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The Seal Louse (Echinophthirius Horridus) in the Dutch Wadden Sea: Investigation of Vector‑Borne Pathogens Jörg Hirzmann1†, David Ebmer1†, Guillermo J

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The Seal Louse (Echinophthirius Horridus) in the Dutch Wadden Sea: Investigation of Vector‑Borne Pathogens Jörg Hirzmann1†, David Ebmer1†, Guillermo J Hirzmann et al. Parasites Vectors (2021) 14:96 https://doi.org/10.1186/s13071-021-04586-9 Parasites & Vectors RESEARCH Open Access The seal louse (Echinophthirius horridus) in the Dutch Wadden Sea: investigation of vector-borne pathogens Jörg Hirzmann1†, David Ebmer1†, Guillermo J. Sánchez‑Contreras2, Ana Rubio‑García2, Gerd Magdowski3, Ulrich Gärtner3, Anja Taubert1 and Carlos Hermosilla1* Abstract Background: Belonging to the anopluran family Echinophthiriidae, Echinophthirius horridus, the seal louse, has been reported to parasitise a broad range of representatives of phocid seals. So far, only a few studies have focused on the vector function of echinophthiriid lice, and knowledge about their role in pathogen transmission is still scarce. The current study aims to investigate the possible vector role of E. horridus parasitising seals in the Dutch Wadden Sea. Methods: E. horridus seal lice were collected from 54 harbour seals (Phoca vitulina) and one grey seal (Halichoerus grypus) during their rehabilitation period at the Sealcentre Pieterburen, The Netherlands. DNA was extracted from pooled seal lice of individual seals for molecular detection of the seal heartworm Acanthocheilonema spirocauda, the rickettsial intracellular bacterium Anaplasma phagocytophilum, and the cell wall‑less bacteria Mycoplasma spp. using PCR assays. Results: Seal lice from 35% of the harbour seals (19/54) and from the grey seal proved positive for A. spirocauda. The seal heartworm was molecularly characterised and phylogenetically analysed (rDNA, cox1). A nested PCR was developed for the cox1 gene to detect A. spirocauda stages in seal lice. A. phagocytophilum and a Mycoplasma species previously identifed from a patient with disseminated ‘seal fnger’ mycoplasmosis were detected for the frst time, to our knowledge, in seal lice. Conclusions: Our fndings support the potential vector role of seal lice in the transmission of A. spirocauda and reveal new insights into the spectrum of pathogens occurring in seal lice. Studies on vector competence of E. horridus, espe‑ cially for bacterial pathogens, are essentially needed in the future as these pathogens might have detrimental efects on the health of seal populations. Furthermore, studies on the vector role of diferent echinophthiriid species infect‑ ing a wide range of pinniped hosts should be conducted to extend the knowledge of vector‑borne pathogens. Keywords: Pinnipeds, Phocidae, Marine mammal parasitology, Anoplura, Echinophthiriidae Background mammals, such as pinnipeds (Otariidae, Phocidae, Odo- Representatives of the family Echinophthiriidae belong benidae) and the North American river otter (Lontra to the phthirapteran suborder Anoplura, the sucking canadensis) [1]. Within the Echinophthiriidae, fve gen- lice, and exhibit a host range solely infesting semiaquatic era (Antarctophthirus, Lepidophthirus, Echinophthirius, Proechinophthirus, and Latagophthirus) and 13 species are described [1, 2]. While many echinophthiriid spe- *Correspondence: [email protected]‑giessen.de †Jörg Hirzmann and David Ebmer contributed equally to this work cies display a strict major host specifcity, the seal louse 1 Institute of Parasitology, Biomedical Research Center Seltersberg, Justus Echinophthirius horridus exhibits the broadest host range Liebig University Giessen, Schubertstr. 81, 35392 Giessen, Germany among echinophthiriid lice parasitising eight diferent Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Hirzmann et al. Parasites Vectors (2021) 14:96 Page 2 of 10 species of Phocidae, the earless or true seals, with a geo- an Alphavirus, was isolated from Lepidophthirus mac- graphical distribution confned to the Northern Hemi- rorhini parasitising the Southern elephant seal (Mirounga sphere, including harbour seals (Phoca vitulina) and grey leonina) [6]. seals (Halichoerus grypus) [1]. Furthermore, E. horridus has been suggested to serve Due to their obligate and permanent hematophagous as the obligate intermediate host for the seal heartworm feeding habits [1], members