Echinophthirius horridus

Herzog, Insa, Wohlsein, Peter, Preuss, Anika, Gorb, Stanislav N., Pigeault, emi, Ewers, Christa, Prenger-Berninghoff, Ellen, Siebert, Ursula & Lehnert, Kristina, 2024, Heartworm and seal louse: Trends in prevalence, characterisation of impact and transmission pathways in a unique parasite assembly on seals in the North and Baltic Sea, International Journal for Parasitology: Parasites and Wildlife 23, pp. 100898-100898 : 100898-

4.1. E. horridus and A. spirocauda infections in harbour and grey seals

In this study, harbour seals showed an A. spirocauda prevalence of 13%, while the prevalence of E. horridus was at 4% over the study period of eight years. In comparison to a previous study about harbour seals in the same geographical area between 1996 and 2013, in which the total prevalence of A. spirocauda and E. horridus accounted to 4.4% and 3.4% respectively ( Lehnert et al., 2016), the prevalence of A. spirocauda increased and prevalence of E.horridus remained low. Thus, the prevalence of A. spirocauda within the harbour seal population in the German North and Baltic Sea has almost tripled compared to the previous two decades. In 1988 within a time period of 4 months a prevalence of 24.5% was determined in the Dutch North Sea ( Borgsteede et al., 1991). For the same year a prevalence of 11.4% was registered in the Kattegat-Skagerrak and the Baltic region ( Lunneryd, 1992), while 32.2% were observed in the Wadden Sea of Lower Saxony ( Claussen et al., 1991). All three studies based their investigations on harbour seals, which died during the phocid distemper virus outbreak in 1988/89. This

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implies that, prior to the first PDV epidemic in 1988/89, the prevalence of the heartworm infections within the harbour seal population in the Wadden Sea maintained at a higher level. In the following two decades, the harbour seal population decreased drastically due to two PDV outbreaks (1989/99 and 2002) ( Müller et al., 2004, Hark ¨¨onen et al., 2006), since 2002 the population is recovering and increasing, up to a total number of 26,721 adult animals counted in 2021 (Unger et al., 2022). In consequence of the density dependency of parasites ( Anderson and May 1979, May and Anderson, 1979), the heartworm prevalence may increase with an increasing host density in the defined geographical area. Growing seal populations in German waters result in higher seal densities on haul-outs (Unger et al., 2022), thereby facilitating transmission of the heartworm by seal lice vectors. Equally to the present study, dependency of season was observed in previous decades, however the highest infection rate occurred in summer at Washington Coast ( Dailey and Fallace, 1989), while in this study, winter months showed the highest A. spirocauda prevalence. Transmission patterns of other vector-borne parasites such as the heartworm of dogs ( Dirofilaria immitis ) is influenced by seasonal temperature changes ( Ledesma and Harrington, 2011). To discover transmission patterns for A. spirocuada , further investigations regarding prevalence of mature heartworms as well as monitoring of microfilaria stages in the blood of seals are needed.

In contrary to the prevalence of A. spirocauda , no increase in prevalence of seal louse infections was observed over the last eight years. The prevalence of E. horridus in the study period remained low, similar to previous years ( Lehnert et al., 2016). While no seal lice infection was reported in harbour seals inhabiting the Kattegat-Skagerrak area after the first seal epidemic ( Lunneryd, 1992), seal lice prevalence of 39% was found in Scottish waters, based on a four-year time span of sampling live harbour seals ( Thompson et al., 1998). In addition, 45.5% of investigated harbour seals were infected at the Washington state coast, USA ( Dailey and Fallace, 1989). These notable variations observed in seal louse prevalence in phocid seals may be due to different conditions influencing the different geographic locations. Equally, the sampling bias of ectoparasites has to be taken into account. Ectoparasites may leave the host after death, are eaten by necrophagous birds or lost during the stranding process and transport of the carcass ( Thompson et al., 1998; Lehnert et al., 2021; Rohner et al., 2023). Mild infections can be overlooked at necropsy since manual brushing with a louse comb might not cover the complete fur of the animal and therefore lead to inaccurate prevalence of ectoparasites ( Ignoffo, 1958). The highest prevalence of E. horridus was observed in adult harbour seals, contrary to a previous study in which the prevalence was highest in yearlings in the German Wadden Sea ( Lehnert et al., 2016) and in juvenile harbour seals on the Scottish coastline ( Thompson et al., 1998). Vertical transmission from mother to pups is considered the most important way of transmission (Murray et al., 1965; Murray and Nicholls, 1965; Kim, 1975; Leidenberger et al., 2007; Leonardi et al., 2013). This would again require a similarly high infection rate in adult seals, as seen in the present study. In contrary to previous studies ( Dailey and Fallace, 1989; Thompson et al., 1998), no seasonal component of E. horridus infection was observed.

It is striking that grey seals are twice as often and more severely infected with seal lice compared to harbour seals, while A. spirocauda usually seems to occur only in harbour seals ( Leidenberger et al., 2007). Infections with E. horridus were described in grey seals ( Durden and Musser, 1994), but studies investigating the long-term prevalence and dynamics of ectoparasitic seal lice in grey seals are missing. This study showed a significant increase of seal louse infections in grey seals over the last three years ( Table 2). All infected grey seals, except for one, originated from the Baltic Sea. Recent recolonization of the southern Baltic Sea with steadily increasing numbers of grey seals on haul outs sites ( Galatius et al., 2020) could be linked to higher chances of seal louse transmission rates between grey seals. Due to continued increase of eutrophication, exposure to hazardous substances and marine litter ( HELCOM, 2023) environmental conditions may affect the skin microbiome and immune status ( Sehnal et al., 2021) influencing susceptibility for ectoparasitic infections.

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The different infection patterns of heartworm and seal louse in grey and harbour seals may derive from the genetic constitution of both species. Although both species are closely related, share habitat and dietary preferences ( Boyi et al., 2022), immunological traits influencing susceptibility to infectious diseases ( Schmid-Hempel, 2003) differ between the two hosts. These differences became apparent during the phocine distemper virus epidemic, when grey seals were exposed to the virus and displayed high levels of antibodies but only a small number of animals died due to the virus infection ( Cornwell et al., 1992). Heterozygosity as determining factor for fitness and variations in parasite infection ( Rijks et al., 2008, Hoffman et al., 2014) are considered as possible factor causing varying interspecific susceptibility to parasites in harbour and grey seals ( Lehnert et al., 2023). Genetic exchange within populations is influenced by recent grey seal recolonization of the North ( Reijnders et al., 1995) and Baltic Sea ( Galatius et al., 2020), as well as foraging and movement patterns of grey seals causing them to travel hundreds of kilometres (D. Thompson et al., 1991) while harbour seals rather stay resident in one geographical area ( Stewart et al., 1989; Thompson and Miller, 1990; P.M. Thompson et al., 1991). Additionally, grey seals may be atypical hosts for seal lice and therefore less resistant to seal louse infections, causing more prevalent and severe infection in seal louse-naive individuals ( Daszak et al., 2000). Different infection patterns of A. spirocauda in harbour and grey seals were also discussed to be caused by insufficient sampling ( Measures et al., 1997; Keroack et al., 2018) or high mortality caused by heartworm infections in grey seals ( Keroack et al., 2018).