Here we review the state-of-the-art of pathogens in select marine and terrestrial key species of the Baltic Sea, i.e. ringed seal (Pusa hispida), harbour seal (Phoca vitulina), grey seal (Halichoerus grypus), harbour porpoise (Phocoena phocoena), common eider (Somateria mollissima), pink-footed goose (Anser brachyrhynchus) and white-tailed eagle (Haliaeetus albicilla). This review is the first to merge and present available information and baseline data for the FP7 BONUS BaltHealth project: Baltic Sea multilevel health impacts on key species of anthropogenic hazardous substances. Understanding the spread, prevalence and effects of wildlife pathogens is important for the understanding of animal and ecosystem health, ecosystem function and services, as well as human exposure to zoonotic diseases. This review summarises the occurrence of parasites, viruses and bacteria over the past six decades, including severe outbreaks of Phocine Distemper Virus (PDV), the seroprevalence of Influenza A and the recent increase in seal parasites. We show that Baltic high trophic key species are exposed to multiple bacterial, viral and parasitic diseases. Parasites, such as C. semerme and P. truncatum present in the colon and liver Baltic grey seals, respectively, and anisakid nematodes require particular monitoring due to their effects on animal health. In addition, distribution of existing viral and bacterial pathogens, along with the emergence and spread of new pathogens, need to be monitored in order to assess the health status of key Baltic species. Relevant bacteria are Streptococcus spp., Brucella spp., Erysipelothrix rhusiopathiae, Mycoplasma spp. and Leptospira interrogans; relevant viruses are influenza virus, distemper virus, pox virus and herpes virus. This is of special importance as some of the occurring pathogens are zoonotic and thus also pose a potential risk for human health. Marine mammal handlers, as well as civilians that by chance encounter marine mammals, need to be aware of this risk. It is therefore important to continue the monitoring of diseases affecting key Baltic species in order to assess their relationship to population dynamics and their potential threat to humans. These infectious agents are valuable indicators of host ecology and can act as bioindicators of distribution, migration, diet and behaviour of marine mammals and birds, as well as of climate change and changes in food web dynamics. In addition, infectious diseases are linked to pollutant exposure, overexploitation, immune suppression and subsequent inflammatory disease. Ultimately, these diseases affect the health of the entire ecosystem and, consequently, ecosystem function and services. As global warming is continuously increasing, the impact of global change on infectious disease patterns is important to monitor in Baltic key species in the future.

The nasal mite Halarachne halichoeri (Acari; Halarachnidae) is adapted to live in the marine environment with pinnipeds as its primary host and can cause different levels of upper respiratory disease in both harbour seals (Phoca vitulina) and grey seals (Halichoerus grypus). Historical reports of H. halichoeri occurring in seals from German waters date back to the end of the 19th century. However, with the disappearance of the grey seal from German waters as a consequence of human over-exploitation, the mite vanished from the records and the fauna found in Germany for more than a century. Although a stranding network has been monitoring marine mammal health along the German coasts since the mid 1980s with extensive post-mortem investigations, this study reports the first and subsequent findings of H. halichoeri in grey and harbour seals from the North and Baltic Sea from 2014 onwards. The re-emergence of this endoparasitic mite in North and Baltic Sea habitats seems to have occurred simultaneously with the recolonisation of its primary host, the grey seal. During the course of its recolonisation, it was probably transmitted to harbour seals sharing the same haul-out sites. Molecular analyses showed a high similarity of rDNA sequences with H. halichoeri collected from sea otters (Enhydra lutris) in the USA. However, more thorough analyses of additional gene loci are required to fully assess the exchange and diversity of this parasite between geographically isolated regions and species.

