Contracaecum osculatum (Rudolphi, 1802) Baylis, 1920

Mattiucci, Simonetta, Cipriani, Paolo, Paoletti, Michela, Nardi, Valentina, Santoro, Mario, Bellisario, Bruno & Nascetti, Giuseppe, 2015, Temporal stability of parasite distribution and genetic variability values of Contracaecum osculatum sp. D and C. osculatum sp. E (Nematoda: Anisakidae) from fish of the Ross Sea (Antarctica), International Journal for Parasitology: Parasites and Wildlife 4 (3), pp. 356-367 : 363-364

4.2. Ecological data on C. osculatum sp. D and C. osculatum sp. E

The results here presented confirm the presence of the two Antarctic species of anisakid nematodes of the genus Contracaecum (Raillet and Henry, 1912) , [ C. osculatum sp. D and C. osculatum sp. E ( Orecchia et al., 1994)] as the most prevalent anisakid species recovered from the fish hosts captured in the Ross Sea. The two species were found in the same individual fish hosts, showing a strict simpatry and sintopy. However, a significant difference in their relative proportions in the fish species was observed. This finding could be related to the ecological and feeding habits of the fish host species. The fish species examined in the present study show trophic niche separation ( Brenner et al., 2001), as demonstrated also by a study using stable carbon (C) and nitrogen (N) isotope analyses. Indeed, species of the fish genus Trematomus were differentiated in both C and N isotopic signature ( Rutschmann et al., 2011), indicating respectively a different habitat use and a distinct trophic level. T. bernacchii is the most benthic species of the genus Trematomus ( La Mesa et al., 2004) ; it has been also defined as a shallow benthic species, primarily feeding on benthic prey ( Gon and Heemstra, 1990). Therefore, T. bernacchii is considered as a generalist species, which relies on a wide range of preys that are more or less associated with the sea bottom ( La Mesa et al., 2004). On fish from the Ross Sea area, La Mesa et al. (2004) reported that bivalves were the main food of T. bernacchii , followed by polychaetes, and amphipods ( Fig. 2 ). Our result showed that in T. bernacchii the species C. osculatum sp. E prevailed over C. osculatum sp. D, which was rarely seen in that fish species ( Tables 3 and 4). Further, we found that small sized T. bernacchii (<25 cm) seems to be scarcely infected by Contracaecum larvae (authors personal observation). Another benthic notothenioid, T. hansoni , showed similar low infestation levels as observed in T. bernacchii ( Table 3), but it had a preponderance of C. osculatum sp. D (65.0% in 1993 ‾ 1994 sample, and 70.2% in 2011 ‾ 2012 sample; Table 4, Fig. 2 ). The observed difference in the relative proportions of the two species of Contracaecum spp. could be explained by a different feeding behaviour and feeding habits of these two fish species ( Fig. 2 ).

T. hansoni , despite sharing the benthic life style of T. bernacchii , includes more pelagic items in its diet ( Eastman and Sidell, 2002). La Mesa et al., 1997, report that stomach contents of T. hansoni specimens collected in Terra Nova Bay (Ross Sea) showed a mainly piscivorous (mainly juveniles) diet, with fish eggs as secondary food items, and on several benthic organisms as polychaetes and decapods ( La Mesa et al., 1997). Its food spectrum thus mainly comprises benthic organisms that are more or less associated with the substratum ( La Mesa et al., 1997).

T. newnesi is considered part of cryopelagic community organism ( Andriashev, 1970), and it's often associated with the under surface of the ice. The species can be defined as a frequent plankton feeder in the water column and as an occasional benthic feeder on the substratum (reviewed in Barrera-Oro, 2002); its diet in fact includes both Euphausiacea and more benthic Amphipoda, Isopoda, Polychaeta and some Mollusca ( Daniels, 1982). A marked plasticity in feeding habits and diet diversity of T. newnesi has been found in areas of seasonal sea-ice coverage in the high Antarctic zone ( La Mesa et al., 2000) ( Fig. 2 ). Both C. osculatum species showed high prevalence of infection in T. newnesi , with almost all the examined fish infested ( Table 3), and showing mean intensity (Im) values that were higher in T. newnesi than in the other notothenoids ( Table 2). T. newnesi , with its intermediate characteristics and its peculiar cryopelagic habit, feeding both in the water column on krill, and on substratum benthic organisms (Amphipoda, Polychaeta, and Isopoda), showed a balanced mixed infection with the two Contracaecum species (48.4% C. osculatum sp. D and 51.6% C. osculatum sp. E, Table 4), feeding on both intermediate hosts for the two Contracaecum species ( Fig. 2 ). In a study based on the stable isotope method to investigate trophic niches of Antarctic fishes, Cherel et al., 2011 reports that the intermediate d 13 C value of T. newnesi is in agreement with the semipelagic life style of the species ( Gon and Heemstra, 1990).