of the Echinophthiriidae Acanthocheilonema spirocauda, i.e. A. spirocauda- have the potential to play an important role in the epi- microflariae (L1), taken up by a bloodmeal of the louse, demiology of vector-borne diseases in free-ranging pin- develop into infective L3-stages, which are inoculated to niped populations. Nonetheless, studies on the possible seals during the blood meals [7–9]. Te proposed role vector function of echinophthiriid species are scarce, but of E. horridus as an intermediate host for A. spirocauda some of them already highlighted their role in poten- was supported by the fnding of diferent developmen- tial pathogen transmission (Table 1). Te bacterium Sal- tal stages in dissected lice [7, 9], the signifcant positive monella enteritidis was isolated from blood and tissue of correlation of infestation of seals with E. horridus and Northern fur seals (Callorhinus ursinus) and from the seal infection with A. spirocauda [11], and molecular echinophthiriid lice Antarctophthirus callorhini and/or analyses [10]. Proechinophthirus fuctus collected from the same indi- Echinophthiriid species exhibit special morphologi- viduals. Additionally, these infections were also asso- cal characteristics, which are unique among anopluran ciated with a mortality event of C. ursinus pups [3]. A lice and are the basis of their evolutionary success, being Rickettsia species closely related to the human pathogen infuenced by heterogeneous environmental conditions. Rickettsia rickettsi was isolated from P. fuctus collected Tus, distinct spiracles are equipped with special occlu- from Northern fur seals [4]. Bartonella henselae was sions allowing for gas exchange [12]. Abdominal seg- detected in E. horridus and spleen samples of dissected ments are characterised by a general loss of sclerotization harbour seals [5]. Southern elephant seal virus (SESV), and by a distinct trimming with modifed setae [12, 13], Table 1 Pathogens detected in Echinophthiriidae Echinophthiriid species Detected pathogen References Echinophthirius horridus Acanthocheilonema spirocauda [7–10, Present study] Bartonella henselae [5] Anaplasma phagocytophilum [Present study] Mycoplasma sp. [Present study] Antarctophthirus callorhini Salmonella enteritidis [3] Proechinophthirus fuctus Salmonella enteritidis [3] Rickettsia sp. [4] Lepidophthirus macrorhini Southern elephant seal virus (SESV) [6] Fig. 1 Ultrastructural illustration of Echinophthirius horridus adult and egg (nit) stages. (a) Ventral view of adult E. horridus; (b) two opened nits lacking opercula frmly glued to seal fur hair. Scale bars: (a) 500 μm, (h) 200 μm Hirzmann et al. Parasites Vectors (2021) 14:96 Page 3 of 10 sensorial organs, that are classifed into spines, scales, Collected seal lice specimens as well as eggs (nits) from and hairs [14]. Furthermore, the last two pairs of legs for seal fur, mainly from the head and neck, were fxed in fxation to the host surface are another characteristic of 70% ethanol and morphologically determined by light echinophthiriid lice. E. horridus difers from other mem- microscopy. All seal lice stages examined here were clas- bers of the family by the restructuring of all three pairs of sifed according to morphological features [1, 14–17]. legs into claws and the absence of abdominal scale mani- All fxed specimens were kept at room temperature and festation (Fig. 1) [14–17]. delivered to the Institute of Parasitology, Justus Liebig Due to these morphological adaptions and a strict University Giessen, Germany, for further processing. Te specifty to semiaquatic host species, a coevolution of estimation of the 95% CI was conducted using Kohn and echinophthiriid lice and their hosts has been suggested Senyak [22]. [13, 18, 19]. Tereby, it has been proposed that the ances- tors of pinnipeds must have already been infested with PCR analyses ancestral sucking lice before they ventured into the Seal lice were grouped from each seal and collection marine habitat [8, 20]. As a consequence of their growing date separately, resulting in 64 pools from the 54 har- specialisation to ancestral pinnipeds, ancestors of E. hor- bour seals (P. vitulina) containing 1–20 lice and one ridus lice might have evolved a vector role in the trans- pool of > 1000 lice from the highly infested grey seal pup mission of ancestors of the heartworm A. spirocauda, divided into pools of 15 lice (Additional
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