- Email: [email protected]
Phocine distemper virus in the North and European Seas – Data and models, nature and nurture
B I O L O G I CA L C O N S E RVAT I O N
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/biocon
Phocine distemper virus in the North and European Seas – Data and models, nature and nurture Ailsa J. Halla,*, Paul D. Jepsonb, Simon J. Goodmanc, Tero Ha¨rko¨nend a
Sea Mammal Research Unit, Gatty Marine Laboratory, University of St Andrews, St Andrews, Fife KY16 8LB, UK Institute of Zoology, Zoological Society of London, Regents Park, London NW1 4RY, UK c Institute of Integrative and Comparative Biology, Faculty of Biology, University of Leeds, Leeds LS2 9JT, UK d Swedish Museum of Natural History, Box 50007, S-10405 Stockholm, Sweden b
A R T I C L E I N F O
A B S T R A C T
Available online 5 June 2006
Two outbreaks of phocine distemper have severely affected harbour seal (Phoca vitulina) populations in European and UK waters. The first occurred in 1988 when the causative
Keywords:
virus was identified as a new member of the genus morbillivirus. The second outbreak in
Harbour seal
2002 was first detected on the same Danish Island of Anholt and involved similar popula-
Epidemic
tions and geographical locations. However, despite the obvious similarities between the
Mathematical modelling
epidemics, differences in viral transmission and case mortality were found. Harbour seals
Disease
are highly susceptible to infection while sympatric grey seals (Halichoerus grypus) are resis-
Infection
tant but could be important asymptomatic carriers of the disease. Arctic phocid seals
PDV
remain the most likely source of the virus and grey seals could be the link between these primary hosts and the harbour seal populations further south. Future epidemiological models should therefore consider including multiple host species. The future conservation and management of harbour seal populations vulnerable to PDV relies on the ability to accurately predict the long-term impact on population abundance and distribution. Although knowledge about the behaviour and pathogenesis of the virus has increased substantially and data on host movements and contact rates are accumulating, studies into the determinants of the host range have lagged behind. The development of more realistic epidemiological models should be combined with studies into the factors controlling species and individual susceptibility. Assessing the risk of infection to endangered but currently unexposed potential host species (such as the Hawaiian monk seal, Monachus schauinslandi) is essential for guiding potential conservation management options, such as vaccination. Ó 2006 Elsevier Ltd. All rights reserved.
1.
Introduction
Phocine distemper virus (PDV) emerged as a devastating disease among harbour seals in Northern European and UK coastal waters in 1988 (Kennedy et al., 1988; Osterhaus and Vedder, 1988), causing catastrophic declines in many popula-
tions (Dietz et al., 1989; Hall et al., 1992a; Hall, 1995; Ha¨rko¨nen and Heide-Jørgensen, 1990; Heide-Jørgensen and Ha¨rko¨nen, 1992a). Over the six-month period beginning in April, more than 18,000 carcasses washed up along the shores of Europe and the UK (Fig. 1a, Dietz et al., 1989; Heide-Jørgensen et al., 1992b). PDV is a member of the genus morbillivirus within
* Corresponding author: Tel.: +44 1334 462630; fax: +44 1334 462632. E-mail addresses: [email protected] (A.J. Hall), [email protected] (P.D. Jepson), [email protected] (S.J. Goodman), [email protected] (T. Ha¨rko¨nen). 0006-3207/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2006.04.008
222
B I O L O G I C A L C O N S E RVAT I O N
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
Fig. 1 – Maps showing the temporal and spatial spread of (a) the 1988 epidemic and (b) the 2002 epidemic from Anholt in the Kattegat to UK and Irish waters. The dotted line indicates that the disease did not reach epidemic proportions in Scotland or Northern Ireland, despite PDV seal deaths being found in many regions (shown by the black circles).
the Paramyxoviridae family that causes a severe respiratory and systemic infection in its host and has a high case fatality rate (Harder et al., 1990). In 2002 the disease re-emerged causing a second major outbreak (Jensen et al., 2002), affecting largely the same populations over a similar geographical area (Fig. 1b), with roughly the same epidemic duration and population impacts (more adult males than other sex-age groups were infected) (Ha¨rko¨nen et al., 2006). However, there were differences between the timing of the two epidemics and wide geographical variations in mortality rates. Comparing the two outbreaks may therefore provide important clues as to the nature, origin and enduring impact of the virus.
Information about the PDV virus itself has increased greatly over the last 17 years. The genes encoding for many of the major viral proteins have been sequenced (Curran et al., 1992; Curran et al., 1990; Curran and Rima, 1992; McIlhatton et al., 1997). Knowledge of the pathogenesis and aetiology of the disease and its potential sequelae has been obtained from detailed pathological studies of affected animals (Baker, 1992; Kennedy et al., 1989; Schumacher et al., 1990). However, information about the movements, distribution and population dynamics of its harbour seal host on a wide geographical scale have only recently been reported (Brasseur and Fedak, 2003; Ha¨rko¨nen et al., 1999; Ries et al., 1999).
B I O L O G I C A L C O N S E RVAT I O N
In 1988, the size of many of the harbour seal populations first affected was unknown, thus population counts pre and post-epidemic comparison were only available in a few cases (Heide-Jørgensen and Ha¨rko¨nen, 1988; Heide-Jørgensen et al., 1992c; Thompson et al., 2005; Thompson and Miller, 1992). Indeed, the number of carcasses that washed ashore at some sites exceeded the then current regional population estimate (Dietz et al., 1989). Carcass counts were therefore not a reliable method for estimating mortality from PDV. In areas where harbour seal carcasses were washed onto amenity beaches or where haul out sites were regularly monitored, remains for scientific study were recovered (Hall et al., 1992b; Heide-Jørgensen and Ha¨rko¨nen, 1992a). Although these samples were used to estimate sex and age-related mortality, they could be biased depending on the location and season. Thus the impact of the outbreak could only be determined in those areas where seal counts were available from boat or aerial surveys (Heide-Jørgensen et al., 1992b). With long-term monitoring of harbour seal populations established in 1988 (Ha¨rko¨nen et al., 2002; Ries et al., 1998; Thompson et al., 2005; Thompson et al., 2001), the impact of the PDV outbreak in 2002 could be estimated more accurately (Ha¨rko¨nen et al., 2006). Using a simple compartmental mathematical model, Grenfell et al. (1992) suggested that the viral transmission rate (the transmission coefficient, b) during the 1988 epidemic was probably sufficient for the infection to die out in the Northern European harbour seal populations following the first outbreak. With herd immunity conferred by the acquired immune response to the virus, which for morbilliviruses is usually life-long, they suggested a second outbreak following reintroduction of the virus was unlikely to cause an outbreak on the same scale for at least 10 years. In reality the inter-epidemic period was 14 years. There is now sufficient abundance and distribution data over time to model the dynamics of the virus and its epidemiology at different temporal and spatial scales (Harding et al., 2002; Ha¨rko¨nen, T., personal communication; Lonergan, M., personal communication; Swinton et al., 1999; Swinton et al., 1998). For example, recent studies using mathematical models to focus on the long-term population consequences and risk of quasi-extinction (i.e. the risk of a serious decline in the size of a population) for harbour seals (Harding et al., 2002; Harding et al., 2003; Lonergan and Harwood, 2003) have established that populations with low or variable rates of increase are very vulnerable to serious decline following future PDV outbreaks. However, estimating the risk of quasi-extinction for rapidly growing populations is more difficult (Ha¨rko¨nen et al., 2006). Assumptions regarding levels of immunity, the variance in the population growth and the action of density dependence all have substantial effects on quasi-extinction probabilities in this case (Lonergan and Harwood, 2003). Some of the European harbour seal populations experienced very high population growth rates following the first PDV epidemic; for example the Wadden sea population was increasing at about 9% per annum before the 1988 epidemic, but at 13% between 1989 and 2000 (Ha¨rko¨nen, 2003; Reijnders et al., 1997). However, Harding et al. (2003) concluded that the cumulative effect of recurrent epidemics with mortality rates similar to those seen in 1988 and 2002, even for popula-
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
223
tions with relatively high growth rates between outbreaks, may limit the size of those populations. Despite the progress in monitoring and epidemiological modelling, fundamental information on host movements to estimate contact rate between infective and susceptible hosts is still lacking. PDV is probably endemic in the Arctic phocid seals, such as the harp (Phoca groenlandica) and hooded seals (Cystophora cristata). Serological surveys have found antibody prevalence rates of over 90% for some populations of these species (Duignan et al., 1997; Markussen and Have, 1992; Stuen et al., 1994) although age-specific prevalence data are not available. The sympatric and widely distributed grey seal is potentially a key carrier of infection both between populations and perhaps species (Hammond et al., 2005; Pomeroy et al., 2005) and may be the link between PDV’s putative Arctic primary hosts (Ha¨rko¨nen et al., 2006) and the more southerly populations of harbour seals. Harbour seals are a listed species in the European Habitats Directive (Directive 92/43/EEC on the conservation of natural habitats and of wild flora and fauna) and signatory States are required to set up Special Areas of Conservation (SAC) that are monitored and protected such that a favourable conservation status for the species is ensured. Estimating the impact that PDV may have on harbour seal population dynamics is part of this obligation. But what ecological, epidemiological and individual factors influence the long-term risks of recurrent epidemics? What data are still required to realistically model the dynamics of phocine distemper? In this paper we explore these questions and discuss the potential conservation implications both for the European harbour seal and for endangered seal species not currently exposed to the virus, such as the Hawaiian monk seal.
2. Ecological and epidemiological factors affecting the risk of recurrent epidemics Serological surveys (measuring levels of morbillivirus specific antibodies in the blood of surviving seals) are a key method for determining the proportion of exposed and immune individuals within a population. Individuals sampled from the Scottish harbour seal populations at the start of the outbreak in 2002 suggested that between only 3% and 9% had protective titres (compared to over 70% in 1989) and that the disease could potentially spread rapidly in Scotland once introduced (Thompson et al., 2002). However, the proportion of apparently seronegative individuals that had actually been exposed and were thus immune is not known. There was no significant outbreak of PDV in Scotland in 2002 (Ha¨rko¨nen et al., 2006) and even in 1988 only the Moray Firth population was obviously affected (Thompson and Miller, 1992). Relatively high seal mortality was reported in Orkney based on carcass reports in 1988 (Hall et al., 1992a), but it is thought this reflects mortality in grey seals, particularly pups, as only 151/601 carcasses were confirmed to be harbour seals (SMRU unpublished). It remains puzzling that the epidemic did not spread through the Scottish harbour seal populations in 2002. There were clearly sufficient susceptible individuals within the population and Scotland has approximately 86% of the UK’s
224
B I O L O G I C A L C O N S E RVAT I O N
36,000 harbour seals (SMRU unpublished). The restricted movements of infected individuals, either into the population from elsewhere or within sub-populations, are a potential explanatory factor. One of the central parameters in modelling the spread of an epidemic is R0, defined as the average or expected number of secondary cases produced by each primary infectious individual. If R0 is greater than one then an infectious disease is likely to spread within the population (Grenfell and Dobson, 1995). The size of R0 is affected by contact rates within the population. Estimates of contact rates (from combining a simple compartmental epidemic model with serological data) for Scotland were approximately 1.5– 1.9 for 1988 and 1.2–1.3 for 2002 (Lonergan, M., personal communication). Although these rates were significantly lower in the Scottish populations than in the southeastern English population in 1988, this was not the case in 2002 with similar estimates produced for contact rates in both areas. In addition while mortality among UK harbour seals was highest in southeastern England during both outbreaks, it was significantly lower in 2002 than in 1988 (53% in 1988 and 22% in 2002; Thompson et al., 2005). It therefore appears that although disease transmission was similar throughout the UK in 2002, case mortality from PDV was highly variable among sub-populations.
