Host records and geographical distribution of Corynosoma magdaleni, C. semerme and C. strumosum (Acanthocephala: Polymorphidae)

Abstract A literature survey was conducted to investigate the host and geographical distribution patterns of three Corynosoma species (Acanthocephala: Polymorphidae), viz. C. magdaleni, C. semerme and C. strumosum. All three species appear to be restricted to the Northern Hemisphere. Occurrence records of C. magdaleni are limited to the Northern Atlantic coasts, while C. semerme has a circumpolar distribution. The geographical range of Corynosoma strumosum encompasses the distributions of the other two species, but also extends into warmer southern regions. Some Corynosoma populations are living with their definitive hosts in very isolated locations, such as in the brackish Baltic Sea or different freshwater lakes (e.g. Lake Saimaa). All three species have a heteroxenous life cycle, comprising a peracaridan intermediate host, a fish paratenic host and a mammalian definitive host. Occasionally, an acanthocephalan may enter an accidental host, from which it is unable to complete its life cycle. The host records reported here are categorised by type, i.e. intermediate, paratenic, definitive or accidental. While most of the definitive hosts are shared amongst the three Corynosoma species, C. strumosum showed the broadest range of paratenic hosts, which reflects its more extensive geographical distribution. One aim of this study and extensive literature summary is to guide future sampling efforts and therewith contribute to throw more light on the on-going species and morphotype discussion for this interesting parasite species.


Introduction
The genus Corynosoma comprises 43 marine species (Amin 2013), that infect mammals and piscivorous birds. Aznar et al. (2006) showed that the original concept of Corynosoma was not a monophyletic genus. Phylogenetic analysis revealed that the marine Corynosoma species were more closely related to the genus Andracantha Schmidt, 1975 than to the species living in freshwater habitats. Aznar et al. (2006) erected the genus Pseudocorynosoma Aznar, Pérez-Ponce de León and Raga, 2006 for the freshwater species. Recent phylogenetic analysis based on ribosomal ITS1-5.8S-ITS2 and COI sequences showed that Corynosoma spp., hosted by Pinnipedia and marine Mustelidae formed a monophyletic group (Waindok et al. 2018).
The systematics of Corynosoma species from seals in northern Europe have recently been investigated using both molecular markers (Waindok et al. 2018) and morphology (Leidenberger et al. 2019). These studies have highlighted the limitations of using traditional morphological characters alone for diagnosing species. To determine the true species diversity in this genus, tandem morphological and molecular studies will be required. To guide future sampling efforts, we have conducted a comprehensive literature survey of the host and geographical distribution of three commonly encountered taxa: C. magdaleni Montreuil, 1958, C. semerme (Forssell, 1904 Lühe, 1911 and C. strumosum (Rudolphi, 1802) Lühe, 1904

Host and geographical records
Host and geographical records for the three acanthocephalan taxa were collected from literature. Manual searches were conducted using Pubmed, Web of Science and Google Scholar. Additionally, we used the R (R Core Team 2019) package helminthR (Dallas 2016) to extract records from the Host-Parasite Database of The Natural History Museum in London (Gibson et al. 2005). Geographical records for each Corynosoma species were summarised by MEOW ecoregions (Spalding et al. 2007) and then plotted as a distribution map using the meow R-package (Byrnes 2016).
In most of the Baltic Sea studies, C. semerme was the species most commonly found in seals, followed by C. magdaleni and only rare infections were found for C. strumosum (Nickol et al. 2002, Leidenberger and Bäcklin 2008, Waindok et al. 2018. Co-infections have been observed (Nickol et al. 2002, Leidenberger and Bäcklin 2008, Leidenberger et al. 2019, most commonly involving C. semerme and C. magdaleni , Leidenberger and Bäcklin 2008, Waindok et al. 2018. Interestingly, land-locked seal species show no mixed infections, but only single infections, for example, Phoca hispida saimensis in Lake Saimaa only by C. magdaleni  Geographical distribution of Corynosoma strumosum.  and Pusa caspica in the Caspian Sea only by C. strumosum (Amin et al. 2011). García-Varela et al. (2005) concluded that the Corynosoma species found in the Caspian Sea is C. caspicum and not C. strumosum. Indeed, C. strumosum from the land-locked Caspian seal recorded by Amin et al. 2011 was characterised with proboscis hooks and trunk spines distinct from other Northern European morphological descriptions (Nickol et al. 2002, Waindok et al. 2018, Leidenberger et al. 2019, suggesting that they may not be conspecific. Surprisingly, Corynosoma caspicum Golvan and Mokhayer, 1973, described based on immature specimens from sturgeons in Caspian Sea (Golvan and Mokhayer 1973) and often found in three-spined stickleback (Gasterosteus aculeatus) (Niksirat et al. 2006), has not yet been reported in Pusa caspica or another definitive host. Waindok et al. (2018) described some individuals of C. strumosum from the German North and Baltic Seas with different proboscis morphology, similar to those described by Amin et al. (2011) and stated this as C. magaleni isolate Pv1NS instead. Additionally, they found a cryptic species refered to as "Candidatus Corynosoma nortmeri sp. nov." ' Waindok et al. (2018) in the European study area.
The extent of the geographical and host ranges of the three taxa correlates with the year of their description. Corynosoma strumosum was the first species of the genus to be described (Rudolphi 1802) and has, by far, the broadest geographical and host distributions. Corynosoma semerme, described by Forssell (1904), appears to have a slightly more limited geographical range and far fewer paratenic host records. Relatively few hosts have been reported for C. magdaleni, described by Montreuil (1958) and its geographical range appears to be restricted to the northern Atlantic, in contrast to the circumpolar distributions of the other two species. Up until its description in 1958, specimens of C. magdaleni were almost certainly assigned to the morphologically similar C. strumosum. The potential bias resulting from taxon age should be kept in mind when comparing the reported host and geographical distributions of the three taxa (Fig. 3).