Whereas, Ch. hamatus , with a low d 13 C signature, confirms its epibenthic life style, feeding mainly on pelagic prey ( Gon and Heemstra, 1990). The infestation levels by both C. osculatum species in the channichtyid Ch. hamatus were remarkably higher than the levels recorded in the notothenioid fish species ( Table 3, Fig. 2 ). A 100% prevalence (P) was recorded in samples from both Antarctic expeditions for the Contracaecum larvae of the two species, being present in all the examined Ch. hamatus specimens, and showing extremely high mean intensity values (A = 135.8 for C. osculatum sp. D and A = 25.9 for C. osculatum sp. E recorded in 2011/2012, and A = 102.0 for C. osculatum sp. D and A = 17.6 for C. osculatum sp. E recorded in 1993 ‾ 1994) ( Table 3). The subsample of Contracaecum spp. larvae obtained from Ch. hamatus genetically identified showed a prominent presence of C. osculatum sp. D (83.0% recorded in the subsample of 1993 ‾ 1994, and 84.0% on 2011 ‾ 2012) ( Table 4). Piscivorous fish, such as many larger channichtyds, obviously play an important role as parathenic accumulators of Contracaecum s.l. larvae (Kloser ¨et al., 1992). In the Ross Sea, Ch. hamatus is the most abundant and eurybathic channichtyid ( Eastman and Hubold, 1999; Vacchi et al., 1999), with benthic behaviour, but also capable of vertical migration to feed on pelagic prey ( Eastman and Sidell, 2002). Mintenbeck et al., 2012, defines Chionodraco spp. as demersal fish that only occasionally move in the water column. The large predatory icefish probably show a heavier helminth burden compared with the Trematomus spp. because they are likely more exposed to infection through predation on multiple intermediate hosts, such as invertebrates and smaller fish (see La Mesa et al., 2004).

Thus, considering the relative frequencies observed of the two species of Contracaecum occurring in the different fish hosts, each one characterized by its feeding ecology and diets, some conclusion can be drawn regarding the possible life cycles of C. osculatum sp. D and C. osculatum sp. E in the Antarctic food web ( Fig. 3a and b , respectively). C. osculatum sp. D seems to be associated more with fishes, such as Ch. hamatus and T. hansoni , characterized by benthopelagic habits, and predating on other small fishes and Antarctic krill (presumably Euphausia crystallorophias , the most frequent euphausiid present in the Ross sea). C. osculatum sp. D could include, in its life-cycle, a planktonic intermediate host, such as Euphausia crystallorophias ( Fig. 3a ). Instead, C. osculatum sp. E showed its higher relative proportion in T. bernacchii , which is a fish specialized in predation of strictly benthic organisms. This finding seems to suggest that a possible first intermediate host of C. osculatum sp. E could be represented by benthic organisms ( Fig. 3b ).

Figures

Fig. 2. Schematic distribution of the fish species examined in the present study for larval of C. osculatum sp. D and C. osculatum sp. E, along the continental shelf of the Ross Sea coastal ecosystem. Arrows indicating preferred preys and the diet preference for each fish species are reported according to the literature (La Mesa et al., 2004). The represented pelagic organisms comprise species of euphausiids and fish juveniles, benthic and epibenthic organisms are polychaetes, amphipods, decapods and gastropods. A pie chart with the relative proportions of C. osculatum sp. D and C. osculatum sp. E is given for each fish species. Squares and circles represent the hypothetical distribution of C. osculatum sp. D and C. osculatum sp. E larvae in their intermediate hosts.

Fig. 3. Schematic representation of the hypothetic life-cycle of C. osculatum sp. D (a) and C. osculatum sp. E (b) in the Ross Sea.