3.
Movement and dispersal
Information on the movements of seals is necessary, both within and between populations, for the accurate estimation of R0. Some data on harbour seal movements has been obtained using flipper tagging (Thompson et al., 1994), freeze branding (Ha¨rko¨nen et al., 1999), radio-telemetry (Ries et al., 1998; Thompson, 1989) and satellite relay dataloggers (SRDLs) (Brasseur and Fedak, 2003). Whilst many harbour seals remain in well-defined foraging areas and haulout at the same locations, some do make long movements away from the coast, venturing to new haulout sites (Brasseur and Fedak, 2003). The frequency of this behaviour appears to vary by location. For example, 45/45 harbour seals fitted with SRDLs in the Wash (east England) and St Andrews Bay (east Scotland) remained at these haulout sites, whereas 1/15 tagged in Orkney and Shetland and 2/5 tagged in the Moray Firth moved to distant sites (Sharples, R. and Hammond, P.S. personal communication). There is currently a major effort to obtain movement data for all the European populations so that a collective spatially explicit model can be constructed (Ha¨rko¨nen, T., personal communication). Grey seals are probably asymptomatic carriers of PDV (Pomeroy et al., 2005; Hammond et al., 2005) but more information on the interaction between harbour seals and sympatric grey seals is needed, especially at mixed haulout sites. A large body of data now exists on the large-scale movements and foraging behaviour of grey seals in the North Sea (Matthiopoulos et al., 2004; McConnell et al., 1999). Again most foraging trips return to the same haulout but relocation to a distant haulout site is more frequent than in harbour seals. However, the movements of both harbour and grey seals from the same haulout sites have not been monitored simultaneously.
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
Goodhart (1988) suggested that PDV is endemic in harp seals and was introduced to the harbour seals following the massive 1987 harp seal invasion into the southern Norwegian Sea. However, there are some discrepancies in the evidence to support this theory. The last harp seal was seen in Norwegian waters in May 1987 (Markussen and Have, 1992), almost one year before the first outbreak and none were seen around Anholt (Denmark) where both outbreaks were first detected. In addition, no similar invasion occurred in 2001. An alternative simple explanation is that grey seals, that do haulout on Anholt (Ha¨rko¨nen et al., in press), could have been the carrier of PDV between Arctic seals (that regularly forage in the northern North Sea) (Folkow et al., 1996) and harbour seals in both outbreaks. However, it is a surprise that, if grey seals are the source, the second epidemic did not start at other mixed haulouts, such as in the Wadden Sea. Perhaps the clue here is in the regularity and stability of an individual’s movements. If grey seals travelling between northern Norway and Danish waters are more likely to come into contact with infected harp seals and susceptible harbour seals, this may account for the epidemic point source being on Anholt rather than elsewhere. Since SRDL tags attached to the fur of the seals are shed during the moult and therefore last a maximum of 12 months, there are no data to test this hypothesis. Whatever the explanation, PDV in UK and other European seals must be considered as a two or three host system, which will add considerably complexity to the mathematical models needed and to the data required for their parameterisation. At the finer spatial and temporal scales there is little understanding of the social interactions that characterize the contact pattern between infected and susceptible seals, both within and between species. This social and behavioural aspect to the modelling of disease outbreaks in humans and domestic species is now receiving more widespread attention (Eubank et al., 2004). The PDV models constructed to date have assumed uniform mixing for the contact process (De Koeijer et al., 1998; Grenfell et al., 1992), but this may be too simplistic. The social or network structure of a population, which is expected to show temporal variations (Ha¨rko¨nen and Harding, 2001), will influence disease dynamics. This structure means that each individual has a finite set of contacts to which they can pass infection, known as a ‘‘mixing network’’ (Keeling and Eames, 2005). The characteristics of the mixing network, and how it differs from random mixing have become important concerns in applied epidemiology. A proposed novel approach to quantifying population network structure in seals uses telemetry devices known as node-tags (McConnell et al., 2003). The tags, deployed on individual seals, would record the proximity of other tagged seals within a specified range. When another tag was encountered its identification would be swapped with its neighbour and stored in memory. In addition to the current encounter occasion, individual encounter histories would also be swapped. The tags would thus accrue histories for those segments of the network with which they have had direct or indirect contact and these data would be relayed ashore through a number ‘portal’ tags within the network. While there are some statistical modelling and technological issues to be addressed, this innovative scheme has the potential to estimate the individual contact rates between and within sympatric
B I O L O G I C A L C O N S E RVAT I O N
species, both on land and at sea, and enable the spread of PDV more accurately estimated. Following the first PDV outbreak there was interest in the influence of global warming. Europe appears to be warming faster than the global average (Crowley, 2000) and projections suggest this may continue to increase (Parry, 2000). The hypothesis proposed was that higher ambient temperatures would increase the time harbour seals spend hauled out on land and increase the probability of viral transmission (Lavigne and Schmitz, 1990). However, observations suggest that harbour seals become heat stressed during warm days, resulting in decreased numbers of animals on land (Harwood and Grenfell, 1990; Pauli and Terhune, 1987; Watts, 1996). Climate change could, nevertheless still affect the spread of PDV through changes in prey availability of the reservoir and target hosts. If Arctic capelin stocks (whose crash in 1987 preempted the southward migration of harp seals) were affected this could bring about considerable seal species overlaps, increasing direct contact between infected and susceptible individuals. In addition, environmental change may cause pathogens to shift to new and unexpected hosts. For example, a recent study in Lake Baikal, where Baikal seals (Phoca sibirica) have suffered recurrent outbreaks of canine distemper (CDV), found two species of molluscs to be infected with CDV, confirmed by RT-PCR and passaged through ferrets resulting in acute respiratory infection (Kondratov et al., 2003). This isolated report raises the possibility of non-mammalian PDV reservoirs.
4.
Individual factors
A number of studies have indicated that host genetic diversity plays an important role in buffering populations against widespread epidemics (Altizer et al., 2003). Loci that could potentially be involved in disease resistance include those that directly mediate the immune response (e.g. major histocompatibility complex (MHC) class I and class II; (McClelland et al., 2003; Paterson et al., 1998)), genes for proteins that regulate the immune response such as cytokines or genes encoding for cell receptors that a virus uses to infect cells (Samson et al., 1996). Theoretical models combining epidemiology and population genetics demonstrate that the selection pressure exerted by repeated epidemics with high mortality can drive the rapid evolution of genetic disease resistance over short evolutionary timescales (Galvani and Slatkin, 2004; Harding et al., 2005). In a model of disease resistance evolution, parameterised specifically for recurrent PDV epidemics in a harbour seal population, Harding et al. (2005) show that a disease resistance allele can be pushed from an initial frequency of 1% to 50% in 120 years (16 generations) with a 15 year epidemic interval (eight epidemics). Indeed, they predict that rapid increases in the resistant allele frequency would be seen after just four outbreaks. Therefore even moderate exposure to PDV in the historical past could have selected for disease resistance in exposed populations. However, some of the assumptions under this model might require further testing. A genetic study of European harbour seal populations using microsatellites (neutral nuclear genetic markers) showed the population to be highly structured, which would allow for the differential distribution of alleles that contribute
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
225
to disease susceptibility (Goodman, 1998). However, the results obtained so far do not support simple explanations for genetic associations with phocine distemper mortality. For example, genetic impoverishment of the more severely affected populations was not supported. Indeed, some populations with high mortality had some of the highest levels of genetic variation in the North Sea (Goodman, 1998). Sequence variation at MHC class I loci also appears to be comparable to other carnivores (Goodman, 1995). Genetic associations with PDV susceptibility are likely to be more subtle and will require further investigation of variation at a population level for the types of candidate genes described above. Such work is already feasible using recently developed genomics tools that can be applied to seals. Serological studies have shown widespread exposure to PDV among UK grey seals in both 1988 and 2002 (Harwood et al., 1989; Pomeroy et al., 2005) but no fatal cases of phocine distemper were found in the UK (Jepson, P., personal communication) and only very few unsubstantiated cases have been reported in Germany and Estonia (Ha¨rko¨nen et al., 2006). The main cause of death from PDV is often secondary bacterial infection due to viral immunosuppression and the virus replicates in the lymphoid organs of the body (Baker and Ross, 1992). A membrane glycoprotein known as signalling lymphocyte activation molecule (SLAM, also known as CD150) was found to be the cellular receptor for measles virus in humans (Tatsuo et al., 2000) and a similar molecule was also found to be a receptor for CDV in dogs and RPV in cattle (Tatsuo et al., 2001). Since the expression of specific cellular receptors is one of the major determinants of the host range for a virus (Tatsuo et al., 2001) the first stage in identifying the PDV host range would be to determine the presence of SLAMs in seals (and cetaceans). Although Tatsuo et al. (2001) predict most, if not all, morbilliviruses use SLAMs this needs to be confirmed. Further investigations into the genes encoding these receptors and the frequency of the alleles in different harbour seal populations links back to the potential importance of genetic variability in determining host resistance. For example, in humans population variation in mutant alleles of the gene encoding the chemokine receptor CCR5 provides homozygotes with a strong resistance against infection by HIV; Libert et al. (1998). This is also of particular concern for endangered and threatened species not currently exposed to PDV, such as the Hawaiian monk seal. Although PDV has not yet reached the Pacific Ocean if, or when, it does it is important to know whether this species is at risk of infection. Although PDV was identified as the cause of a mass mortality in the endangered Mediterranean monk seal (Monachus monachus) in 1997 (Osterhaus et al., 1997), phycotoxins from the ingestion of contaminated fish following an algal bloom were also reported as the cause of this die-off (Herna´ndez et al., 1998) and the ultimate cause of mortality remains open to debate (Harwood, 1998). Other mechanisms may govern the host range in morbilliviruses. Alpha/beta interferons (IFN-a/b) are key antiviral cytokines involved in inhibiting viral replication. Exposure of cells to IFN-a/b quickly establishes an antiviral state that blocks cytopathic and degenerative effects (Parisien et al., 2002). Paramyxoviruses can block IFN-a/b signalling, preventing the cell from establishing an antiviral state but this may
226
B I O L O G I C A L C O N S E RVAT I O N
be species specific. For example simian virus 5 (SV5) anatagonizes IFN-a/b in primate cells but not mouse cells. In mouse cells SV5 is unable to block IFN-a/b antiviral responses, which leads to most cells surviving infection and clearing the virus. Indeed, differences in the intracellular signalling protein STAT2 between primates and mice ultimately determine this response. Cell surface interactions are the primary molecular determinants of species specificity for viral infection and identification of these mechanisms will indicate which hosts are vulnerable. Thus understanding variability at the molecular level has direct application to conservation management decisions, particularly those that need to assess the infection risk in currently unexposed species. The potential interactions between PDV and immunosuppressive environmental contaminants as further determinants of the observed mortality patterns within species during both outbreaks have been dealt with extensively elsewhere (DeSwart et al., 1994; Hall et al., 1992b; Reijnders and Aguilar, 2002; Ross et al., 1995). However, increasing evidence, from both in vitro and in vivo studies, suggest there are species differences in the immunosuppressive effects of organochlorine (OC) contaminants, with grey seals being relatively resistant compared to harbour seals. The most compelling evidence for an effect of contaminants on harbour seal immunity was reported following an experiment in captivity. Immune function in a group of harbour seals fed fish with high concentrations of various OC contaminants was compared to a control group (De Swart et al., 1996; Ross et al., 1995). Immunity was found to be depressed in the contaminant fed group, particularly natural killer (NK) cell activity and proliferative lymphocyte responses after stimulation, suggesting an impaired T cell function. These functions are known to be important in the clearance of virus infections (Finberg and Benacerraf, 1981). A recent in vitro study (Hammond et al., 2005) compared the effects of polychlorinated biphenyl (PCB) exposure on innate immunity in harbour and grey seals. Phagocytic activity of harbour seal leukocytes was decreased at exposure levels of 3 and 30 ng ml 1 but there was no effect on grey seal leukocytes. Similarly respiratory burst activity was decreased in harbour seals at the higher exposure level but not in the grey seals. In addition, there was no significant relationship between lactational exposure to PCBs and infection or reduced immunity in grey seal pups born at the Isle of May in the Firth of Forth, Scotland (Hall et al., 1997). Harbour seals in the Wadden Sea experienced some of the highest exposure levels of OC contaminants in Europe (Reijnders, 1980) and it was hypothesised that the 1988 PDV epidemic selected against those seals with the highest contaminant loads. The significantly higher population growth rate following the outbreak (Reijnders et al., 1997) coupled with the reduced levels of contaminants in the surviving population might support this view (Aguilar et al., 2002) although other explanations are equally plausible such as density dependent effects. Interestingly, whilst the levels of OC contaminants in the Wadden Sea harbour seals have decreased by 50–65%, those in the blubber of harbour seals in southeastern England (the Wash) have decreased by less than 10% over the same 14 year period, and the concentrations in the seals that died of PDV in 2002 were significantly
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
higher than the survivors (Hall, unpublished). It therefore remains important to determine how the molecular mechanisms involved in contaminant immunosuppression and susceptibility are related to those determining viral susceptibility.