Overview of the life cycle
The heteroxenous life cycle of Corynosoma species involves a peracaridan intermediate host, a paratenic host (fish) and a mammalian definitive host. While there are numerous studies on C. semerme and C. strumosum (Tables 3,4,5,6,7,8), there have been few studies on C. magdaleni, besides its original description by Montreuil 1958 (Tables 1, 2). The intermediate host of C. magdaleni is unknown. Lake Saimaa may be a good location to search for the intermediate host of C. magdaleni, because the other Corynosoma species appear to be absent from this land-locked waterbody . A total of five species of paratenic host (all Actinopterygii) have been reported for C. magdaleni; three from Canada and two from the Baltic Sea (Table 1). In Canada, only C. magdaleni is reported together with C. wegeneri Heinze, 1934. In the definitive hosts (Table 2), the species seems to prefer the last part of the small intestine (ileum) and the colon. Corynosoma semerme has been reported from the whole intestine, but is typically found at a higher density in the large intestine, especially the cecum and rectum (Nickol et al. 2002, Leidenberger andBäcklin 2008), where C. strumosum and C. magdaleni are not generally observed. Microhabitat segregation might facilitate reproductive isolation of the three species, especially in mixed infections that are often observed in seals from the Baltic Sea (Nickol et al. 2002, Leidenberger and Bäcklin 2008, but less commonly in the North Sea (Waindok et al. 2018). While the three Corynosoma species share most of their definitive hosts, they show some differences in their paratenic hosts. We found that C. strumosum shares three paratenic hosts with both other species, none with C. magdaleni only, but > 20 paratenic hosts are shared with C. semerme. More than 80 paratenic hosts were described for C. strumosum and these are, up to now, not reported from any of the other two species (Tables 1, 4, 6).         (Brandt, 1851), which further confirmed amphipods as potential intermediate hosts.

