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

Abstract

The ectoparasitic seal louse, Echinophthirius horridus infects harbour (Phoca vitulina) and grey seals (Halichoerus grypus) in the North and Baltic Sea. The endoparasitic heartworm Acanthocheilonema spirocauda parasitizes the right heart and blood vessels of harbour seals. The complete lifecycle of the heartworm is not entirely understood although the seal louse is assumed to serve as vector for its transmission. Knowledge about the impact of both parasite species on host health are scarce. In this study, necropsy data and archived parasites of harbour and grey seals in German waters were analysed to determine long-term seal louse (SLP) and heartworm prevalence (HWP) from 2014 to 2021. Histology, microbiology and scanning electron microscopy (SEM) were applied on seal louse infected and uninfected skin to investigate associated lesions and the health impact. During the study period, HWP in harbour seals was 13%, the SLP in harbour seals was 4% and in grey seals 10%. HWP of harbour seals was significantly higher during the winter months compared to the summer. SLP in adults was significantly higher in comparison to juvenile harbour seals. SLP varied significantly between grey seals from the North and Baltic Sea. Filarial nematodes were detected in the haemocoel, pharynx, and intestine of E. horridus highlighting the seal louse as vector for heartworms. Alopecia and folliculitis were associated with the attachment posture of E. horridus and microbiological investigations isolated bacteria commonly associated with folliculitis.

Keywords: Grey seals; Harbour seals; Heartworm; Host-parasite relationship; Marine mammal parasites; Seal louse.

Graphical abstract

Fig. 1

Levels of infection with E. horridus in P. vitulina. A: Mild E. horridus infection of a harbour seal yearling, asterisk pointing at E. horridus B: Close up of E. horridus in the head area of a harbour seal C: Severe E. horridus infection of a harbour seal D: Close up of severe E. horridus infection. Scale bars: A-D 1 cm.

Fig. 2

Sampling routine of E. horridus infected seal skin for histological and bacteriological examinations. A: Mild E. horridus infection of a harbour seal yearling, asterisk pointing at E. horridus. B: Close up of E. horridus C: Removing of E. horridus D: Cutting and removing of the infected skin with a sterile forceps for further investigations. Scale bars: A-D 1 cm.

Fig. 3

A: Prevalence of A. spirocauda and E. horridus in harbour seals in the North and Baltic Sea from 1996 to 2021, data from 1996 to 2013 according to Lehnert et al. (2016). B: Prevalence of A. spirocauda and E. horridus in harbour seals during the seasons in the North and Baltic Sea from 2014 to 2021.

Fig. 4

Histological sections and staining of E. horridus revealing filarial stages in E. horridus. A: Filarial stages (arrowheads) in the pharynx. bar = 20 μm. B: Filarial stage (arrow) in the mouth region. bar = 40 μm. C: Filarial stage (arrowhead) in the intestine (in) surrounded by erythrocytes (e). bar = 15 μm. D: Filarial stage in the haemocoel (hc) of the abdomen of E. horridus (square). E: Close up of filarial stage. mp = mouthparts, mo = mouth, cu = cuticula. A–C: Haematoxylin - Eosin stain, D: Giemsa stain.

Fig. 5

Scanning electron microscopic images of E. horridus attached to seal skin and fur. A: E. horridus utilizing a hair follicle of harbour seal skin. B: E. horridus attached to seal hair with the head pointing towards seal skin. C: E. horridus with six claws attached to seal fur. D: Close up of an unattached claw of E. horridus. Asterisks positioned on nits of E. horridus. Sale bars: A 200 μm, B 400 μm, C 400 μm, D 100 μm.