5.
Conservation and management
PDV remains a threat to the conservation of European harbour seals and more realistic epidemiological models are required to inform conservation management decisions, particularly within the harbour seal SACs. It has been asserted that although ‘‘all models are wrong, some models are useful’’ (Box, 1979). While it is highly unlikely that a future PDV outbreak could be prevented, predicting the impact and spread is important, particularly for the development of contingency plans and carcasses collection strategies. Risk assessment models that also incorporate interactions with anthropogenic factors, such as environmental contaminants, will indicate where efforts to reduce exposures should be directed. Although knowledge about the behaviour and pathogenesis of the virus has increased substantially between outbreaks, studies into the determinants of the host range and individual susceptibility have lagged behind. Yet assessing the risk of infection to threatened or endangered but currently unexposed species is essential to determine the efficacy of practical conservation management options (such as vaccination or relocation). Such measures are costly and logistically difficult to implement and are further reason for the continued refinement of PDV epidemiological models.
Acknowledgements The authors would like to thank Bernie McConnell, John Harwood and Catriona Stephenson for their valuable and constructive comments on this manuscript and the anonymous referees for their very helpful additional suggestions.
R E F E R E N C E S
Aguilar, A., Borrell, A., Reijnders, P.J.H., 2002. Geographical and temporal variation in levels of organochlorine contaminants in marine mammals. Mar. Environ. Res. 53, 425–452. Altizer, S., Harvell, D., Friedle, D., 2003. Rapid evolutionary dynamics and disease threats to biodiversity. TREE 18, 589–596. Baker, J.R., 1992. The pathology of phocine distemper. Sci. Tot. Environ. 115, 1–7. Baker, J.R., Ross, H.M., 1992. The role of bacteria in phocine distemper. Sci. Tot. Environ. 115, 9–14. Box, G.P., 1979. Robustness in the strategy of scientific model building. In: Launer, R.L., Wilkinson, G.N. (Eds.), Statistics. Academic Press, New York. Brasseur, S.M., Fedak, M., 2003. Habitat use of seals in relation to recreation, fisheries and large intra-structural works. Management of North Sea Harbour and Grey Seal Populations. Common Wadden Sea Secretariat, Ecomare, Texel, Netherlands. pp. 27–33. Crowley, T.J., 2000. Causes of climate change over the past 1000 years. Science 289, 270–277.
B I O L O G I C A L C O N S E RVAT I O N
Curran, M.D., Rima, B.K., 1992. The genes encoding the phosphoproteins and matrix proteins of phocine distemper virus. J. Gen. Virol. 73, 1587–1591. Curran, M.D., Oloan, D., Rima, B.K., Kennedy, S., 1990. Nucleotide-sequence analysis of phocine distemper virus reveals its distinctness from canine-distemper virus. Vet. Rec. 127, 430–431. Curran, M.D., Lu, T.J., Rima, B.K., 1992. The fusion protein gene of phocine distemper virus—nucleotide and deduced amino-acid-sequences and a comparison of morbillivirus fusion proteins. Arch. Virol. 126, 159–169. De Koeijer, A., Diekmann, O., Reijnders, P.J.H., 1998. Modelling the spread of phocine distemper virus among harbour seals. Bull. Math. Biol. 60, 585–596. DeSwart, R.L., Ross, P.S., Vedder, L.J., Timmerman, H.H., Heisterkamp, S., Van Loveren, H., Vos, J.G., Reijnders, P.J.H., Osterhaus, A.D.M.E., 1994. Impairment of immune function in harbor seals (Phoca vitulina) feeding on fish from polluted waters. Ambio 23, 155–159. De Swart, R.L., Ross, P.S., Vos, J.G., Osterhaus, A.D., 1996. Impaired immunityin harbour seals (Phoca vitulina) exposed to bioaccumulated environmental contaminants: review of a long-term feeding study. Environ. Health Perspect. 104, 823–828. Dietz, R., Heide-Jørgensen, M-P., Ha¨rko¨nen, T., 1989. Mass deaths of harbor seals (Phoca vitulina) in Europe. Ambio 18, 258–264. Duignan, P.J., Nielsen, O., House, C., Kovacs, K., Duffy, N., Early, G., Sadove, S., St Aubin, D.J., Rima, B.K., Geraci, J.R., 1997. Epizootiology of morbillivirus infection in harp, hooded and ringed seals from the Canadian Arctic and western Atlantic. J. Wild. Dis. 33, 7–19. Eubank, S., Guclu, H., Kumar, V.S., Marathe, M.V., Srinivasan, A., Toroczkai, Z., Wang, N., 2004. Modelling disease outbreaks in realistic urban social networks. Nature (London) 429, 180–184. Finberg, R., Benacerraf, A., 1981. Induction, control and consequences of virus specific cytotoxic T cells. Immunol. Rev. 58, 157–180. Folkow, L.P., Martensson, P-E., Blix, A.S., 1996. Annual distribution of hooded seals (Cystophora cristata) in the Greenland and Norwegian seas. Polar Biol. 16, 179–189. Galvani, A.P., Slatkin, M., 2004. Intense selection in an age-structured population. Proc. Biol. Sci. 271, 171–176. Goodhart, C.B., 1988. Did virus transfer from Harp seals to commons seals? Nature (London) 336, 21. Goodman, S.J. 1995. Molecular population genetics of the European harbour seal (Phoca vitulina) in relation to the 1988 Phocine Distemper Virus epizootic. PhD Thesis, University of Cambridge, Cambridge, UK. Goodman, S.J., 1998. Patterns of extensive genetic differentiation and variation among European harbor seals (Phoca vitulina vitulina) revealed using microsatellite DNA polymorphisms. Mol. Biol. Evol. 15, 104–118. Grenfell, B., Dobson, A., 1995. Ecology of Infectious Diseases in Natural Populations. Cambridge University Press, Cambridge. Grenfell, B.T., Lonergan, M.E., Harwood, J., 1992. Quantitative investigations of the epidemiology of phocine distemper virus (PDV) in European common seal populations. Sci. Tot. Environ. 115, 15–29. Hall, A.J., 1995. Morbilliviruses in marine mammals. Trends Microbiol. 3, 4–9. Hall, A.J., Pomeroy, P., Harwood, J., 1992a. The descriptive epizootiology of phocine distemper in the UK during 1988/89. Sci. Tot. Environ. 115, 31–44. Hall, A.J., Law, R.J., Wells, D.E., Harwood, J., Ross, H.M., Kennedy, S., Allchin, C.R., Campbell, L.A., Pomeroy, P.P., 1992b. Organochlorine levels in common seals (Phoca vitulina) that were victims and survivors of the 1988 phocine distemper epizootic. Sci. Tot. Environ. 115, 145–162.
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
227
Hall, A.J., Pomeroy, P., Green, N., Jones, K., Harwood, J., 1997. Infection, haematology and biochemistry in grey seal pups exposed to chlorinated biphenyls. Mar. Environ. Res. 43, 81–98. Hammond, J.A., Hall, A.J., Dyrynda, L., 2005. Comparison of polychlorinated biphenyl (PCB) induced effects on innate immune functions in harbour and grey seals. Aquat. Toxicol. 74, 126–138. Hammond, J.A., Pomeroy, P., Hall, A.J., Smith, V.J., 2005. Identification and real-time PCR quantification of phocine distemper virus from two colonies of Scottish grey seals in 2002. J. Gen. Virol. 86, 2563–2567. Harder, T., Willhaus, T., Frey, H-R., Liess, B., 1990. Morbillivirus infection of seals during the 1988 epidemic in the Bay of Heligoland: III Transmission studies of cell culture-propogated phocine distemper virus in harbour seals and a grey seal: clinical, virological and serological results. J. Vet. Med. B 37, 641–650. Harding, K.C., Ha¨rko¨nen, T., Caswell, H., 2002. The 2002 European seal plague: epidemiology and population consequences. Ecol. Lett. 5, 727–732. Harding, K.C., Ha¨rko¨nen, T., Pineda, J., 2003. Estimating quasi-extinction risk of European harbour seals: reply to Lonergan and Harwood 2003. Ecol. Lett. 6, 894–897. Harding, K.C., Hansen, B., Goodman, S., 2005. Acquired immunity and stochasticity in epidemic intervals impede the evolution of host disease resistance. Am. Nat. 166, 722–730. Ha¨rko¨nen, T., 2003. Development of populations of harbour seals and grey seals in the Wadden Sea and the North Sea since 1988. Management of North Sea Harbour and Grey Seal Populations. Common Wadden Sea Secretariat, Ecomare, Texel, Netherlands. pp. 13–17. Ha¨rko¨nen, T., Harding, K.C., 2001. Spatial structure of harbour seal populations and the implications thereof. Can. J. Zool. 79, 2115–2127. Ha¨rko¨nen, T., Heide-Jørgensen, M-P., 1990. Short-term effects of the mass dying of Harbour seals in the Kattegat-Skagerrak area during 1988. Z. Saugetierkunde 55, 233–238. Ha¨rko¨nen, T., Harding, K.C., Lunneryd, S.G., 1999. Age- and sex-specific behaviour in harbour seals Phoca vitulina leads to biased estimates of vital population parameters. J. Appl. Ecol. 36, 825–841. Ha¨rko¨nen, T., Harding, K.C., Heide-Jørgensen, M-P., 2002. Rates of increase in age-structured populations: a lesson from the European harbour seals. Can. J. Zool. 80, 1498–1510. Ha¨rko¨nen, T., Dietz, R., Reijnders, P.J.H., Teilmann, J., Thompson, P.M., Harding, K., Hall, A.J., Brasseur, S.M.J.M., Siebert, U., Goodman, S., Jepson, P., Dau Rasmussen, T., 2006. A review of the 1988 and 2002 phocine distemper virus epidemics in European harbour seals. Dis. Aquat. Org. 68, 115–130. Ha¨rko¨nen, T., Brasseur, S.M., Teilmann, J., Vincent, C., Dietz, R., Abt, K., Reijnders, P.J.H., in press. Status of grey seals along mainland Europe from the Southwestern Baltic to France. NAMMCO Scientific Publications. Harwood, J., 1998. What killed the monk seals? Nature, (London) 393, 17–18. Harwood, J., Grenfell, B., 1990. Long-term risks of recurrent seal plagues. Mar. Pollut. Bull. 21, 284–287. Harwood, J., Carter, S.D., Hughes, D.E., Bell, S.C., Baker, J.R., Cornwell, H.J.C., 1989. Seal disease predictions. Nature (London) 339, 670. Heide-Jørgensen, M.-P., Ha¨rko¨nen, T., 1988. Rebuilding seal stocks in the Kattegat-Skagerrak. Mar. Mamm. Sci. 4, 231–246. Heide-Jørgensen, M.P., Ha¨rko¨nen, T., 1992a. Epizootiology of the seal disease in the Eastern North-Sea. J. Appl. Ecol. 29, 99–107. Heide-Jørgensen, M.-P., Ha¨rko¨nen, T., Dietz, R., Thompson, P., 1992b. Retrospective of the 1988 European seal epizootic. Dis. Aquat. Org. 13, 37–62.