Host order
Corynosoma strumosum seems to have fewer definitive hosts than C. semerme (Table 5), but the species shows also numerous reported paratenic hosts in Europe, North America, the Caspian Sea, Sea of Okhotsk and Northwest Pacific (Table 6), belonging to the classes Actinoptergyii and Petromyzonti. Even if the Corynosoma spp. are observed in many fish species, they are not able to become sexually mature in fish (Forssell 1905, Lundström 1942. This is the reason why fish may only play an important role as paratenic host. The definitive host of Corynosoma has fish as prey, but numerous fish-eating species become accidentally infected and become dead-end hosts (see Tables 7, 8 C. semerme and C. strumosum, respectively). While it is not known how long a life cycle of Corynosoma spp. takes, the development of the cystacanths to become mature helminths in seals is suggested to take 2-3 weeks (Helle and Valtonen 1981) and the season and/or temperature might have a strong effect on the sex-age structure of Corynosoma spp. Valtonen 1981, Popov andFortunato 1987). Aznar et al. (2006) characterised the marine Corynosoma clade as cosmopolitan and, in the past, the marine genus was able to adapt their complex life cycle to extreme environments like the brackish Baltic Sea, Lake Saimaa and the Caspian Sea. It is also postulated that the right intermediate and paratenic host is available and serves as a reservoir for the cystacanth. Marine glacial relict species serve or are supposed to serve as intermediate hosts for Corynosoma species in the Baltic Sea (e.g. the amphipod Monoporeia affinis (Lindström, 1855) and the isopod Saduria entomon (Linnaeus, 1758)). Lundström (1942) discussed the idea that the Corynosoma spp., like Echinorhynchus salmonis Müller, 1784, may be a marine glacial relict species, because these species are also found in the Arctic Sea, White Sea and numerous freshwater and relict lakes (e.g. Lake Saimaa, Lake Ladoga, Lake Onega).  mentioned, that the C. semerme cystacanths, observed in Baltic fish, differed clearly in the morphological characters (trunk length), while C. magdaleni and C. strumosum cystacanths were hard to separate ( C. strumosum only slightly larger than C. magdaleni). This is interesting, especially since also Waindok et al.
(2018) mentioned some difficulties with the identification of C. strumosum. Acanthocephalans from harbour seals of the North Sea were initially diagnosed as C. strumosum, based on morphological characters; however, molecular markers (COI and ITS) indicated that they should have been assigned to C. magdaleni.
Another study, Hernández-Orts et al. (2017), based on partial sequences of the mitochondrial cytochrome c oxidase 1 gene ( cox1), clearly segregated the Northern Hemisphere species (C. magdaleni and C. strumosum) and Southern Hemisphere species (C. hannae and C. australe Johnston, 1937). Corynosoma hannae from the Southern Hemisphere is most similar to C. semerme from the Northern Hemisphere, having no genital spines in females. It could be possible that parallel evolution may have evolved two similar complex parasitic Corynosoma systems in pinnipeds. It is still unresolved, whether the only report of C. semerme from the Southern Hemisphere by Johnston and Edmonds (1953) is C. hannae or not (discussed by Hernández-Orts et al. 2017).
Another possible assumption could be that the marine genus, Corynosoma, entered the Baltic Sea at the same time as their definitive hosts and this reflects their population history. The Baltic grey seal population is suggested to have diverged from the Eastern Atlantic/North Sea ones between 4,200 and 10,000 years ago (Fietz et al. 2016, Klimova et al. 2014, when the breeding habitats were shifted more easterly during the Baltic Sea formation. For the ringed seal, the allele frequency differentiation between the Baltic and Arctic populations were weak (Palo et al. 2001), while a northern invasion from continental seals during the Plio-Pleistocene to the basins was suggested to be most likely (Palo and Väinölä 2006). The ringed seal is the exclusive seal species in the land-locked Lake Saimaa, Finland. It also formed isolated populations in the Arctic and North-western Pacific (Popov and Fortunato 1987). The Caspian seal is another very isolated population and is supposed to be a relict species as well. Today, the ringed seal is very isolated in the Baltic Sea, as well as a small population of harbour seals (Härkönen et al. 2005).

Conclusion
Obviously, with the geographical isolation, Corynosoma species show plastic morphological characters and possible morphotypes (e.g. Fortunato 1987, Amin et al. 2011). Which role the intermediate and paratenic host play in the isolation is not known today. Sinisalo and Valtonen (1998) found an indication of segregation of C. magdaleni and C. strumosum in their paratenic hosts in the Gulf of Bothnia, Baltic Sea, Finland. In general, there is too little information available on the ecology and distribution of each of the Corynosoma spp. Future studies should try to combine genetic and new morphological tools (like SEM and the proboscis profiler) to throw more light on the ongoing species and morphotype discussion for Corynosoma spp. We see the greatest challenge is the access to good and sufficient material for further analyses. Our reported geographical distribution patterns (Suppl. material 1) and summary of definitive and paratenic hosts may contribute to and motivate further investigations on this interesting parasite group.
Corynosoma semerme and C. strumosum have extensive host and geographical ranges, providing opportunities for reproductive isolation of lineages. Speciation in acanthocephalans is often cryptic and Waindok et al. (2018) have already demonstrated the presence of a cryptic species, "Candidatus Corynosoma nortmeri," in the North Sea. Further work to investigate the species diversity in Corynosoma will require a tandem morphological and molecular study of acanthocephalans collected from all known hosts, throughout their geographical ranges. The present study should prove to be a useful guide for future sampling efforts.