The 1988 and 2002 phocine distemper virus epidemics in European harbour seals

We present new and revised data for the phocine distemper virus (PDV) epidemics that resulted in the deaths of more than 23 000 harbour seals Phoca vitulina in 1988 and 30,000 in 2002. On both occasions the epidemics started at the Danish island of Anholt in central Kattegat, and subsequently spread to adjacent colonies in a stepwise fashion. However, this pattern was not maintained throughout the epidemics and new centres of infection appeared far from infected populations on some occasions: in 1988 early positive cases were observed in the Irish Sea, and in 2002 the epidemic appeared in the Dutch Wadden Sea, 6 wk after the initiation of the outbreak at Anholt Island. Since the harbour seal is a rather sedentary species, such 'jumps' in the spread among colonies suggest that another vector species could have been involved. We discussed the role of sympatric species as disease vectors, and suggested that grey seal populations could act as reservoirs for PDV if infection rates in sympatric species are lower than in harbour seals. Alternatively, grey seals could act as subclinical infected carriers of the virus between Arctic and North Sea seal populations. Mixed colonies of grey and harbour seal colonies are found at all locations where the jumps occurred. It seems likely that grey seals, which show long-distance movements, contributed to the spread among regions. The harbour seal populations along the Norwegian coast and in the Baltic escaped both epidemics, which could be due either to genetic differences among harbour seal populations or to immunity. Catastrophic events such as repeated epidemics should be accounted for in future models and management strategies of wildlife populations.     

Evaluating the influence of epidemiological parameters and host ecology on the spread of phocine distemper virus through populations of harbour seals

Background

Outbreaks of phocine distemper virus (PDV) in Europe during 1988 and 2002 were responsible for the death of around 23,000 and 30,000 harbour seals, respectively. These epidemics, particularly the one in 2002, provided an unusual opportunity to estimate epidemic parameters for a wildlife disease. There were marked regional differences in the values of some parameters both within and between epidemics.

Methodology and Principal Findings

We used an individual-based model of seal movement that allowed us to incorporate realistic representations of space, time and animal behaviour into a traditional epidemiological modelling framework. We explored the potential influence of a range of ecological (foraging trip duration, time of epidemic onset, population size) and epidemiological (length of infectious period, contact rate between infectious and susceptible individuals, case mortality) parameters on four readily-measurable epidemic characteristics (number of dead individuals, duration of epidemic, peak mortality date and prevalence) and on the probability that an epidemic would occur in a particular region. We analysed the outputs as if they were the results of a series of virtual experiments, using Generalised Linear Modelling. All six variables had a significant effect on the probability that an epidemic would be recognised as an unusual mortality event by human observers.

Conclusions

Regional and temporal variation in contact rate was the most likely cause of the observed differences between the two epidemics. This variation could be a consequence of differences in the way individuals divide their time between land and sea at different times of the year.     

Persistence thresholds for phocine distemper virus infection in harbour seal Phoca vitulina metapopulations

1. This paper explores the concept of the critical community size for persistence of infection in wildlife populations. We use as a case study the 1988 epidemic of phocine distemper virus in the North Sea population of harbour seals, Phoca vitulina .
2. We summarize the available data on this epidemic and use it to parameterize a stochastic compartmental model for an infection spreading through a spatial array of patches coupled by nearest-neighbour mixing, with replacement of susceptibles occurring as a discrete annual event.
3. A combination of analytical and simulation techniques is used to show that the high levels of transmission between different seal subpopulations, combined with the small annual birth cohort, act to make persistence of infection impossible in this harbour seal population at realistic population levels. The well known mechanisms by which metapopulation structures may act to promote persistence can be seen to have an effect only at weaker levels of spatial coupling, and higher levels of host recruitment, than those empirically observed.     