228
B I O L O G I C A L C O N S E RVAT I O N
Heide-Jørgensen, M.P., Ha¨rko¨nen, T., Aberg, P., 1992c. Long-term effects of epizootic in harbor seals in the Kattegat-Skagerrak and adjacent areas. Ambio 21, 511–516. Herna´ndez, M., Robinson, I., Aguilar, A., Gonzalea, L.M., Lopez-Jurado, L.F., Reyero, M.I., Cacho, E., Franco, J., Eduardo Costas, V.L-R., 1998. Did algal toxins cause monk seal mortality? Nature, (London) 393, 28–29. Jensen, T., van de Bildt, M., Dietz, H., Andersen, T., Hammer, A., Kuiken, T., Osterhaus, A.D.M.E., 2002. Another phocine distemper outbreak in Europe. Science 297, 209. Keeling, M., Eames, K., 2005. Networks and epidemic models. J. R. Soc. Interf. 2, 295–307. Kennedy, S., Smyth, J.A., McCullough, S.J., Allan, G.M., McNeilly, F., McQuaid, S., 1988. Confirmation of cause of recent seal deaths. Nature (London) 335, 404. Kennedy, S., Smythe, J.A., Cush, P.F., Duignan, P., Platten, M., McCullough, S.J., Allan, G.M., 1989. Histopathologic and immunocytochemical studies of distemper in seals. Vet. Pathol. 26, 97–103. Kondratov, I.G., Denikina, N.N., Belikov, S.I., Durymanova, A.A., Ustinova, E.N., Shestopalov, A.M., 2003. Mollusks as a natural reservoir of morbilliviruses. Doklady Biol. Sci. 389, 154–156. Lavigne, D.M., Schmitz, O.J., 1990. Global warming and increasing population densities: a prescription for seal plagues. Mar. Pollut. Bull. 21, 280–284. Libert, F., Cochaux, F.P., Beckman, G., Samson, M., Aksenova, M., Cao, A., Czeizel, A., Claustres, M., de la Rua, C., Ferrari, M., Ferrec, C., Glover, G., Grinde, B., Guran, S., Kucinskas, V., Lavinha, J., Mercier, B., Ogur, G., Peltonen, L., Rosatelli, C., Schwartz, M., Spitsyn, V., Timar, L., Beckman, L., Parmentier, M., Vassart, G., 1998. The deltaccr5 mutation conferring protection against HIV-1 in Caucasian populations has a single and recent origin in Northeastern Europe. Hum. Mol. Genet. 7, 399–406. Lonergan, M., Harwood, J., 2003. The potential effects of repeated outbreaks of phocine distemper among harbour seals: a response to Harding et al.. Ecol. Lett. 6, 889–898. Markussen, N.H., Have, P., 1992. Phocine distemper virus infection in Harp seals Phoca groenlandica. Mar. Mamm. Sci. 8, 19–26. Matthiopoulos, J., McConnell, B., Duck, C., Fedak, M., 2004. Using satellite telemetry and aerial counts to estimate space use by grey seals around the British Isles. J. Appl. Ecol. 41, 476–491. McClelland, E.E., Penn, D.J., Potts, W.K., 2003. Major histocompatibility complex heterozygote superiority during coinfection. Infect. Immun. 71, 2079–2086. McConnell, B.J., Fedak, M.A., Lovell, P., Hammond, P.S., 1999. Movements and foraging areas of grey seals in the North Sea. J. Appl. Ecol. 36, 573–590. McConnell, B.J., Fedak, M., Matthiopoulos, J., Lovell, P., 2003. Telemetry: Bits, Models, Phones and Dust. Page 14. 15th Biennial Conference on the Biology of Marine Mammals. Society for Marine Mammalogy, Greensboro, North Carolina. McIlhatton, M.A., Curran, M.D., Rima, B.K., 1997. Nucleotide-sequence analysis of the large (L) genes of phocine distemper virus and canine distemper virus (corrected sequence). J. Gen. Virol. 78, 571–576. Pt 3. Osterhaus, A., Vedder, E.J., 1988. Identification of virus causing recent seal deaths. Nature, (London) 335, 20. Osterhaus, A., Groen, J., Niesters, H., Van de Bildt, M., Martina, B., Vedder, L., Vos, J., Egmond, H., Sidi, B.A., Barham, M.E.O., 1997. Morbillivirus in monk seal mass mortality. Nature, (London) 388, 838–839. Parisien, J.P., Lau, J.F., Horvath, C.M., 2002. STAT2 acts as a host range determinant for species-specific paramyxovirus interferon antagonism and simian virus 5 replication. J. Virol. 76, 6435–6441. Parry, M. 2000. Assessment of potential effects and adaptation for climate change in Europe. The Europe Acacia Project, Jackson
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
Environmental Institute, University of East Anglia, Norwich, UK. Paterson, S., Wilson, K., Pemberton, J.M., 1998. Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Proc. Nat. Acad. Sci. 95, 3714–3719. Pauli, B., Terhune, J., 1987. Meteorological influences on harbour seal haul out. Aquat. Mamm. 13, 114–118. Pomeroy, P.P., Hammond, J.A., Hall, A.J., Lonergan, M., Duck, C.D., Smith, V.J., Thompson, H., 2005. Morbillivirus neutralizing antibodies in Scottish grey seals: assessing the effects of the 1988 and 2002 PDV epizootics. Mar. Ecol. Prog. Ser. 287, 241–250. Reijnders, P.J.H., 1980. Organochlorine and heavy metal residues in harbour seals from the Wadden sea and their possible effects on reproduction. Neth. J. Sea Res. 14, 30–65. Reijnders, P.J.H., Aguilar, A., 2002. Pollution and marine mammals. In: Perrin, W., Wursig, B., Thewissen, J. (Eds.), Encyclopedia of Marine Mammals. Academic Press, San Diego, pp. 948–956. Reijnders, P.J.H., Ries, E.H., Tougaard, S., Norgaard, N., Heidemann, G., Schwarz, J., Vareschi, E., Traut, I.M., 1997. Population development of harbour seals Phoca vitulina in the Wadden Sea after the 1988 virus epizootic. J. Sea Res. 38, 161–168. Ries, E.H., Hiby, L.R., Reijnders, P.J.H., 1998. Maximum likelihood population size estimation of harbour seals in the Dutch Wadden Sea based on a mark-recapture experiment. J. Appl. Ecol. 35, 332–339. Ries, E.H., Traut, I.M., Brinkman, A.G., Reijnders, P.J.H., 1999. Net dispersal of harbour seals within the Wadden Sea before and after the 1988 epizootic. J. Sea Res. 41, 233–244. Ross, P.S., DeSwart, R.L., Reijnders, P.J.H., Van Loveren, H., Vos, J.G., Osterhaus, A.D.M.E., 1995. Contaminant-related suppression of delayed-type hypersensitivity and antibody responses in harbor seals fed herring from the Baltic sea. Environ. Health Perspect. 103, 162–167. Samson, M., Libert, F., Doranz, B.J., Rucker, J., Liesnard, C., Farber, C.M., Saragosti, S., Lapoumeroulie, C., Cognaux, J., Forceille, C., Muyldermans, G., Verhofstede, C., Burtonboy, G., Georges, M., Imai, T., Rana, S., Yi, Y., Smyth, R.J., Collman, R.G., Doms, R.W., Vassart, G., Parmentier, M., 1996. Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature (London) 382, 722–725. Schumacher, U., Horny, H.-P., Heidemann, G., Schultz, W., Welsch, U., 1990. Histopathological findings in Harbour seals (Phoca vitulina) found dead on the German North Sea Coast. J. Comp. Pathol. 102, 299–309. Stuen, S., Have, P., Osterhaus, A.D.M.E., Arnemo, J.M., Moustgaard, A., 1994. Serological investigation of virus infections in harp seals Phoca groenlandica and hooded seals Cystophora cristata. Vet. Rec. 134, 502–503. Swinton, J., Harwood, J., Grenfell, B., Gilligan, C., 1998. Persistence thresholds for phocine distemper virus infection in harbour seal (Phoca vitulina) metapopulations. J. Anim. Ecol. 67, 54–68. Swinton, J., Gilligan, C.A., Harwood, J., Hall, A.J., 1999. Scaling of phocine distemper virus transmission with harbour seal community size. Ecologie 30, 231–240. Tatsuo, H., Ono, N., Tanaka, K., Yanagi, Y., 2000. SLAM (CDw150) is a cellular receptor for measles virus. Nature (London) 406, 893–897. Tatsuo, H., Ono, N., Yanagi, Y., 2001. Morbilliviruses use signaling lymphocyte activation molecules (CD150) as cellular receptors. J. Virol. 75, 5842–5850. Thompson, P.M., 1989. Seasonal changes in the distribution and composition of common seal (Phoca vitulina) haul-out groups. J. Zool. Lond. 217, 281–294.
B I O L O G I C A L C O N S E RVAT I O N
Thompson, P.M., Miller, D., 1992. Phocine distemper virus outbreak in the Moray Firth common seal population: an estimate of mortality. Sci. Tot. Environ. 115, 57–65. Thompson, P.M., Kovacs, K.M., McConnell, B.J., 1994. Natal dispersal of harbour seals (Phoca vitulina) from breeding sites in Orkney, Scotland. J. Zool. Lond. 234, 668–673. Thompson, P.M., Van Parijs, S., Kovacs, K.M., 2001. Local declines in the abundance of harbour seals: implications for the designation and monitoring of protected areas. J Appl. Ecol. 38, 117–125.
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
229
Thompson, P.M., Thompson, H., Hall, A.J., 2002. Prevalence of morbillivirus antibodies in Scottish harbour seals. Vet. Rec. 151, 609–610. Thompson, D., Lonergan, M.E., Duck, C., 2005. Population dynamics of harbour seals (Phoca vitulina) in England: growth and catastrophic declines. J Appl. Ecol. 42, 638–648. Watts, P., 1996. The diel hauling out cycle of harbour seals in an open marine environment: correlations and constraints. J. Zool. Lond. 240, 175–200.