The 1988 and 2002 phocine distemper virus (PDV) outbreaks in European harbour seals Phoca vitulina are among the largest mass mortality events recorded in marine mammals. Despite its large impact on harbour seal population numbers, and 3 decades of studies, many questions regarding the spread and temporal origin of PDV remain unanswered. Here, we sequenced and analysed 7123 bp of the PDV genome, including the coding and non-coding regions of the entire P, M, F and H genes in tissues from 44 harbour seals to shed new light on the origin and spread of PDV in 1988 and 2002. The phylogenetic analyses trace the origin of the PDV strain causing the 1988 outbreak to between May 1987 and April 1988, while the origin of the strain causing the 2002 outbreak can be traced back to between June 2001 and May 2002. The analyses further point to several independent introductions of PDV in 1988, possibly linked to a southward mass immigration of harp seals in the winter and spring of 1987-1988. The vector for the 2002 outbreak is unknown, but the epidemiological analyses suggest the subsequent spread of PDV from the epicentre in the Kattegat, Denmark, to haul-out sites in the North Sea through several independent introductions.

Phocine distemper virus (PDV) is a morbillivirus that circulates within pinnipeds in the North Atlantic. PDV has caused two known unusual mortality events (UMEs) in western Europe (1988, 2002), and two UMEs in the northwest Atlantic (2006, 2018). Infrequent cross-species transmission and waning immunity are believed to contribute to periodic outbreaks with high mortality in western Europe. The viral ecology of PDV in the northwest Atlantic is less well defined and outbreaks have exhibited lower mortality than those in western Europe. This study sought to understand the molecular and ecological processes underlying PDV infection in eastern North America. We provide phylogenetic evidence that PDV was introduced into northwest Atlantic pinnipeds by a single lineage and is now endemic in local populations. Serological and viral screening of pinniped surveillance samples from 2006 onward suggest there is continued circulation of PDV outside of UMEs among multiple species with and without clinical signs. We report six full genome sequences and nine partial sequences derived from harbour and grey seals in the northwest Atlantic from 2011 through 2018, including a possible regional variant. Work presented here provides a framework towards greater understanding of how recovering populations and shifting species may impact disease transmission.

Canine distemper virus (CDV) and phocine distemper virus (PDV) are major pathogens to terrestrial and marine mammals. Yet little is known about the timing and geographical origin of distemper viruses and to what extent it was influenced by environmental change and human activities. To address this, we (i) performed the first comprehensive time-calibrated phylogenetic analysis of the two distemper viruses, (ii) mapped distemper antibody and virus detection data from marine mammals collected between 1972 and 2018, and (iii) compiled historical reports on distemper dating back to the eighteenth century. We find that CDV and PDV diverged in the early seventeenth century. Modern CDV strains last shared a common ancestor in the nineteenth century with a marked radiation during the 1930s–1950s. Modern PDV strains are of more recent origin, diverging in the 1970s–1980s. Based on the compiled information on distemper distribution, the diverse host range of CDV and basal phylogenetic placement of terrestrial morbilliviruses, we hypothesize a terrestrial CDV-like ancestor giving rise to PDV in the North Atlantic. Moreover, given the estimated timing of distemper origin and radiation, we hypothesize a prominent role of environmental change such as the Little Ice Age, and human activities like globalization and war in distemper virus evolution.

Pestiviruses are widespread pathogens causing severe acute and chronic diseases among terrestrial mammals. Recently, Phocoena pestivirus (PhoPeV) was described in harbour porpoises (Phocoena phocoena) of the North Sea, expanding the host range to marine mammals. While the role of the virus is unknown, intrauterine infections with the most closely related pestiviruses— Bungowannah pestivirus (BuPV) and Linda virus (LindaV)—can cause increased rates of abortions and deaths in young piglets. Such diseases could severely impact already vulnerable harbour porpoise populations. Here, we investigated the presence of PhoPeV in 77 harbour porpoises, 277 harbour seals (Phoca vitulina), grey seals (Halichoerus grypus) and ringed seals (Pusa hispida) collected in the Baltic Sea region between 2002 and 2019. The full genome sequence of a pestivirus was obtained from a juvenile female porpoise collected along the coast of Zealand in Denmark in 2011. The comparative Bayesian phylogenetic analyses revealed a close relationship between the new PhoPeV sequence and previously published North Sea sequences with a recent divergence from genotype 1 sequences between 2005 and 2009. Our findings provide further insight into the circulation of PhoPeV and expand the distribution from the North Sea to the Baltic Sea region with possible implications for the vulnerable Belt Sea and endangered Baltic Proper harbour porpoise populations.