Age- and sex-specific mortality patterns in an emerging wildlife epidemic: the phocine distemper in European harbour seals

Analyses of the dynamics of diseases in wild populations typically assume all individuals to be identical. However, profound effects on the long-term impact on the host population can be expected if the disease has age and sex dependent dynamics. The Phocine Distemper Virus (PDV) caused two mass mortalities in European harbour seals in 1988 and in 2002. We show the mortality patterns were highly age specific on both occasions, where young of the year and adult (>4 yrs) animals suffered extremely high mortality, and sub-adult seals (1-3 yrs) of both sexes experienced low mortality. Consequently, genetic differences cannot have played a main role explaining why some seals survived and some did not in the study region, since parents had higher mortality levels than their progeny. Furthermore, there was a conspicuous absence of animals older than 14 years among the victims in 2002, which strongly indicates that the survivors from the previous disease outbreak in 1988 had acquired and maintained immunity to PDV. These specific mortality patterns imply that contact rates and susceptibility to the disease are strongly age and sex dependent variables, underlining the need for structured epidemic models for wildlife diseases. Detailed data can thus provide crucial information about a number of vital parameters such as functional herd immunity. One of many future challenges in understanding the epidemiology of the PDV and other wildlife diseases is to reveal how immune system responses differ among animals in different stages during their life cycle. The influence of such underlying mechanisms may also explain the limited evidence for abrupt disease thresholds in wild populations.     

The potential effects of repeated outbreaks of phocine distemper among harbour seals: a response to Harding et al. (2002)

In 2002 phocine distemper virus (PDV) reappeared in the European harbour seal (Phoca vitulina) population. This outbreak seems to have followed a similar pattern to the 1988 one which killed almost 60% of individuals in most localities. Harding et al. (2002) suggested that there is a relatively high (18%) risk that recurrent outbreaks of PDV could reduce the European harbour seal population by 90%. We show that incorporating the effects of observation error during population surveys and of the long‐term immunity of survivors of morbillivirus outbreaks indicate a much lower level of risk (<1%). This suggests that, while the immediate effects of the disease are dramatic, it is unlikely that recurrent epidemics will pose serious conservation problems for this species under current conditions.     

Stage-structured transmission of phocine distemper virus in the Dutch 2002 outbreak

Heterogeneities in transmission among hosts can be very important in shaping infectious disease dynamics. In mammals with strong social organization, such heterogeneities are often structured by functional stage: juveniles, subadults and adults. We investigate the importance of such stage-related heterogeneities in shaping the 2002 phocine distemper virus (PDV) outbreak in the Dutch Wadden Sea, when more than 40 per cent of the harbour seals were killed. We do this by comparing the statistical fit of a hierarchy of models with varying transmission complexity: homogeneous versus heterogeneous mixing and density- versus frequency-dependent transmission. We use the stranding data as a proxy for incidence and use Poisson likelihoods to estimate the ‘who acquires infection from whom’ (WAIFW) matrix. Statistically, the model with strong heterogeneous mixing and density-dependent transmission was found to best describe the transmission dynamics. However, patterns of incidence support a model of frequency-dependent transmission among adults and juveniles. Based on the maximum-likelihood WAIFW matrix estimates, we use the next-generation formalism to calculate an R₀ between 2 and 2.5 for the Dutch 2002 PDV epidemic.     

Serologic study of phocine distemper in a population of harbor seals in Scotland.

A serologic survey of the prevalence of morbillivirus antibodies was conducted in a population of harbor seals (Phoca vitulina) from northeastern Scotland, where mortality was comparatively low during the 1988 phocine distemper virus outbreak. None of the 12 seals sampled before the epizootic were seropositive. Thirty-five (52%) of 68 seals sampled after the beginning of the epizootic were seropositive, although there were significant age-related differences in both the number of seropositive individuals and in antibody levels. Marking studies showed that most seropositive seals caught during the peak of the epizootic survived for several months. Thus, the low mortality observed in this population did not appear to result from a lack of contact with the virus.     

Antibodies to canine distemper and phocine distemper viruses in polar bears from the Canadian arctic

Serum samples collected from 200 polar bears (Ursus marititnus) from two populations in the Canadian arctic, the western Hudson Bay and Lancaster Sound populations, between 1989 and 1996, were tested for antibodies to canine distemper (CDV) and phocine distemper viruses (PDV) using virus neutralization. Antibodies to CDV and PDV were detected in 48 and six polar bears, respectively. All six bears that tested positive for PDV also tested positive for CDV; in only one case did the antibody titer for PDV exceed that of CDV. Differences in antibody prevalence to CDV were detected between populations and age classes but not sex or year of sampling.     