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/biocon
Phocine distemper virus in the North and European Seas – Data and models, nature and nurture Ailsa J. Halla,*, Paul D. Jepsonb, Simon J. Goodmanc, Tero Ha¨rko¨nend a
Sea Mammal Research Unit, Gatty Marine Laboratory, University of St Andrews, St Andrews, Fife KY16 8LB, UK Institute of Zoology, Zoological Society of London, Regents Park, London NW1 4RY, UK c Institute of Integrative and Comparative Biology, Faculty of Biology, University of Leeds, Leeds LS2 9JT, UK d Swedish Museum of Natural History, Box 50007, S-10405 Stockholm, Sweden b
A R T I C L E I N F O
A B S T R A C T
Available online 5 June 2006
Two outbreaks of phocine distemper have severely affected harbour seal (Phoca vitulina) populations in European and UK waters. The first occurred in 1988 when the causative
Keywords:
virus was identified as a new member of the genus morbillivirus. The second outbreak in
Harbour seal
2002 was first detected on the same Danish Island of Anholt and involved similar popula-
Epidemic
tions and geographical locations. However, despite the obvious similarities between the
Mathematical modelling
epidemics, differences in viral transmission and case mortality were found. Harbour seals
Disease
are highly susceptible to infection while sympatric grey seals (Halichoerus grypus) are resis-
Infection
tant but could be important asymptomatic carriers of the disease. Arctic phocid seals
PDV
remain the most likely source of the virus and grey seals could be the link between these primary hosts and the harbour seal populations further south. Future epidemiological models should therefore consider including multiple host species. The future conservation and management of harbour seal populations vulnerable to PDV relies on the ability to accurately predict the long-term impact on population abundance and distribution. Although knowledge about the behaviour and pathogenesis of the virus has increased substantially and data on host movements and contact rates are accumulating, studies into the determinants of the host range have lagged behind. The development of more realistic epidemiological models should be combined with studies into the factors controlling species and individual susceptibility. Assessing the risk of infection to endangered but currently unexposed potential host species (such as the Hawaiian monk seal, Monachus schauinslandi) is essential for guiding potential conservation management options, such as vaccination. Ó 2006 Elsevier Ltd. All rights reserved.
1.
Introduction
Phocine distemper virus (PDV) emerged as a devastating disease among harbour seals in Northern European and UK coastal waters in 1988 (Kennedy et al., 1988; Osterhaus and Vedder, 1988), causing catastrophic declines in many popula-
tions (Dietz et al., 1989; Hall et al., 1992a; Hall, 1995; Ha¨rko¨nen and Heide-Jørgensen, 1990; Heide-Jørgensen and Ha¨rko¨nen, 1992a). Over the six-month period beginning in April, more than 18,000 carcasses washed up along the shores of Europe and the UK (Fig. 1a, Dietz et al., 1989; Heide-Jørgensen et al., 1992b). PDV is a member of the genus morbillivirus within
* Corresponding author: Tel.: +44 1334 462630; fax: +44 1334 462632. E-mail addresses: [email protected] (A.J. Hall), [email protected] (P.D. Jepson), [email protected] (S.J. Goodman), [email protected] (T. Ha¨rko¨nen). 0006-3207/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2006.04.008
222
B I O L O G I C A L C O N S E RVAT I O N
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
Fig. 1 – Maps showing the temporal and spatial spread of (a) the 1988 epidemic and (b) the 2002 epidemic from Anholt in the Kattegat to UK and Irish waters. The dotted line indicates that the disease did not reach epidemic proportions in Scotland or Northern Ireland, despite PDV seal deaths being found in many regions (shown by the black circles).
the Paramyxoviridae family that causes a severe respiratory and systemic infection in its host and has a high case fatality rate (Harder et al., 1990). In 2002 the disease re-emerged causing a second major outbreak (Jensen et al., 2002), affecting largely the same populations over a similar geographical area (Fig. 1b), with roughly the same epidemic duration and population impacts (more adult males than other sex-age groups were infected) (Ha¨rko¨nen et al., 2006). However, there were differences between the timing of the two epidemics and wide geographical variations in mortality rates. Comparing the two outbreaks may therefore provide important clues as to the nature, origin and enduring impact of the virus.
Information about the PDV virus itself has increased greatly over the last 17 years. The genes encoding for many of the major viral proteins have been sequenced (Curran et al., 1992; Curran et al., 1990; Curran and Rima, 1992; McIlhatton et al., 1997). Knowledge of the pathogenesis and aetiology of the disease and its potential sequelae has been obtained from detailed pathological studies of affected animals (Baker, 1992; Kennedy et al., 1989; Schumacher et al., 1990). However, information about the movements, distribution and population dynamics of its harbour seal host on a wide geographical scale have only recently been reported (Brasseur and Fedak, 2003; Ha¨rko¨nen et al., 1999; Ries et al., 1999).
B I O L O G I C A L C O N S E RVAT I O N
In 1988, the size of many of the harbour seal populations first affected was unknown, thus population counts pre and post-epidemic comparison were only available in a few cases (Heide-Jørgensen and Ha¨rko¨nen, 1988; Heide-Jørgensen et al., 1992c; Thompson et al., 2005; Thompson and Miller, 1992). Indeed, the number of carcasses that washed ashore at some sites exceeded the then current regional population estimate (Dietz et al., 1989). Carcass counts were therefore not a reliable method for estimating mortality from PDV. In areas where harbour seal carcasses were washed onto amenity beaches or where haul out sites were regularly monitored, remains for scientific study were recovered (Hall et al., 1992b; Heide-Jørgensen and Ha¨rko¨nen, 1992a). Although these samples were used to estimate sex and age-related mortality, they could be biased depending on the location and season. Thus the impact of the outbreak could only be determined in those areas where seal counts were available from boat or aerial surveys (Heide-Jørgensen et al., 1992b). With long-term monitoring of harbour seal populations established in 1988 (Ha¨rko¨nen et al., 2002; Ries et al., 1998; Thompson et al., 2005; Thompson et al., 2001), the impact of the PDV outbreak in 2002 could be estimated more accurately (Ha¨rko¨nen et al., 2006). Using a simple compartmental mathematical model, Grenfell et al. (1992) suggested that the viral transmission rate (the transmission coefficient, b) during the 1988 epidemic was probably sufficient for the infection to die out in the Northern European harbour seal populations following the first outbreak. With herd immunity conferred by the acquired immune response to the virus, which for morbilliviruses is usually life-long, they suggested a second outbreak following reintroduction of the virus was unlikely to cause an outbreak on the same scale for at least 10 years. In reality the inter-epidemic period was 14 years. There is now sufficient abundance and distribution data over time to model the dynamics of the virus and its epidemiology at different temporal and spatial scales (Harding et al., 2002; Ha¨rko¨nen, T., personal communication; Lonergan, M., personal communication; Swinton et al., 1999; Swinton et al., 1998). For example, recent studies using mathematical models to focus on the long-term population consequences and risk of quasi-extinction (i.e. the risk of a serious decline in the size of a population) for harbour seals (Harding et al., 2002; Harding et al., 2003; Lonergan and Harwood, 2003) have established that populations with low or variable rates of increase are very vulnerable to serious decline following future PDV outbreaks. However, estimating the risk of quasi-extinction for rapidly growing populations is more difficult (Ha¨rko¨nen et al., 2006). Assumptions regarding levels of immunity, the variance in the population growth and the action of density dependence all have substantial effects on quasi-extinction probabilities in this case (Lonergan and Harwood, 2003). Some of the European harbour seal populations experienced very high population growth rates following the first PDV epidemic; for example the Wadden sea population was increasing at about 9% per annum before the 1988 epidemic, but at 13% between 1989 and 2000 (Ha¨rko¨nen, 2003; Reijnders et al., 1997). However, Harding et al. (2003) concluded that the cumulative effect of recurrent epidemics with mortality rates similar to those seen in 1988 and 2002, even for popula-
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
223
tions with relatively high growth rates between outbreaks, may limit the size of those populations. Despite the progress in monitoring and epidemiological modelling, fundamental information on host movements to estimate contact rate between infective and susceptible hosts is still lacking. PDV is probably endemic in the Arctic phocid seals, such as the harp (Phoca groenlandica) and hooded seals (Cystophora cristata). Serological surveys have found antibody prevalence rates of over 90% for some populations of these species (Duignan et al., 1997; Markussen and Have, 1992; Stuen et al., 1994) although age-specific prevalence data are not available. The sympatric and widely distributed grey seal is potentially a key carrier of infection both between populations and perhaps species (Hammond et al., 2005; Pomeroy et al., 2005) and may be the link between PDV’s putative Arctic primary hosts (Ha¨rko¨nen et al., 2006) and the more southerly populations of harbour seals. Harbour seals are a listed species in the European Habitats Directive (Directive 92/43/EEC on the conservation of natural habitats and of wild flora and fauna) and signatory States are required to set up Special Areas of Conservation (SAC) that are monitored and protected such that a favourable conservation status for the species is ensured. Estimating the impact that PDV may have on harbour seal population dynamics is part of this obligation. But what ecological, epidemiological and individual factors influence the long-term risks of recurrent epidemics? What data are still required to realistically model the dynamics of phocine distemper? In this paper we explore these questions and discuss the potential conservation implications both for the European harbour seal and for endangered seal species not currently exposed to the virus, such as the Hawaiian monk seal.
2. Ecological and epidemiological factors affecting the risk of recurrent epidemics Serological surveys (measuring levels of morbillivirus specific antibodies in the blood of surviving seals) are a key method for determining the proportion of exposed and immune individuals within a population. Individuals sampled from the Scottish harbour seal populations at the start of the outbreak in 2002 suggested that between only 3% and 9% had protective titres (compared to over 70% in 1989) and that the disease could potentially spread rapidly in Scotland once introduced (Thompson et al., 2002). However, the proportion of apparently seronegative individuals that had actually been exposed and were thus immune is not known. There was no significant outbreak of PDV in Scotland in 2002 (Ha¨rko¨nen et al., 2006) and even in 1988 only the Moray Firth population was obviously affected (Thompson and Miller, 1992). Relatively high seal mortality was reported in Orkney based on carcass reports in 1988 (Hall et al., 1992a), but it is thought this reflects mortality in grey seals, particularly pups, as only 151/601 carcasses were confirmed to be harbour seals (SMRU unpublished). It remains puzzling that the epidemic did not spread through the Scottish harbour seal populations in 2002. There were clearly sufficient susceptible individuals within the population and Scotland has approximately 86% of the UK’s
224
B I O L O G I C A L C O N S E RVAT I O N
36,000 harbour seals (SMRU unpublished). The restricted movements of infected individuals, either into the population from elsewhere or within sub-populations, are a potential explanatory factor. One of the central parameters in modelling the spread of an epidemic is R0, defined as the average or expected number of secondary cases produced by each primary infectious individual. If R0 is greater than one then an infectious disease is likely to spread within the population (Grenfell and Dobson, 1995). The size of R0 is affected by contact rates within the population. Estimates of contact rates (from combining a simple compartmental epidemic model with serological data) for Scotland were approximately 1.5– 1.9 for 1988 and 1.2–1.3 for 2002 (Lonergan, M., personal communication). Although these rates were significantly lower in the Scottish populations than in the southeastern English population in 1988, this was not the case in 2002 with similar estimates produced for contact rates in both areas. In addition while mortality among UK harbour seals was highest in southeastern England during both outbreaks, it was significantly lower in 2002 than in 1988 (53% in 1988 and 22% in 2002; Thompson et al., 2005). It therefore appears that although disease transmission was similar throughout the UK in 2002, case mortality from PDV was highly variable among sub-populations.
