The present analysis of the time scale changes in helminth communities in N. coriiceps demonstrates that community patterns almost did not change during the six-year term, although the climate variables differed. Analysis of meteorological data in the UAS water area revealed a slight but significant increase in water and air temperature and a decrease in water salinity, which is consistent with the results of long-term observations in various regions of West Antarctica (Vaughan et al. 2003; Turner et al. 2014; Gutt et al. 2015). However, the range of these changes was apparently insufficient to significantly impact the helminth community patterns. Most community patterns showed a stable trend, and the observed changes look like fluctuations close to the steady trend; however, some changes appeared to be statistically significant. The differences in the species compositions of communities are very slight. On the other hand, the essential differences in community patterns were caused by the differences in prevalence and intensity of N. coriiceps infection by separate helminth species.
The direct comparison of prevalence and intensity of the helminth taxonomic categories between the samples collected in 2014 and 2020 showed that nine of these categories significantly changed the infection parameters during the six years between them (see Table 1). Six species (Pseudoterranova sp., Contracaecum sp., A. nototheniae, monolocular metacestodes, bilocular metacestodes, Metacanthocephalus rennicki) and Diphyllobothrium sp. were also found to have a significant impact on the differences between helminth infracommunities in 2014 and 2020. Not all of those taxonomical categories were classified in the 'common' cluster (see Fig. 4). Namely, A. nototheniae and monolocular metacestode are in a 'rare' category cluster; the status of bilocular metacestodes and Contracaecum sp. is unstable. It can be interpreted that the changes are not significant because they did not affect the majority of the 'core' species in the community.
Three taxonomic categories, the acanthocephalan M. rennicki, bilocular metacestodes and the nematode Pseudoterranova sp., are central nodes for species associations (Fig. 2), indicating their essential role in the formation of the community patterns. In the two latter species, the infection intensity increased significantly during six years between the samples, while both infection prevalence and intensity decreased in M. rennicki. In our opinion, these changes may indicate the trend in changes in the helminth community of the studied N. coriiceps population. Further studies on the transmission peculiarities of the species in the marine ecosystem near Galindez Island may reveal the exact reasons for such changes. A similar increase in infection parameters of larval helminths in N. coriiceps and Parachaenichthys charcoti were reported previously from the same area (Kuzmina et al. 2020, 2021a, b, 2022 b, c) as well as in other Antarctic fish species (Rokicki et al. 2009; Kuhn et al. 2018; Muñoz and Cartes 2020); while in other cases, researchers observed a decrease in the abundance of larval stages of acanthocephalans or some ascaroid nematodes (Laskowski et al. 2012; Rokicki et al. 2009). Presumably, increasing infection rates of various fishes with helminth larvae are caused by the increase in the abundance and density of populations of their definitive hosts, which are marine mammals and fish-eating birds in Antarctica.
Associations between helminth taxonomical categories revealed in our study using the copula graphical model, in our opinion, are related to the biology and routes of transmission of these individual parasite species. Besides, we propose that two acanthocephalan species with the strongest associations, M. rennicki (MREN) and M. johnstoni (MJOH) (see Fig. 2), may represent one species. Metacanthocephalus johnstoni was separated from M. rennicki by Zdzitowiecki mainly using qualitative characteristics such as more extended proboscis and proboscis receptacle, longer embryophores, the position of nerve ganglions and large dimensions of mature females (Zdzitowiecki 1983); we saw on many worms that all these morphological characters can be variable. Therefore, molecular studies of fresh specimens are needed to elucidate whether these two species' names are synonyms. The high intensity of associations of the trematodes G. bowersi (GBOW) and E. oatesi (EOAT) is undoubtedly due to the similarity of their transmission routes using the same species of intermediate and/or paratenic hosts (Rocka 2006; Faltynkova et al. 2017, 2022). Presumably, the high intensity of association between trematodes and bilocular metacestodes is also related to their transmission using the same intermediate/paratenic hosts (Rocka 2017).
Three taxonomically distant helminth species, the nematode Pseudoterranova sp. (PSEU), cestode Diphyllobothrium sp. (DIPH) and acanthocephalans Corynosoma spp. (CORY), have the same definitive hosts of these helminths – Antarctic seals (Rocka 2004, 2006, 2017; Laskowski and Zdzitowiecki 2017). For polymorphid acanthocephalans (Order Polymorphida) such as Corynosoma spp., crustaceans of the order Amphipoda are known as intermediate hosts in Antarctic waters (Hoberg 1986; Zdzitowiecki 2001; Zdzitowiecki and Presler 2001). Intermediate hosts of diphyllobothriid cestodes and anisakid nematodes in Antarctic waters remain unknown (Rocka 2003, 2017). We suppose that the solid associations of these helminth species revealed in our study may indicate that the same species of Amphipoda serve as the intermediate hosts for all these helminths which promotes simultaneous fish infection. An increase in the populations of Weddell seals, Leptonychotes weddellii, and other pinnipeds observed in the waters of Galindez Island in recent decades (Dykyy and Peklo 2012) increased helminth infection of teleost fishes with these helminths (Kuzmina et al. 2022b).
The negative association between the acanthocephalan Metacanthocephalus rennicki (MREN) and bilocular metacestodes (MBIL) may indicate a mutual competitive relationship. However, direct competition is hardly possible in the two species with different niches in the host (site of infection). Presumably, factors other than direct competition might cause a negative association between these species. Investigation of those factors may be the subject of a separate study.
The positive correlation between fish size and intensity of infection found in our study is somewhat expected and is reasonable as bigger fish provide a more resource-rich ecological niche for helminths (Rocka 2006, 2017; Klimpel et al. 2017). Also, it was documented for different Antarctic fish species in previous research (Hoogester and White 1981; Palm et al. 1998; Zdzitowiecki and Laskowski 2004; Münster et al. 2017; Muñoz and Rebolledo 2018; Muñoz and Cartes 2020; Kuzmina et al. 2020; Alt et al. 2022) that bigger individuals, which are usually older than smaller ones, accumulate a larger number of larval stages of helminths compared to smaller specimens.
Thus, the results of our study show that despite the presence of small but significant changes in the climatic factors (mean air and water temperature and water salinity) between 2014 and 2020, these factors did not directly affect the infection patterns in N. coriiceps’ helminth community in West Antarctica over such a short period. On the other hand, we believe that the changes in infection patterns observed in the present study may be associated with the influence of biotic factors that affect the helminths’ transmission such as changes in the populations of intermediate, paratenic and definitive hosts of helminths (marine invertebrates, mammals and birds) in Antarctic ecosystems.