Increasing numbers of harbour seals and grey seals in the Solent

Harbour seals (Phoca vitulina) and grey seals (Halichoerus grypus) both occur within the UK, but display regional contrasting population trends. While grey seals are typically increasing in number, harbour seals have shown varying trends in recent decades following repeated pandemics. There is a need for monitoring of regional and local populations to understand overall trends. This study utilized a 20‐year dataset of seal counts from two neighboring harbours in the Solent region of south England. Generalized additive models showed a significant increase in the numbers of harbour (mean 5.3–30.5) and grey (mean 0–12.0) seals utilizing Chichester Harbour. Conversely, in Langstone Harbour there has been a slight decrease in the number of harbour seals (mean 5.3–4.0). Accompanying photographic data from 2016 to 18 supports the increase in seal numbers within Chichester Harbour, with a total of 68 harbour and 8 grey seals identified. These data also show evidence of site fidelity of harbour seals in this area, with almost a quarter of animals resighted within the past three years. Overall, this long‐term study indicates an increasing number of both harbour and grey seals within the Solent. However, more research is required to identify the drivers of this trend.     

Phocine distemper virus uses phocine and other animal SLAMs as a receptor but not human SLAM

Morbilliviruses use the signaling lymphocyte activation molecule (SLAM) as a receptor to infect their hosts. Seals are almost the only animal species that show apparent infection with phocine distemper virus (PDV). Seal SLAM functioned as a PDV receptor. However, dolphin- and dog-SLAM molecules, but not human SLAM, were also fully functional PDV receptors. These data suggest that the host range of PDV is not simply determined by its SLAM usage. However, human nonsusceptibility to PDV infection may be at least partly attributable to the inability of PDV to use human SLAM as a receptor.     

Serologic survey for Brucella spp., phocid herpesvirus-1, phocid herpesvirus-2, and phocine distemper virus in harbor seals from Alaska, 1976-1999

Harbor seals (Phoca vitulina richardsi) were captured in the coastal regions of Southeast Alaska, Gulf of Alaska, Prince William Sound (PWS), and Kodiak Island during 1976-1999. Blood was collected from 286 seals. Sera were tested for evidence of exposure to Brucella spp., phocid herpesvirus-1 (PhoHV-1), phocid herpesvirus-2 (PhHV-2), and phocine distemper virus (PDV). Antibody prevalence rates were 46% (46/100) for Brucella spp., 93% (225/243) for PhoHV-1, 0% (0/286) for PhHV-2, and 1% (2/160) for PDV. Antibody prevalence for Brucella spp. was directly related to host age. Antibody prevalence for PhoHV-1 was higher in PWS as compared to the other three regions. No evidence of mortality attributable to these four agents was observed during the course of this study. Based on the results of this survey, none of these agents is considered a significant mortality factor in harbor seals from the four regions of coastal Alaska included in the study.     

Antibodies against european phocine herpesvirus isolates detected in sera of Antarctic seals

Summary Neutralizing antibodies against European phocine herpesvirus were detected in sera of to two Antarctic seal species, Weddell seals (Leptonychotes weddellii) and crabeater seals (Lobodon carcinophagus), collected in the eastern Weddell Sea. A large number of positive sera crossneutralized canine herpesvirus, but only few sera also contained antibodies to feline herpesvirus. The Weddell seals suffered from a respiratory disease when the sera were collected (January–February, 1990). The significance and possible origin of herpesvirus infections in Antarctic seals documented for the first time in this communication is discussed. All sera were negative for antibodies against phocine and canine distemper viruses.     

The enigma of the landlocked Baikal and Caspian seals addressed through phylogeny of phocine mitochondrial sequences

The endemic seals of Lake Baikal ( Phoca sibirica ) and of the Caspian Sea ( Phoca caspica ) inhabit ancient continental basins that have remained isolated from primary marine seal habitats for millions of years. The species have been united with the Arctic ringed seal, Phoca hispida , into (sub)genus Pusa , but the age and route of invasions to/from the continental basins remain controversial. A phylogenetic analysis of nine northern phocines based on three mitochondrial genes (Cyt b , COI, COII, total 3369 bp) provided no support for the monophyly of the Pusa group. The three species are involved in an apparent polytomy with the boreal harbour seal, Phoca vitulina , and grey seal, Halichoerus grypus . From the average estimated interspecies divergence (4.1%), the radiation of this group plausibly took place in the Late Pliocene 2–3 Mya. This dating does not fit the prevailing hypotheses on the origin of the landlocked taxa in association with Middle Pleistocene glacial events, or of the Caspian seal as a direct descendant of Miocene fossil phocines of the continental Paratethyan basin. The current phocine diversity more likely results from marine radiations, and the continental seals invaded their basins through Plio-Pleistocene (marine) connections from the north. The palaeohydrography that would have enabled the invasions at that time still remains an enigma.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 61–72.     