3.
Movement and dispersal
Information on the movements of seals is necessary, both within and between populations, for the accurate estimation of R0. Some data on harbour seal movements has been obtained using flipper tagging (Thompson et al., 1994), freeze branding (Ha¨rko¨nen et al., 1999), radio-telemetry (Ries et al., 1998; Thompson, 1989) and satellite relay dataloggers (SRDLs) (Brasseur and Fedak, 2003). Whilst many harbour seals remain in well-defined foraging areas and haulout at the same locations, some do make long movements away from the coast, venturing to new haulout sites (Brasseur and Fedak, 2003). The frequency of this behaviour appears to vary by location. For example, 45/45 harbour seals fitted with SRDLs in the Wash (east England) and St Andrews Bay (east Scotland) remained at these haulout sites, whereas 1/15 tagged in Orkney and Shetland and 2/5 tagged in the Moray Firth moved to distant sites (Sharples, R. and Hammond, P.S. personal communication). There is currently a major effort to obtain movement data for all the European populations so that a collective spatially explicit model can be constructed (Ha¨rko¨nen, T., personal communication). Grey seals are probably asymptomatic carriers of PDV (Pomeroy et al., 2005; Hammond et al., 2005) but more information on the interaction between harbour seals and sympatric grey seals is needed, especially at mixed haulout sites. A large body of data now exists on the large-scale movements and foraging behaviour of grey seals in the North Sea (Matthiopoulos et al., 2004; McConnell et al., 1999). Again most foraging trips return to the same haulout but relocation to a distant haulout site is more frequent than in harbour seals. However, the movements of both harbour and grey seals from the same haulout sites have not been monitored simultaneously.
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
Goodhart (1988) suggested that PDV is endemic in harp seals and was introduced to the harbour seals following the massive 1987 harp seal invasion into the southern Norwegian Sea. However, there are some discrepancies in the evidence to support this theory. The last harp seal was seen in Norwegian waters in May 1987 (Markussen and Have, 1992), almost one year before the first outbreak and none were seen around Anholt (Denmark) where both outbreaks were first detected. In addition, no similar invasion occurred in 2001. An alternative simple explanation is that grey seals, that do haulout on Anholt (Ha¨rko¨nen et al., in press), could have been the carrier of PDV between Arctic seals (that regularly forage in the northern North Sea) (Folkow et al., 1996) and harbour seals in both outbreaks. However, it is a surprise that, if grey seals are the source, the second epidemic did not start at other mixed haulouts, such as in the Wadden Sea. Perhaps the clue here is in the regularity and stability of an individual’s movements. If grey seals travelling between northern Norway and Danish waters are more likely to come into contact with infected harp seals and susceptible harbour seals, this may account for the epidemic point source being on Anholt rather than elsewhere. Since SRDL tags attached to the fur of the seals are shed during the moult and therefore last a maximum of 12 months, there are no data to test this hypothesis. Whatever the explanation, PDV in UK and other European seals must be considered as a two or three host system, which will add considerably complexity to the mathematical models needed and to the data required for their parameterisation. At the finer spatial and temporal scales there is little understanding of the social interactions that characterize the contact pattern between infected and susceptible seals, both within and between species. This social and behavioural aspect to the modelling of disease outbreaks in humans and domestic species is now receiving more widespread attention (Eubank et al., 2004). The PDV models constructed to date have assumed uniform mixing for the contact process (De Koeijer et al., 1998; Grenfell et al., 1992), but this may be too simplistic. The social or network structure of a population, which is expected to show temporal variations (Ha¨rko¨nen and Harding, 2001), will influence disease dynamics. This structure means that each individual has a finite set of contacts to which they can pass infection, known as a ‘‘mixing network’’ (Keeling and Eames, 2005). The characteristics of the mixing network, and how it differs from random mixing have become important concerns in applied epidemiology. A proposed novel approach to quantifying population network structure in seals uses telemetry devices known as node-tags (McConnell et al., 2003). The tags, deployed on individual seals, would record the proximity of other tagged seals within a specified range. When another tag was encountered its identification would be swapped with its neighbour and stored in memory. In addition to the current encounter occasion, individual encounter histories would also be swapped. The tags would thus accrue histories for those segments of the network with which they have had direct or indirect contact and these data would be relayed ashore through a number ‘portal’ tags within the network. While there are some statistical modelling and technological issues to be addressed, this innovative scheme has the potential to estimate the individual contact rates between and within sympatric
B I O L O G I C A L C O N S E RVAT I O N
species, both on land and at sea, and enable the spread of PDV more accurately estimated. Following the first PDV outbreak there was interest in the influence of global warming. Europe appears to be warming faster than the global average (Crowley, 2000) and projections suggest this may continue to increase (Parry, 2000). The hypothesis proposed was that higher ambient temperatures would increase the time harbour seals spend hauled out on land and increase the probability of viral transmission (Lavigne and Schmitz, 1990). However, observations suggest that harbour seals become heat stressed during warm days, resulting in decreased numbers of animals on land (Harwood and Grenfell, 1990; Pauli and Terhune, 1987; Watts, 1996). Climate change could, nevertheless still affect the spread of PDV through changes in prey availability of the reservoir and target hosts. If Arctic capelin stocks (whose crash in 1987 preempted the southward migration of harp seals) were affected this could bring about considerable seal species overlaps, increasing direct contact between infected and susceptible individuals. In addition, environmental change may cause pathogens to shift to new and unexpected hosts. For example, a recent study in Lake Baikal, where Baikal seals (Phoca sibirica) have suffered recurrent outbreaks of canine distemper (CDV), found two species of molluscs to be infected with CDV, confirmed by RT-PCR and passaged through ferrets resulting in acute respiratory infection (Kondratov et al., 2003). This isolated report raises the possibility of non-mammalian PDV reservoirs.
4.
Individual factors
A number of studies have indicated that host genetic diversity plays an important role in buffering populations against widespread epidemics (Altizer et al., 2003). Loci that could potentially be involved in disease resistance include those that directly mediate the immune response (e.g. major histocompatibility complex (MHC) class I and class II; (McClelland et al., 2003; Paterson et al., 1998)), genes for proteins that regulate the immune response such as cytokines or genes encoding for cell receptors that a virus uses to infect cells (Samson et al., 1996). Theoretical models combining epidemiology and population genetics demonstrate that the selection pressure exerted by repeated epidemics with high mortality can drive the rapid evolution of genetic disease resistance over short evolutionary timescales (Galvani and Slatkin, 2004; Harding et al., 2005). In a model of disease resistance evolution, parameterised specifically for recurrent PDV epidemics in a harbour seal population, Harding et al. (2005) show that a disease resistance allele can be pushed from an initial frequency of 1% to 50% in 120 years (16 generations) with a 15 year epidemic interval (eight epidemics). Indeed, they predict that rapid increases in the resistant allele frequency would be seen after just four outbreaks. Therefore even moderate exposure to PDV in the historical past could have selected for disease resistance in exposed populations. However, some of the assumptions under this model might require further testing. A genetic study of European harbour seal populations using microsatellites (neutral nuclear genetic markers) showed the population to be highly structured, which would allow for the differential distribution of alleles that contribute
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
225
to disease susceptibility (Goodman, 1998). However, the results obtained so far do not support simple explanations for genetic associations with phocine distemper mortality. For example, genetic impoverishment of the more severely affected populations was not supported. Indeed, some populations with high mortality had some of the highest levels of genetic variation in the North Sea (Goodman, 1998). Sequence variation at MHC class I loci also appears to be comparable to other carnivores (Goodman, 1995). Genetic associations with PDV susceptibility are likely to be more subtle and will require further investigation of variation at a population level for the types of candidate genes described above. Such work is already feasible using recently developed genomics tools that can be applied to seals. Serological studies have shown widespread exposure to PDV among UK grey seals in both 1988 and 2002 (Harwood et al., 1989; Pomeroy et al., 2005) but no fatal cases of phocine distemper were found in the UK (Jepson, P., personal communication) and only very few unsubstantiated cases have been reported in Germany and Estonia (Ha¨rko¨nen et al., 2006). The main cause of death from PDV is often secondary bacterial infection due to viral immunosuppression and the virus replicates in the lymphoid organs of the body (Baker and Ross, 1992). A membrane glycoprotein known as signalling lymphocyte activation molecule (SLAM, also known as CD150) was found to be the cellular receptor for measles virus in humans (Tatsuo et al., 2000) and a similar molecule was also found to be a receptor for CDV in dogs and RPV in cattle (Tatsuo et al., 2001). Since the expression of specific cellular receptors is one of the major determinants of the host range for a virus (Tatsuo et al., 2001) the first stage in identifying the PDV host range would be to determine the presence of SLAMs in seals (and cetaceans). Although Tatsuo et al. (2001) predict most, if not all, morbilliviruses use SLAMs this needs to be confirmed. Further investigations into the genes encoding these receptors and the frequency of the alleles in different harbour seal populations links back to the potential importance of genetic variability in determining host resistance. For example, in humans population variation in mutant alleles of the gene encoding the chemokine receptor CCR5 provides homozygotes with a strong resistance against infection by HIV; Libert et al. (1998). This is also of particular concern for endangered and threatened species not currently exposed to PDV, such as the Hawaiian monk seal. Although PDV has not yet reached the Pacific Ocean if, or when, it does it is important to know whether this species is at risk of infection. Although PDV was identified as the cause of a mass mortality in the endangered Mediterranean monk seal (Monachus monachus) in 1997 (Osterhaus et al., 1997), phycotoxins from the ingestion of contaminated fish following an algal bloom were also reported as the cause of this die-off (Herna´ndez et al., 1998) and the ultimate cause of mortality remains open to debate (Harwood, 1998). Other mechanisms may govern the host range in morbilliviruses. Alpha/beta interferons (IFN-a/b) are key antiviral cytokines involved in inhibiting viral replication. Exposure of cells to IFN-a/b quickly establishes an antiviral state that blocks cytopathic and degenerative effects (Parisien et al., 2002). Paramyxoviruses can block IFN-a/b signalling, preventing the cell from establishing an antiviral state but this may
226
B I O L O G I C A L C O N S E RVAT I O N
be species specific. For example simian virus 5 (SV5) anatagonizes IFN-a/b in primate cells but not mouse cells. In mouse cells SV5 is unable to block IFN-a/b antiviral responses, which leads to most cells surviving infection and clearing the virus. Indeed, differences in the intracellular signalling protein STAT2 between primates and mice ultimately determine this response. Cell surface interactions are the primary molecular determinants of species specificity for viral infection and identification of these mechanisms will indicate which hosts are vulnerable. Thus understanding variability at the molecular level has direct application to conservation management decisions, particularly those that need to assess the infection risk in currently unexposed species. The potential interactions between PDV and immunosuppressive environmental contaminants as further determinants of the observed mortality patterns within species during both outbreaks have been dealt with extensively elsewhere (DeSwart et al., 1994; Hall et al., 1992b; Reijnders and Aguilar, 2002; Ross et al., 1995). However, increasing evidence, from both in vitro and in vivo studies, suggest there are species differences in the immunosuppressive effects of organochlorine (OC) contaminants, with grey seals being relatively resistant compared to harbour seals. The most compelling evidence for an effect of contaminants on harbour seal immunity was reported following an experiment in captivity. Immune function in a group of harbour seals fed fish with high concentrations of various OC contaminants was compared to a control group (De Swart et al., 1996; Ross et al., 1995). Immunity was found to be depressed in the contaminant fed group, particularly natural killer (NK) cell activity and proliferative lymphocyte responses after stimulation, suggesting an impaired T cell function. These functions are known to be important in the clearance of virus infections (Finberg and Benacerraf, 1981). A recent in vitro study (Hammond et al., 2005) compared the effects of polychlorinated biphenyl (PCB) exposure on innate immunity in harbour and grey seals. Phagocytic activity of harbour seal leukocytes was decreased at exposure levels of 3 and 30 ng ml 1 but there was no effect on grey seal leukocytes. Similarly respiratory burst activity was decreased in harbour seals at the higher exposure level but not in the grey seals. In addition, there was no significant relationship between lactational exposure to PCBs and infection or reduced immunity in grey seal pups born at the Isle of May in the Firth of Forth, Scotland (Hall et al., 1997). Harbour seals in the Wadden Sea experienced some of the highest exposure levels of OC contaminants in Europe (Reijnders, 1980) and it was hypothesised that the 1988 PDV epidemic selected against those seals with the highest contaminant loads. The significantly higher population growth rate following the outbreak (Reijnders et al., 1997) coupled with the reduced levels of contaminants in the surviving population might support this view (Aguilar et al., 2002) although other explanations are equally plausible such as density dependent effects. Interestingly, whilst the levels of OC contaminants in the Wadden Sea harbour seals have decreased by 50–65%, those in the blubber of harbour seals in southeastern England (the Wash) have decreased by less than 10% over the same 14 year period, and the concentrations in the seals that died of PDV in 2002 were significantly
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
higher than the survivors (Hall, unpublished). It therefore remains important to determine how the molecular mechanisms involved in contaminant immunosuppression and susceptibility are related to those determining viral susceptibility.
