A). These are 'Large areas defined by the presence of distinct biotas that have at least some cohesion over evolutionary time frames' (Spalding et al., 2007). Eastern Pacific Ocean Provinces are included for comparative purposes. The 'Magellanic Province' spans both Oceans as it includes the North Patagonian Gulfs, the Patagonian Shelf, the Falklands, the Channels and Fjords of Southern Chile and Chiloense. Overall data included in the survey include this Province in the discussion of the Atlantic fauna. The database suffers from the problems inherent in this type of enterprise, such as errors in entry, duplicates, omissions, typos (both in original reports and data entry), wrong attributions and unrecognised synonymies. Another problem is the lack of precision in the locality descriptions in many papers. These records have been omitted. Also omitted from the main analysis have been records of parasites and/or fishes which have not been identified to species. It has not been possible to consider the validity and synonymies of all the species, but in general the names follow that used in the World Register of Marine Species (WoRMS Editorial Board, 2015), compiled mainly by Dr David Gibson, and the series of 'Keys to the Trematoda' (Gibson et al., 2002;Jones et al., 2005;Bray et al., 2008).

Results
Considering the number of records accumulated, it might be considered that we know a good proportion of the fauna, but the effort in different parts of the Ocean has certainly not been even.
The following data relating to the 17 regions of the Atlantic Ocean have been collated, along with the five Eastern Pacific regions: the number of species, genera and families in each region, the number of lines in the database per species, genus and family. These latter three parameters give an estimate of the effort in each region ( Table 2). The number of lines in the database for each region is displayed on the Map (Fig. 1B). As can be seen, the Tropical Northwest Atlantic (12) has the most described species, followed by the Mediterranean Sea (4). In terms of lines per taxon, the Northern European Seas Province (2) is the most studied region, but the Arctic (1), Mediterranean Sea (4) and possibly the Cold Temperate Northwest Atlantic (5) and the Tropical Northwest Atlantic (12), have very similar levels of effort. The effort in the southwestern Atlantic (13, 14, 47, 48) is considerably less and no records were recovered from the North Brazilian Shelf Province (13). The best known fauna from this region is Warm Temperate Southwestern Atlantic (47). The south-eastern Atlantic (16, 17, 50) is the least studied continental coastal zone (with only two records recovered from the Benguela region -50). The two mid-Southern Atlantic Island provinces (15 and 49) have only one record each.
The database has in total 9,880 records of 1,274 species in 430 genera and 45 families, of which 8,633 are from the Atlantic Ocean, with 1,125 species in 384 genera and 45 families. About 1,000 species are endemic to the Atlantic Ocean basin, but Lessepsian migrants and other identifications of Indo-West Pacific species confuse the picture.
A major problem with interpretation of the database in this fashion is that it is reliant on accurate identifications. In addition, little effort has been made, hitherto, to explore the genetic validity of Atlantic species. Relatively recent works by, for example, Jousson (Jousson et al., 1999(Jousson et al., , 2000Jousson, 2001), Blasco-Costa (Blasco-Costa et al., 2009a, b, 2010, Antar (Antar et al., 2015) in the Mediterranean and Curran, Pulis and Andres Pulis et al., 2014) in the Gulf of Mexico, are the exception. In the wider Atlantic the study of some deep-sea species of Lepidapedon Stafford, 1904 and other lepidapedids and fellodistomids (Lumb et al., 1993;Bray et al., 1994Bray et al., , 1999 has shown that cryptic species are common. New investigations should, wherever possible, include molecular evidence for the status of taxa.

