Results and discussion

Only one fur seal was found with helminths present in the lungs (prevalence of 5%). The infected animal was a subadult female (total length = 101 cm) found dead on Cassino Beach (32°14′39.9″S, 53°22′02.6″W). It was in a highly emaciated condition. Internally, cervical lymph nodes were increased in size and were haemorrhagic. In the lungs, congestion and yellowish grapelike structures (diameter about 2 mm) corresponding to multiple cysts were seen. Each cyst was about 50 μm in diameter and was occupied by convoluted fine worms, predominantly by larger gravid females, with many larvae inside. The total number of females recovered was not precisely estimated precision due to the intense fragmentation of the worms’ bodies. Two males were recovered.

The identification of the species was based on the general morphological characteristics of the Parafilaroides genus, while specific identification was based on two fragmented males and three whole females. In the males, the shape and size of the spicules were verified, which were exactly the same as those described and represented by Dailey (Reference Dailey2009). Spicules were thin and minute, equal in size, and measuring 35 μm in length (fig. 1a). In the lateral view, the capitulum was rounded, knob-like, followed by two swellings and contractions before long arcuated lamina (fig. 1b). The gubernaculum was slightly concave, attenuated on proximal and distal ends (fig. 1a, b). Females showed a single sphincter forming the vulva, and the length between anus and vulva was approximately twice that between it and the tip of the tail, forming a longer and more attenuated tail than in other Parafilaroides species.

Fig. 1.

Parafilaroides normani from Arctocephalus australis found dead on the southern Brazilian coast. (A, B) Posterior end of a male showing the spicule morphology as described by Dailey (Reference Dailey2009); arrow indicates the capitulum. (C) Histological preparation of an infected lung in slices of females with innumerable larvae inside (arrow).

Few works have focused on P. normani since its first description. Although the characterization of the mitochondrial genome collected from the Australian fur seal, A. pusillus doriferus, is available in the genome bank (Jabbar et al., Reference Jabbar, Mohandas and Gasser2014), a previous study using molecular analyses in the same region identified Parafilaroides sp. (Jacobus et al., Reference Jacobus, Marigo, Gastal, Taniwaki, Ruoppolo, Catão-Dias and Tseng2016). It is not known why this kind of analysis was achieved only at genus level. Morphological data have been used primarily to identify metazoan parasites, and molecular analyses have been a tool in cryptic situations, since they are valuable in the detection of new species (Nadler et al., Reference Nadler, Lyons, Pagan, Hyman and Beron-Vera2013).

Even with many damaged worms, most of the females and two males were enough to evaluate structures of taxonomic importance, as used by Dailey (Reference Dailey2009), to identify the species. Molecular analysis was not performed due to the small sample volume and its total use for parasitological preparations. Morphology of the worms was different from the six recognized species, P. gymnurus, P. decorus, Parafilaroides hydrurgae, Parafilaroides hispidus, Parafilaroides measuresae and Parafilaroides gullandae, and it matched the original description of P. normani, including the spicule shape and size, the kind of vaginal sphincter musculature and the vulva-to-anus length (Dailey, Reference Dailey2009).

Filaroids found in marine mammals’ lungs are known as heteroxen worms, and these need one or more intermediate hosts (Measures, Reference Measures, Samuel, Pybus and Kocan2001; Lehnert et al., Reference Lehnert, von Samson-Himmelstjerna, Schaudien, Bleidorn, Wohlsein and Siebert2010). Previous studies performed with P. decorus have indicated that the fish Girella nigricans is a potential transmitter of infection to Z. californianus in the Northern Hemisphere (Dailey, Reference Dailey1970; Measures, Reference Measures, Samuel, Pybus and Kocan2001). No data about the life cycle of P. normani are available. On the southern coast of Brazil, Marigo (Reference Marigo2003) found that four out of six pinnipeds studied presented severe pneumonia due to parasites, and concluded that the lesions caused by them were more debilitating for the animal than those caused by gastrointestinal helminths. On the coast of Santa Catarina State, a recent study recorded lethal pneumonia caused by Parafilaroides sp. infection, associated with a g-herpes virus and Sarcocystis sp., in a juvenile A. tropicalis (Reisfeld et al., Reference Reisfeld, Sacristán and Sánchez-Sarmiento2019). In the present study, we recorded the presence of P. normani for the first time, but as the focus was to verify the prevalence of worms, it was impossible to be certain of the primary cause of death or to confirm if it was directly or indirectly associated with parasite infection.

Considering the low prevalence observed, the relevance of the infection is questionable, and it may have been an accidental and isolated case. High incidence of pathogenic helminths may suggest strategic colonization and dispersion behaviour, in which they infect with low prevalence and intensity to avoid loss of hosts (Sukhdeo, Reference Silva1994). Parafilaroides sp. are frequently associated with severe pneumonia, which may not be caused by the exclusive presence of the worms. On the other hand, low prevalence could also indicate accidental infection. The presence of gravid females of P. normani excludes this hypothesis, because it indicates that the fur seals examined are suitable definitive hosts for the parasite's life cycle.

In general, lungworms usually infect young seals and fur seals with more prevalence (Gosselin & Measures, Reference Gosselin and Measures2011; Ulrich et al., Reference Sukhdeo2016). Subadult specimens of A. australis that frequent coastal waters in southern Brazil come from Uruguay. A previous parasitological study in 105 pups (0–18 months of age) of the same species from Uruguayan reproductive colonies did not record the presence of pulmonary helminths (Katz et al., Reference Katz, Morgades and Castro-Ramos2012). The infection found in the subadult female reported in the present study suggests that the fur seals get the infection after 18 months of age, when many of them move away from the colonies toward southern Brazil and have a higher probability of encountering prey-infected organisms (Silva, Reference Silva2004). Considering the low prevalence found in the present study, more studies in subadult fur seals, including larger samples from southern Brazil with complete pathological and molecular analysis, would distinguish the mitochondrial genome of P. normani from A. australis and reveal the importance of the infections in the population's mortality rate in the South Atlantic.

This work reports the nematode P. normani in A. australis for the first time, and this is a new record of the biogeographic distribution in the South Atlantic Ocean for this nematode, including along the coast of Brazil.