5.
Conservation and management
PDV remains a threat to the conservation of European harbour seals and more realistic epidemiological models are required to inform conservation management decisions, particularly within the harbour seal SACs. It has been asserted that although ‘‘all models are wrong, some models are useful’’ (Box, 1979). While it is highly unlikely that a future PDV outbreak could be prevented, predicting the impact and spread is important, particularly for the development of contingency plans and carcasses collection strategies. Risk assessment models that also incorporate interactions with anthropogenic factors, such as environmental contaminants, will indicate where efforts to reduce exposures should be directed. Although knowledge about the behaviour and pathogenesis of the virus has increased substantially between outbreaks, studies into the determinants of the host range and individual susceptibility have lagged behind. Yet assessing the risk of infection to threatened or endangered but currently unexposed species is essential to determine the efficacy of practical conservation management options (such as vaccination or relocation). Such measures are costly and logistically difficult to implement and are further reason for the continued refinement of PDV epidemiological models.
Acknowledgements The authors would like to thank Bernie McConnell, John Harwood and Catriona Stephenson for their valuable and constructive comments on this manuscript and the anonymous referees for their very helpful additional suggestions.
R E F E R E N C E S
Aguilar, A., Borrell, A., Reijnders, P.J.H., 2002. Geographical and temporal variation in levels of organochlorine contaminants in marine mammals. Mar. Environ. Res. 53, 425–452. Altizer, S., Harvell, D., Friedle, D., 2003. Rapid evolutionary dynamics and disease threats to biodiversity. TREE 18, 589–596. Baker, J.R., 1992. The pathology of phocine distemper. Sci. Tot. Environ. 115, 1–7. Baker, J.R., Ross, H.M., 1992. The role of bacteria in phocine distemper. Sci. Tot. Environ. 115, 9–14. Box, G.P., 1979. Robustness in the strategy of scientific model building. In: Launer, R.L., Wilkinson, G.N. (Eds.), Statistics. Academic Press, New York. Brasseur, S.M., Fedak, M., 2003. Habitat use of seals in relation to recreation, fisheries and large intra-structural works. Management of North Sea Harbour and Grey Seal Populations. Common Wadden Sea Secretariat, Ecomare, Texel, Netherlands. pp. 27–33. Crowley, T.J., 2000. Causes of climate change over the past 1000 years. Science 289, 270–277.
B I O L O G I C A L C O N S E RVAT I O N
Curran, M.D., Rima, B.K., 1992. The genes encoding the phosphoproteins and matrix proteins of phocine distemper virus. J. Gen. Virol. 73, 1587–1591. Curran, M.D., Oloan, D., Rima, B.K., Kennedy, S., 1990. Nucleotide-sequence analysis of phocine distemper virus reveals its distinctness from canine-distemper virus. Vet. Rec. 127, 430–431. Curran, M.D., Lu, T.J., Rima, B.K., 1992. The fusion protein gene of phocine distemper virus—nucleotide and deduced amino-acid-sequences and a comparison of morbillivirus fusion proteins. Arch. Virol. 126, 159–169. De Koeijer, A., Diekmann, O., Reijnders, P.J.H., 1998. Modelling the spread of phocine distemper virus among harbour seals. Bull. Math. Biol. 60, 585–596. DeSwart, R.L., Ross, P.S., Vedder, L.J., Timmerman, H.H., Heisterkamp, S., Van Loveren, H., Vos, J.G., Reijnders, P.J.H., Osterhaus, A.D.M.E., 1994. Impairment of immune function in harbor seals (Phoca vitulina) feeding on fish from polluted waters. Ambio 23, 155–159. De Swart, R.L., Ross, P.S., Vos, J.G., Osterhaus, A.D., 1996. Impaired immunityin harbour seals (Phoca vitulina) exposed to bioaccumulated environmental contaminants: review of a long-term feeding study. Environ. Health Perspect. 104, 823–828. Dietz, R., Heide-Jørgensen, M-P., Ha¨rko¨nen, T., 1989. Mass deaths of harbor seals (Phoca vitulina) in Europe. Ambio 18, 258–264. Duignan, P.J., Nielsen, O., House, C., Kovacs, K., Duffy, N., Early, G., Sadove, S., St Aubin, D.J., Rima, B.K., Geraci, J.R., 1997. Epizootiology of morbillivirus infection in harp, hooded and ringed seals from the Canadian Arctic and western Atlantic. J. Wild. Dis. 33, 7–19. Eubank, S., Guclu, H., Kumar, V.S., Marathe, M.V., Srinivasan, A., Toroczkai, Z., Wang, N., 2004. Modelling disease outbreaks in realistic urban social networks. Nature (London) 429, 180–184. Finberg, R., Benacerraf, A., 1981. Induction, control and consequences of virus specific cytotoxic T cells. Immunol. Rev. 58, 157–180. Folkow, L.P., Martensson, P-E., Blix, A.S., 1996. Annual distribution of hooded seals (Cystophora cristata) in the Greenland and Norwegian seas. Polar Biol. 16, 179–189. Galvani, A.P., Slatkin, M., 2004. Intense selection in an age-structured population. Proc. Biol. Sci. 271, 171–176. Goodhart, C.B., 1988. Did virus transfer from Harp seals to commons seals? Nature (London) 336, 21. Goodman, S.J. 1995. Molecular population genetics of the European harbour seal (Phoca vitulina) in relation to the 1988 Phocine Distemper Virus epizootic. PhD Thesis, University of Cambridge, Cambridge, UK. Goodman, S.J., 1998. Patterns of extensive genetic differentiation and variation among European harbor seals (Phoca vitulina vitulina) revealed using microsatellite DNA polymorphisms. Mol. Biol. Evol. 15, 104–118. Grenfell, B., Dobson, A., 1995. Ecology of Infectious Diseases in Natural Populations. Cambridge University Press, Cambridge. Grenfell, B.T., Lonergan, M.E., Harwood, J., 1992. Quantitative investigations of the epidemiology of phocine distemper virus (PDV) in European common seal populations. Sci. Tot. Environ. 115, 15–29. Hall, A.J., 1995. Morbilliviruses in marine mammals. Trends Microbiol. 3, 4–9. Hall, A.J., Pomeroy, P., Harwood, J., 1992a. The descriptive epizootiology of phocine distemper in the UK during 1988/89. Sci. Tot. Environ. 115, 31–44. Hall, A.J., Law, R.J., Wells, D.E., Harwood, J., Ross, H.M., Kennedy, S., Allchin, C.R., Campbell, L.A., Pomeroy, P.P., 1992b. Organochlorine levels in common seals (Phoca vitulina) that were victims and survivors of the 1988 phocine distemper epizootic. Sci. Tot. Environ. 115, 145–162.
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
227
Hall, A.J., Pomeroy, P., Green, N., Jones, K., Harwood, J., 1997. Infection, haematology and biochemistry in grey seal pups exposed to chlorinated biphenyls. Mar. Environ. Res. 43, 81–98. Hammond, J.A., Hall, A.J., Dyrynda, L., 2005. Comparison of polychlorinated biphenyl (PCB) induced effects on innate immune functions in harbour and grey seals. Aquat. Toxicol. 74, 126–138. Hammond, J.A., Pomeroy, P., Hall, A.J., Smith, V.J., 2005. Identification and real-time PCR quantification of phocine distemper virus from two colonies of Scottish grey seals in 2002. J. Gen. Virol. 86, 2563–2567. Harder, T., Willhaus, T., Frey, H-R., Liess, B., 1990. Morbillivirus infection of seals during the 1988 epidemic in the Bay of Heligoland: III Transmission studies of cell culture-propogated phocine distemper virus in harbour seals and a grey seal: clinical, virological and serological results. J. Vet. Med. B 37, 641–650. Harding, K.C., Ha¨rko¨nen, T., Caswell, H., 2002. The 2002 European seal plague: epidemiology and population consequences. Ecol. Lett. 5, 727–732. Harding, K.C., Ha¨rko¨nen, T., Pineda, J., 2003. Estimating quasi-extinction risk of European harbour seals: reply to Lonergan and Harwood 2003. Ecol. Lett. 6, 894–897. Harding, K.C., Hansen, B., Goodman, S., 2005. Acquired immunity and stochasticity in epidemic intervals impede the evolution of host disease resistance. Am. Nat. 166, 722–730. Ha¨rko¨nen, T., 2003. Development of populations of harbour seals and grey seals in the Wadden Sea and the North Sea since 1988. Management of North Sea Harbour and Grey Seal Populations. Common Wadden Sea Secretariat, Ecomare, Texel, Netherlands. pp. 13–17. Ha¨rko¨nen, T., Harding, K.C., 2001. Spatial structure of harbour seal populations and the implications thereof. Can. J. Zool. 79, 2115–2127. Ha¨rko¨nen, T., Heide-Jørgensen, M-P., 1990. Short-term effects of the mass dying of Harbour seals in the Kattegat-Skagerrak area during 1988. Z. Saugetierkunde 55, 233–238. Ha¨rko¨nen, T., Harding, K.C., Lunneryd, S.G., 1999. Age- and sex-specific behaviour in harbour seals Phoca vitulina leads to biased estimates of vital population parameters. J. Appl. Ecol. 36, 825–841. Ha¨rko¨nen, T., Harding, K.C., Heide-Jørgensen, M-P., 2002. Rates of increase in age-structured populations: a lesson from the European harbour seals. Can. J. Zool. 80, 1498–1510. Ha¨rko¨nen, T., Dietz, R., Reijnders, P.J.H., Teilmann, J., Thompson, P.M., Harding, K., Hall, A.J., Brasseur, S.M.J.M., Siebert, U., Goodman, S., Jepson, P., Dau Rasmussen, T., 2006. A review of the 1988 and 2002 phocine distemper virus epidemics in European harbour seals. Dis. Aquat. Org. 68, 115–130. Ha¨rko¨nen, T., Brasseur, S.M., Teilmann, J., Vincent, C., Dietz, R., Abt, K., Reijnders, P.J.H., in press. Status of grey seals along mainland Europe from the Southwestern Baltic to France. NAMMCO Scientific Publications. Harwood, J., 1998. What killed the monk seals? Nature, (London) 393, 17–18. Harwood, J., Grenfell, B., 1990. Long-term risks of recurrent seal plagues. Mar. Pollut. Bull. 21, 284–287. Harwood, J., Carter, S.D., Hughes, D.E., Bell, S.C., Baker, J.R., Cornwell, H.J.C., 1989. Seal disease predictions. Nature (London) 339, 670. Heide-Jørgensen, M.-P., Ha¨rko¨nen, T., 1988. Rebuilding seal stocks in the Kattegat-Skagerrak. Mar. Mamm. Sci. 4, 231–246. Heide-Jørgensen, M.P., Ha¨rko¨nen, T., 1992a. Epizootiology of the seal disease in the Eastern North-Sea. J. Appl. Ecol. 29, 99–107. Heide-Jørgensen, M.-P., Ha¨rko¨nen, T., Dietz, R., Thompson, P., 1992b. Retrospective of the 1988 European seal epizootic. Dis. Aquat. Org. 13, 37–62.