The status of digenean families in the Atlantic Ocean
The number of genera and species found in the families in the Atlantic Ocean are listed in Table 3, the distribution of records of the families in the Atlantic Ocean are listed in Table 4, and the distribution of reports of the three most species-rich families are illustrated in Figures 2-4. The most species-rich, and jointly the most widespread, family is the Opecoelidae Ozaki, 1925 (Fig. 2), which is found in 13 of the 17 Atlantic regions. Considering that four of the zones are more or less completely unstudied, this presumably means that they are found in all zones. The second most species-rich family, the Hemiuridae Looss, 1899 has a very similar distribution pattern (Fig. 3). The third most species-rich family, the Bucephalidae, is found in fewer zones (11) than three less species-rich families (Fig. 4, Table 3). It is notable that the number of genera in the Bucephalidae Poche, 1907 is relatively few, but molecular results indicate that most of the currently recognised genera are polyphyletic (Nolan et al., 2015). Apart from the four more or less unstudied regions mentioned above (13, 15, 49 and 50), records of bucephalids are missing from the Magellanic (48) and the Tropical Southwestern Atlantic (14) regions. These are also poorly studied regions, and it is likely that bucephalids are, in fact, found in all regions.
The Atlantic is depauperate in some families that are relatively common in the Indo-West Pacific Region: the Gyliauchenidae Fukui, 1929, Enenteridae Yamaguti, 1958, Opistholebetidae Fukui, 1929 aguti, 1939. These data emphasize again the paucity of work in some regions. The Lepidapedidae Yamaguti, 1958 is mainly a deep-sea family and the lack of deep-sea studies in the southern part of the Atlantic in particular is highlighted by its occurrence in only eight zones. On the other hand, the paucity of records of microphallids, echinostomatids and brachycladiids probably reflects the real situation. Microphallids are rarely found in fishes, but they do occur there occasionally (Siddiqi & Cable, 1960) and the occurrence of a brachycladiid in a shark is likely to be an accidental occurrence, although it was found in its usual site, the liver (Adams et al., 1998). The record of the ovigerous echinostomatid Himasthla tensa Linton, 1940 in the Atlantic cod Gadus morhua L. must also be considered an accidental infection (Linton, 1940).

The Atlantic Ocean and the Eastern Pacific Ocean
According to our database 109 species are shared between the Atlantic Ocean and the Eastern Pacific region. These can be divided into four categories.
Thirteen species are circum-boreal, probably with a continuous population between the oceans via the Arctic Ocean (Table 5).
The remaining species reported in both the Atlantic Ocean and the Eastern Pacific Ocean is Tubulovesicula lindbergi (Layman, 1930) Yamaguti, 1934, originally reported from Peter the Great Bay off Northeastern Russia (Layman, 1930), and well reported in both the western and the eastern North Pacific. The two reports from the Atlantic, from off Puerto Rico (Siddiqi & Cable, 1960) and Ghana (Fischthal & Thomas, 1972), are puzzling and probably represent misidentifications. This situation also illustrates the problems encountered in studies based on large databases, where it is not possible to verify every record.

Lessepsian migration
The effect of man on the distribution of marine digeneans is exemplified by the effects of migration through the Suez Canal, so-called Lessepsian migration. We can be confident that this is changing the fauna, but to what extent it is not yet clear. For example, the herbivorous rabbit fish Siganus rivulatus Forsskål & Niebuhr has passed into the Mediterranean Sea, causing great damage to native algal assemblages (Sala et al., 2011), and bringing with it the wide-spread Indo-Pacific parasite Thulinia microrchis (Yamaguti, 1934) Bray, Cribb & Barker, 1993(as Hysterolecitha sigani Manter, 1969) (see Fischthal, 1980;Bray et al., 1993). Also, recently, the cornetfish Fistularia commersonii Rüppell has spread right across the Mediterranean Sea along with its parasite Allolepidapedon fistulariae Yamaguti, 1940 (and other worms) (Pais et al., 2007). It is not yet known if these Lessepsian migrant parasites have spread into the open Atlantic Ocean. With the opening in August 2015 of a new channel parallel to the old one, the exchange of fauna between the Red and Mediterranean Seas is bound to increase (Galil et al., 2015).

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Ethical approval This article does not contain any studies with animals performed by any of the authors.
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