Modelling the wind-borne spread of highly pathogenic avian influenza virus between farms

A quantitative understanding of the spread of contaminated farm dust between locations is a prerequisite for obtaining much-needed insight into one of the possible mechanisms of disease spread between farms. Here, we develop a model to calculate the quantity of contaminated farm-dust particles deposited at various locations downwind of a source farm and apply the model to assess the possible contribution of the wind-borne route to the transmission of Highly Pathogenic Avian Influenza virus (HPAI) during the 2003 epidemic in the Netherlands. The model is obtained from a Gaussian Plume Model by incorporating the dust deposition process, pathogen decay, and a model for the infection process on exposed farms. Using poultry- and avian influenza-specific parameter values we calculate the distance-dependent probability of between-farm transmission by this route. A comparison between the transmission risk pattern predicted by the model and the pattern observed during the 2003 epidemic reveals that the wind-borne route alone is insufficient to explain the observations although it could contribute substantially to the spread over short distance ranges, for example, explaining 24% of the transmission over distances up to 25 km.     

Transmission of lungworms of harbour porpoises and harbour seals: Molecular tools determine potential vertebrate intermediate hosts

Harbour porpoises (Phocoena phocoena) and harbour seals (Phoca vitulina) from German waters are infected by six species of lungworms (Metastrongyloidea). These nematodes parasitise the respiratory tract, are pathogenic and often cause secondary bacterial infections. In spite of their clinical and epidemiological significance, the life cycle and biology of lungworms in the marine environment is still largely unknown. Regions of ribosomal DNA (ITS-2) of all lungworms parasitising harbour porpoises and harbour seals in German waters were sequenced to characterise and compare the different species. The phylogenetic relationship among the lungworm species was analysed by means of their ITS-2 nucleotide sequences and the species-specific traits of the ITS-2 were used to screen wild fish as possible intermediate hosts for larval lungworms. Molecular markers were developed to identify larval nematodes via in-situ hybridisation of tissues of harbour porpoise and harbour seal prey fish. Potential wild intermediate fish hosts from the North Sea were dissected and found to harbour larval nematodes. Histological examination and in-situ hybridisation of tissue samples from these fish showed lungworm larvae within the intestinal wall. Based on larval ITS-2 nucleotide sequences, larval nematodes were identified as Pseudalius inflexus and Parafilaroides gymnurus. Turbot (Psetta maxima) bred and raised in captivity were experimentally infected with live L1s of Otostrongylus circumlitus and ensheathed larvae were recovered from the gastrointestinal tract of turbot and identified using molecular tools. Our results show that fish intermediate hosts play a role in the transmission of metastrongyloid nematodes of harbour porpoises and harbour seals.     

Modelling the dynamics of senescence spread

Cellular senescence is a cell surveillance mechanism that arrests the cell cycle in damaged cells. The senescent phenotype can spread from cell to cell through paracrine and juxtacrine signalling, but the dynamics of this process are not well understood. Although senescent cells are important in ageing, wound healing and cancer, it is unclear how the spread of senescence is contained in senescent lesions. In the absence of the immune system, senescence could theoretically spread infinitely from one cell to another, but this contradicts experimental evidence. To investigate this issue, we developed both a minimal mathematical model and a stochastic simulation of senescence spread. Our results suggest that differences in the number of signalling molecules secreted between subtypes of senescent cells can limit the spread of senescence. We found that dynamic, time-dependent paracrine signalling prevents the uncontrolled spread of senescence, and we demonstrate how model parameters can be determined using Bayesian inference in a proposed experiment.     

Prevalence of antibodies against canine distemper virus among red foxes in Luxembourg

Canine distemper virus (CDV) has a wide host spectrum, and during the past years, distemper has been observed in species that were previously not considered to be susceptible. In this study, we investigated the prevalence of CDV-specific antibodies in red foxes (Vulpes vulpes) sampled between May and November 1997. About 9 to 13% of the Luxembourg red fox population is positive for antibodies against CDV. Thus a sizeable proportion of red foxes has been exposed to CDV in the wild. The significance of CDV in red foxes is discussed.