228
B I O L O G I C A L C O N S E RVAT I O N
Heide-Jørgensen, M.P., Ha¨rko¨nen, T., Aberg, P., 1992c. Long-term effects of epizootic in harbor seals in the Kattegat-Skagerrak and adjacent areas. Ambio 21, 511–516. Herna´ndez, M., Robinson, I., Aguilar, A., Gonzalea, L.M., Lopez-Jurado, L.F., Reyero, M.I., Cacho, E., Franco, J., Eduardo Costas, V.L-R., 1998. Did algal toxins cause monk seal mortality? Nature, (London) 393, 28–29. Jensen, T., van de Bildt, M., Dietz, H., Andersen, T., Hammer, A., Kuiken, T., Osterhaus, A.D.M.E., 2002. Another phocine distemper outbreak in Europe. Science 297, 209. Keeling, M., Eames, K., 2005. Networks and epidemic models. J. R. Soc. Interf. 2, 295–307. Kennedy, S., Smyth, J.A., McCullough, S.J., Allan, G.M., McNeilly, F., McQuaid, S., 1988. Confirmation of cause of recent seal deaths. Nature (London) 335, 404. Kennedy, S., Smythe, J.A., Cush, P.F., Duignan, P., Platten, M., McCullough, S.J., Allan, G.M., 1989. Histopathologic and immunocytochemical studies of distemper in seals. Vet. Pathol. 26, 97–103. Kondratov, I.G., Denikina, N.N., Belikov, S.I., Durymanova, A.A., Ustinova, E.N., Shestopalov, A.M., 2003. Mollusks as a natural reservoir of morbilliviruses. Doklady Biol. Sci. 389, 154–156. Lavigne, D.M., Schmitz, O.J., 1990. Global warming and increasing population densities: a prescription for seal plagues. Mar. Pollut. Bull. 21, 280–284. Libert, F., Cochaux, F.P., Beckman, G., Samson, M., Aksenova, M., Cao, A., Czeizel, A., Claustres, M., de la Rua, C., Ferrari, M., Ferrec, C., Glover, G., Grinde, B., Guran, S., Kucinskas, V., Lavinha, J., Mercier, B., Ogur, G., Peltonen, L., Rosatelli, C., Schwartz, M., Spitsyn, V., Timar, L., Beckman, L., Parmentier, M., Vassart, G., 1998. The deltaccr5 mutation conferring protection against HIV-1 in Caucasian populations has a single and recent origin in Northeastern Europe. Hum. Mol. Genet. 7, 399–406. Lonergan, M., Harwood, J., 2003. The potential effects of repeated outbreaks of phocine distemper among harbour seals: a response to Harding et al.. Ecol. Lett. 6, 889–898. Markussen, N.H., Have, P., 1992. Phocine distemper virus infection in Harp seals Phoca groenlandica. Mar. Mamm. Sci. 8, 19–26. Matthiopoulos, J., McConnell, B., Duck, C., Fedak, M., 2004. Using satellite telemetry and aerial counts to estimate space use by grey seals around the British Isles. J. Appl. Ecol. 41, 476–491. McClelland, E.E., Penn, D.J., Potts, W.K., 2003. Major histocompatibility complex heterozygote superiority during coinfection. Infect. Immun. 71, 2079–2086. McConnell, B.J., Fedak, M.A., Lovell, P., Hammond, P.S., 1999. Movements and foraging areas of grey seals in the North Sea. J. Appl. Ecol. 36, 573–590. McConnell, B.J., Fedak, M., Matthiopoulos, J., Lovell, P., 2003. Telemetry: Bits, Models, Phones and Dust. Page 14. 15th Biennial Conference on the Biology of Marine Mammals. Society for Marine Mammalogy, Greensboro, North Carolina. McIlhatton, M.A., Curran, M.D., Rima, B.K., 1997. Nucleotide-sequence analysis of the large (L) genes of phocine distemper virus and canine distemper virus (corrected sequence). J. Gen. Virol. 78, 571–576. Pt 3. Osterhaus, A., Vedder, E.J., 1988. Identification of virus causing recent seal deaths. Nature, (London) 335, 20. Osterhaus, A., Groen, J., Niesters, H., Van de Bildt, M., Martina, B., Vedder, L., Vos, J., Egmond, H., Sidi, B.A., Barham, M.E.O., 1997. Morbillivirus in monk seal mass mortality. Nature, (London) 388, 838–839. Parisien, J.P., Lau, J.F., Horvath, C.M., 2002. STAT2 acts as a host range determinant for species-specific paramyxovirus interferon antagonism and simian virus 5 replication. J. Virol. 76, 6435–6441. Parry, M. 2000. Assessment of potential effects and adaptation for climate change in Europe. The Europe Acacia Project, Jackson
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
Environmental Institute, University of East Anglia, Norwich, UK. Paterson, S., Wilson, K., Pemberton, J.M., 1998. Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Proc. Nat. Acad. Sci. 95, 3714–3719. Pauli, B., Terhune, J., 1987. Meteorological influences on harbour seal haul out. Aquat. Mamm. 13, 114–118. Pomeroy, P.P., Hammond, J.A., Hall, A.J., Lonergan, M., Duck, C.D., Smith, V.J., Thompson, H., 2005. Morbillivirus neutralizing antibodies in Scottish grey seals: assessing the effects of the 1988 and 2002 PDV epizootics. Mar. Ecol. Prog. Ser. 287, 241–250. Reijnders, P.J.H., 1980. Organochlorine and heavy metal residues in harbour seals from the Wadden sea and their possible effects on reproduction. Neth. J. Sea Res. 14, 30–65. Reijnders, P.J.H., Aguilar, A., 2002. Pollution and marine mammals. In: Perrin, W., Wursig, B., Thewissen, J. (Eds.), Encyclopedia of Marine Mammals. Academic Press, San Diego, pp. 948–956. Reijnders, P.J.H., Ries, E.H., Tougaard, S., Norgaard, N., Heidemann, G., Schwarz, J., Vareschi, E., Traut, I.M., 1997. Population development of harbour seals Phoca vitulina in the Wadden Sea after the 1988 virus epizootic. J. Sea Res. 38, 161–168. Ries, E.H., Hiby, L.R., Reijnders, P.J.H., 1998. Maximum likelihood population size estimation of harbour seals in the Dutch Wadden Sea based on a mark-recapture experiment. J. Appl. Ecol. 35, 332–339. Ries, E.H., Traut, I.M., Brinkman, A.G., Reijnders, P.J.H., 1999. Net dispersal of harbour seals within the Wadden Sea before and after the 1988 epizootic. J. Sea Res. 41, 233–244. Ross, P.S., DeSwart, R.L., Reijnders, P.J.H., Van Loveren, H., Vos, J.G., Osterhaus, A.D.M.E., 1995. Contaminant-related suppression of delayed-type hypersensitivity and antibody responses in harbor seals fed herring from the Baltic sea. Environ. Health Perspect. 103, 162–167. Samson, M., Libert, F., Doranz, B.J., Rucker, J., Liesnard, C., Farber, C.M., Saragosti, S., Lapoumeroulie, C., Cognaux, J., Forceille, C., Muyldermans, G., Verhofstede, C., Burtonboy, G., Georges, M., Imai, T., Rana, S., Yi, Y., Smyth, R.J., Collman, R.G., Doms, R.W., Vassart, G., Parmentier, M., 1996. Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature (London) 382, 722–725. Schumacher, U., Horny, H.-P., Heidemann, G., Schultz, W., Welsch, U., 1990. Histopathological findings in Harbour seals (Phoca vitulina) found dead on the German North Sea Coast. J. Comp. Pathol. 102, 299–309. Stuen, S., Have, P., Osterhaus, A.D.M.E., Arnemo, J.M., Moustgaard, A., 1994. Serological investigation of virus infections in harp seals Phoca groenlandica and hooded seals Cystophora cristata. Vet. Rec. 134, 502–503. Swinton, J., Harwood, J., Grenfell, B., Gilligan, C., 1998. Persistence thresholds for phocine distemper virus infection in harbour seal (Phoca vitulina) metapopulations. J. Anim. Ecol. 67, 54–68. Swinton, J., Gilligan, C.A., Harwood, J., Hall, A.J., 1999. Scaling of phocine distemper virus transmission with harbour seal community size. Ecologie 30, 231–240. Tatsuo, H., Ono, N., Tanaka, K., Yanagi, Y., 2000. SLAM (CDw150) is a cellular receptor for measles virus. Nature (London) 406, 893–897. Tatsuo, H., Ono, N., Yanagi, Y., 2001. Morbilliviruses use signaling lymphocyte activation molecules (CD150) as cellular receptors. J. Virol. 75, 5842–5850. Thompson, P.M., 1989. Seasonal changes in the distribution and composition of common seal (Phoca vitulina) haul-out groups. J. Zool. Lond. 217, 281–294.
B I O L O G I C A L C O N S E RVAT I O N
Thompson, P.M., Miller, D., 1992. Phocine distemper virus outbreak in the Moray Firth common seal population: an estimate of mortality. Sci. Tot. Environ. 115, 57–65. Thompson, P.M., Kovacs, K.M., McConnell, B.J., 1994. Natal dispersal of harbour seals (Phoca vitulina) from breeding sites in Orkney, Scotland. J. Zool. Lond. 234, 668–673. Thompson, P.M., Van Parijs, S., Kovacs, K.M., 2001. Local declines in the abundance of harbour seals: implications for the designation and monitoring of protected areas. J Appl. Ecol. 38, 117–125.
1 3 1 ( 2 0 0 6 ) 2 2 1 –2 2 9
229
Thompson, P.M., Thompson, H., Hall, A.J., 2002. Prevalence of morbillivirus antibodies in Scottish harbour seals. Vet. Rec. 151, 609–610. Thompson, D., Lonergan, M.E., Duck, C., 2005. Population dynamics of harbour seals (Phoca vitulina) in England: growth and catastrophic declines. J Appl. Ecol. 42, 638–648. Watts, P., 1996. The diel hauling out cycle of harbour seals in an open marine environment: correlations and constraints. J. Zool. Lond. 240, 175–200.